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The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival

Drew Bonkowski, Vladimir Katyshev, Roumen D Balabanov and 2 more

Fluids and Barriers of the CNS · 2011 · Review

doi:10.1186/2045-8118-8-8

Abstract

The French scientist Charles Benjamin Rouget identified the pericyte nearly 140 years ago. Since that time the role of the pericyte in vascular function has been difficult to elucidate. It was not until the development of techniques to isolate and culture pericytes that scientists have begun to understand the true impact of this unique cell in the maintenance of tissue homeostasis. In the brain the pericyte is an integral cellular component of the blood-brain barrier and, together with other cells of the neurovascular unit (endothelial cells, astrocytes and neurons) the pericyte makes fine-tuned regulatory adjustments and adaptations to promote tissue survival. These regulatory changes involve trans-cellular communication networks between cells. In this review we consider evidence for cell-to-cell crosstalk between pericytes and astrocytes during development and in adult brain.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

The blood-brain barrier (BBB) regulates the passage of nutrients, essential components, proteins, chemical substances and microscopic organisms between the bloodstream and the parenchymal tissue. The anatomical constituents of the BBB are the endothelial cells (EC), pericytes, and basal lamina (matrix proteins) that with astrocytes, neurons, and possibly other glial cells, comprise the neurovascular unit. Together, the cells of the neurovascular unit adapt to environmental changes and make fine-tuned regulatory decisions that maintain homeostasis and promote tissue survival. Nowhere is such tight regulation more important than in the brain where bioenergetic and metabolic homeostasis is integral for neuronal survival. Dysregulation at the neurovascular level is linked to many common human CNS pathologies, making the unit a potential target for therapeutic intervention.

The role of the CNS pericyte in the neurovascular unit is still unclear although with improved culturing techniques and the use of genetically engineered animals it has become increasingly clear that pericytes are integral to BBB function. It is known that pericytes are highly complex regulatory cells that communicate with ECs and other cells of the neurovascular unit such as neurons by direct physical contact and through autocrine and paracrine signaling pathways. However, while there is abundant indirect evidence there is little direct evidence of pericyte-astrocyte communication. In this review we will summarize what is known about pericyte-astrocyte transcellular communication. We will discuss vascular development, BBB function and regulation of the neurovascular unit. The potential role of pericyte-astrocyte crosstalk in development of disease pathology will also be covered.

1. Pericytes

Pericytes were described over 100 years ago in 1873 by the French scientist Charles-Marie Benjamin Rouget and dubbed the Rouget cell. The Rouget cell was renamed in the early 1900s to reflect its anatomical location with in the microvasculature abluminal to the EC and luminal to parenchymal cells (reviewed in). In the brain, pericytes are located in pre-capillary arterioles, capillaries and post capillary venules. They synthesize and deposit elements of the basal lamina and are totally surrounded by this vascular compartment. Pericytes are local regulatory cells that are important for the maintenance of vascular homeostasis and hemostasis, and are a source of adult pluripotent stem cells. Pericytes are important cellular constituents of the BBB and actively communicate with other cells of the neurovascular unit such as EC, astrocytes, and neurons. While the communication networks involving pericytes and endothelial cells have been considered in a number of publications, less is known of the cell-to-cell communication involving astrocytes.

Since its original discovery there has been much confusion and controversy about the pericyte as reflected by the numerous conflicting publications and definitions found in the literature. The pericyte has been referred to as: a) A contractile cell that surrounds the capillary in a tunic-like fashion. b) A branching contractile cell on the abluminal wall of a capillary. c) A peculiar elongated, contractile cell wrapped around pre-capillary arterioles 'outside' the basement membrane. d) A relatively undifferentiated connective tissue cell in the capillaries or other small blood vessels also called the adventitial cell. e) A smooth muscle/pericyte or smooth muscle cell of the capillaries. f) A broad flat cell with slender projections that wraps around the capillaries. g) A mesenchymal stem-like cell, associated with the walls of small blood vessels. As a relatively undifferentiated cell, it serves to support these vessels, but it can differentiate into a fibroblast, smooth muscle cell, or macrophage as well other cell populations if required. h) A pluripotent or pericyte progenitor cell.

In the mature CNS capillary, the pericyte is located between the EC and parenchymal astrocytes and neurons and is surrounded by the basal lamina. Pericytes have a prominent round nucleus that clearly differs in shape from the elongated cigar shaped nucleus of the EC. The pericyte extends long processes that extend over the vessel wall. The morphological pattern of projections appears to be somewhat heterogeneous. Pericyte projections can extend around the capillary as originally described by Rouget. The classic wrapping pattern is also somewhat heterogeneous. The most common association of the pericyte with the capillary is one in which the pericyte processes are large and broad and span a continuous surface of the vessel. Alternatively these processes may form finger-like projections that are more confined and ensheath a more finite portion of the vessel surface. A third pattern of pericyte orientation in the microvessel involves a retraction of projections with protrusion of the cells away from the capillaries this represents a migrating pericyte. Pericytes may also extend along the axis of the capillary. It is unclear whether morphological differences in pericyte coverage represent changes in pericyte function. It is clear however that pericytes can migrate away from the capillary surface during angiogenesis, in response to stress stimuli and possibly under other conditions. In normal capillaries the wrapping pattern predominates but under pathological conditions the migrating patterns increase and are associated with upregulation of cell surface proteases.

The CNS pericyte is surrounded by the basal lamina on all sides. During development and during angiogenesis the pericyte, assisted by nearby astrocytes discussed below, deposits basal lamina components. Even extended pericyte projections, observed using electron microscopy, have a thin layer of basal lamina. The basal lamina has been shown to become thicker or thinner in response to stress stimuli. Changes in the basal lamina can be directly associated with pericyte expression of proteases and ultimate migration from its vascular location.

The intact basal lamina may provide anchoring and structural integrity to the capillary but it may also be involved in regulation of pericyte function and differentiation. It seems intuitive that there must be a reason why the pericyte is surrounded by laminal proteins. Αvβ8 integrin is important in neurovascular cell adhesion. Pericytes encased in the basal lamina or exposed to laminal proteins do not usually differentiate (Dore-Duffy, unpublished observations). Thus migration through the basal lamina is necessary before pericytes can function in their stem cell capacity. Regulation at the level of the basal lamina may also be integral to vascular adaptability to an ever-changing environment and to pericyte signaling mechanisms.

In its pericapillary location, the pericyte may signal nearby ECs, astrocytes, neurons, smooth muscle cells and perhaps other pericytes. Pericyte-EC contacts include peg and socket arrangements and gap junctions. Gap junctions allow pericytes to communicate with ECs through the exchange of ions and small molecules. Peg-and-socket contacts enable pericytes to penetrate through the basal lamina and make contact with other cells and nearby vessels. Junction complexes including adhesion plaques also support transmission of contractile forces from pericytes to other cells. Pericyte gap junctions contain N-cadherin, a variety of adhesion molecules, β-catenin, extracellular matrix (ECM) molecules such as fibronectin, and a number of integrins. Thus, pericytes are involved in highly complex signaling cascades that enable this cell to respond to changes in the microenvironment. However, it is unclear whether gap junctions and peg and socket contacts are naturally present or whether they are initiated during changes in functional activity. For example, it is known that pericytes interdigitate with ECs during the early phases of angiogenesis and with neurons during the maturation of newly-formed vessels. These sites of communication are altered under pathological conditions. During cerebral edema or diabetes, gap junctions are substantially decreased or disrupted in retinal pericytes. Diabetes-induced changes in gap junctions may be regulated by high glucose. Pericyte-EC communication via gap junctions is fundamental to the adaptive responses to compromised bioenergetic homeostasis. Crosstalk between ECs, pericytes, as well as astrocytes is involved in regulation of insulin transport. Pericyte/EC crosstalk is also integral to physiological angiogenesis, and is likely to be important in adaptation to hypoxic injury and focal capillary contractility.

2. Pericytes and astrocytes during vasculogenesis and angiogenesis

Vasculogenesis is the formation of new blood-vessels by differentiation of vascular precursor cells during development. During retinal development, a role for astrocyte-pericyte communication has been established. Retinal vascularization begins in the inner retinal layer and sprouts radially from the optic nerve to reach the periphery of the retina. Subsequently, retinal vessels sprout into the deep retinal layer to vascularize three parallel nerve fiber layers and two plexiform layers. Experiments using retinal models have tested the hypothesis that astrocytes and pericytes influence this process by affecting the composition of the extracellular matrix. Fibronectin, but not laminin, is expressed in zones of vasculogenesis immediately prior to vessel formation. At this time astrocytes and pericytes spread into the tissue and may be involved in the initiation of vasculogenesis. In fact, it is unclear whether platelet-derived growth factor receptors PDGFβR+/PDGFαR+ pericytes and/or PDGFαR+ immature astrocytes are the regulating cell type. Increased amounts of fibronectin mRNA suggest that fibronectin is synthesized by cells within this same region. Pericytes are known to synthesize most extracellular matrix protein components. Differentiation of endothelial cells is correlated with the appearance of pericytes in the vessel wall and laminin in the vascular basement membrane. Astrocyte-conditioned medium stimulates fibronectin expression by both primary endothelial cells and pericytes. Astrocyte-induced pericyte synthesis of fibronectin and perhaps laminin is an essential step in the initiation of retinal vasculogenesis. It is, however, unclear whether a similar mechanism functions in the brain.

Vascularization in the brain during development is derived from a preformed perineural vascular plexus and occurs almost exclusively through sprouting angiogenesis that starts at embryonic day 9 in vertebrates. Angiogenesis is the formation of new vessels from existing vessels. Sprouting angiogenesis is an invasive process that involves proteolytic activities required for degradation of the basal lamina, with pericyte and endothelial migration through tissue matrix. During vessel formation, the recruitment of pericytes and astrocytes to newly-forming vascular tubes is closely associated with the formation of tight junctions. At P4, invading vessels are in direct contact with pericytes, but not with astrocytes. With the progression of development, foot processes of astrocytes are gathered around retinal vessels and the maturation of tight junction ZO-1 in endothelial cells is more clearly defined. Tight junctions can be formed with contact from pericytes without the ensheathment of the astrocytic foot processes. From in vitro studies it is clear that pericytes induce synthesis of both occludin and claudin through the release of angiopoetin-1. Thus tight junction formation in the BBB could be developed, in part, by cellular interactions between EC and pericytes followed by astrocytes (as reviewed in). The expression of ZO-1 is augmented by astrocytes. Moreover, ZO-1 as well as occludin or claudin together may be biological indicators of barrier maturation. The role of the pericyte in BBB function will be discussed below.

Studies using glial fibrillary acidic protein (GFAP)-knockout mice (GFAP-/-) indicate that, although astrocyte foot interactions with the microvasculature are missing, neovascularization and the formation of tight junctions as well as other CNS morphology appears to be natural. Astrocyte neuronal interactions are disrupted. These data suggest that astrocyte interaction with the capillaries or neurons is not essential for tight junction formation. Of interest is that GFAP-/- mice are prone to hemorrhagic injury. Similar observations were observed by McCarthy and colleagues in studies using animals lacking alphav integrins. In contrast, administration of the gliotoxin 6-aminonicotinamide (6-AN) to chick embryos during both early and late embryonic development showed a good correlation between perivascular glial depletion and BBB impairment suggesting that astroglia do in fact play a role in BBB prenatal differentiation and must in some way contribute to vascular function. Taken together the results suggest that, while astrocyte formation of end-feet is not essential for tight junction formation, astrocytes are an important component contributing to normal vessel structural integrity. These results may also indicate that pericytes or other CNS cellular components can compensate for the lack of direct astrocyte signaling.

Using in vitro model systems to study vasculogenesis, scientists have learned that both pericytes and astrocytes are involved in formation of capillary structures. Both cell types form endothelial connections with newly forming vessels (Figure 1) realigning themselves according to the same arrangement seen in vivo. Pericytes in co-culture associate with EC more rapidly than astrocytes. In multi-cellular systems involving pericytes, astrocytes, and EC newly forming tubes have the three dimensional structure of a vessel and exhibit both a lumen and tight junctions. Tube formation in triple cultures is more rapid than that observed in EC/pericyte or EC/astrocyte, co-cultures. The triple co-culture of pericytes and astrocytes with ECs is thought by most investigators to represent a better model system to study the BBB. This may be in part due to the role of agrin, aquaporin 4, and astrocyte polarity in the BBB.

The process of vasculogenesis and differentiation is a complex system that involves crosstalk between numerous cells and is regulated by a number of signaling pathways.

Cell surface proteases expressed on both EC and pericytes exert additional subtle functions in sprouting angiogenesis. These functions involve membrane type-1 matrix metalloproteinase (MT1-MMP), other MMPs, and ADAMs (a disintegrin and metalloproteinase domain). Proteases modulate the balance between pro- and anti-angiogenic factors by activation of growth factors and chemokines, shedding of chemokines and cytokines from membrane-bound precursors, and generation of (matrix) protein fragments that inhibit or activate angiogenesis. Furthermore, they participate in the recruitment of leukocytes and progenitor cells, which contribute to the initiation and progression of angiogenesis. Pericytes are involved in the initiation as well as termination of angiogenesis (as reviewed in). At the initiation of angiogenesis, pericytes are involved in induction of endothelial activation accompanied by augmentation of a variety of proteases, adhesion molecules and proteoglycans. Astrocyte expression of tumor necrosis factor converting enzyme (TACE/ADAM-17) may facilitate pericyte PDGFβR signaling mechanisms. Alternatively, at maturation the recruitment of pericytes to the newly-formed endothelial tubes is accompanied by silencing of MMP activities. Recruitment to the newly-formed vessel with termination of angiogenesis involves PDGFβ as well as transforming growth factor beta (TGFβ). PDGFβ is thought to be essential for the retention of pericytes in the newly-formed vessels. Ablation of PDGFβ results in an embryonic lethal mutation associated with multiple vascular abnormalities.

3.1 Contractility

The concept that pericytes regulate blood flow at the capillary level was originally proposed by Steinach and Kahn in 1903 and Ni in 1922. Both scientific groups studied the effects of electrical stimulation or exposure to toxic stimuli on capillary diameter. Doré reviewed this area in 1923. As stated by Doré,: "Until a few years ago the capillaries were regarded as elastic tubes undergoing passive distension in accordance with the general blood pressure, the state of contraction or dilatation of the supplying arterioles, and the nutrition of the vascular walls". The concepts put forward in this 1923 review are on target with exciting more-recently published data.

CNS pericytes have receptors for a large number of vasoactive signaling molecules suggesting that they have the capacity to be involved in cerebrovascular autoregulation. Expression of alpha muscle actin (αSMA) and the intermediate filament desmin, two proteins found in smooth muscle cells, as well as their adherence to the endovascular cells make them potential candidates for the regulation of capillary diameter and focal capillary blood flow. Electrical stimulation of retinal and cerebellar pericytes is reported to evoke a localized capillary constriction. ATP in the retina or noradrenaline in the cerebellum also results in constriction of capillaries by pericytes. Glutamate reverses the constriction produced by noradrenaline.

Following simulated ischemia and traumatic brain injury (TBI), capillary pericytes are induced to express αSMA and upregulation of pericyte αSMA is correlated with a focal decrease in capillary diameter. Upregulation of muscle actin was mediated by endothelin-1. Other investigators have shown that capillary contraction can be directly linked to metabolic need. Exposure to substances that increase pericyte calcium level induces vessel contraction with a concomitant decrease in the capillary lumen diameter. The contractile response appears to involve a cascade of events resulting in the inhibition of Na+/Ca2+ exchangers on the EC. Hypoxia, which closes gap junctions, switches the effect of lactate from contraction to relaxation. Thus, pericyte function may be linked with local vascular adaptation to changes in bioenergetic requirements and is intimately linked to astrocyte function.

The calcium-dependent transcription factor NFATc3 is a member of the nuclear factor of activated T cells (NFAT)-family of transcription factors. NFATc3 is critical for embryonic vascular development and differentiation. Filosa and colleagues investigated the role of glutamate in control of NFATc3 regulation in pericytes. Coronal cortical slices from neonatal rats were subjected to electrical field stimulation or were treated with glutamate receptor agonist (+/-)-1-aminocyclopentane-trans-1,3-dicarboxylic acid (t-ACPD). Electrical field stimulation induced NFATc3 nuclear accumulation in pericytes and astrocytes. The response in pericytes was dependent on metabotropic glutamate receptor (mGluR) activation. NFATc3 nuclear accumulation in pericytes was prevented when astrocytic function was abolished with the gliotoxin L-alpha-aminoadipate. Results suggest that astrocyte glutamate, via mGluR activation, may regulate gene transcription in pluripotent vascular pericytes.

3.2 BBB Permeability

It has been known for decades that the CNS tissue microenvironment provides the cues for BBB induction and differentiation (as reviewed in). Development of the BBB (barrier genesis) is the result of coordinated molecular signaling at the neurovascular interface. Only recently has the canonical Wnt/beta-catenin pathway and the Wnt7a/7b growth factors been implicated in CNS angiogenesis and in BBB induction. This pathway interacts with other pathways that are crucial for vascular development such as VEGF. Wnt/beta-catenin pathways enhance pericyte mesenchymal differentiation in the presence of TGF-beta3, as demonstrated by increased Sox-9 expression and glycosaminoglycan release into the extracellular matrix. In contrast, transduction of pericytes with a recombinant adenovirus encoding dominant-negative T-cell factor-4 blocked Wnt/beta-catenin signaling and inhibited pericyte differentiation to chondrocytes, leading to reduced Sox-9, reduced type II collagen expression and reduced glycosaminoglycan accumulation. These data demonstrate that TGF-beta3 induces the chondrogenic differentiation of pericytes by inducing Wnt/beta-catenin signaling and T-cell factor-induced gene transcription. In response to injury, the Wnt/beta catenin signaling pathway is enhanced in proliferating NG2 chondroitin sulphate proteoglycan positive cells undergoing differentiation to NG2 glia. It is unclear whether induction of Wnt/beta-catenin signaling in pericytes is responsible for the regulation of the BBB by augmenting the number of NG2+ astrocyte subsets.

Pericytes play a key role in vascular remodeling during development and in the adult. Considerable insight into pericyte biology during development has arisen from studies employing genetically-manipulated mice with disrupted PDGFβ/platelet PDGFβR signaling. During development, EC-secreted PDGFβ binds to pericyte PDGFβR receptors located on the pericyte plasma membrane resulting in dimerization of the receptor. Pericytes themselves produce PDGFβ and thus may signal in an autocrine fashion. PDGF stimulates the proliferation, migration, and recruitment of pericytes to the vascular wall of newly-formed blood vessels. PDGFβ and PDGFβR knockout mice have diminished pericyte numbers and a lack of pericyte coverage. The mutation is embryonic lethal with abnormal vasculogenesis. Loss of pericytes also results in loss of BBB integrity during embryogenesis clearly showing that pericytes are essential to the differentiation of the BBB during development and have an important role in regulating the BBB. The exact mechanisms are still somewhat unclear as pericytes have been shown to both induce permeability and to inhibit permeability during development.

PDGFβ and PDGFβR interactions are also involved in pericyte-mediated regulation of vascular function in the adult brain and have a pivotal role in the regulation of the cerebral microcirculation. However, the functional roles of CNS pericytes in the adult and aging brain are less well understood. In the adult animal, it is generally accepted that pericyte association with the microvessel is essential to vascular integrity and that loss of pericytes leads to an increase in vascular leakage and altered vascular function. However, loss of pericytes does not always result in a permanent loss of function and does not always result in disease. Pericytes migrate naturally during the early phases of physiological angiogenesis to make way for growing sprouts, or in response to stress or injury. Migration from the microvessels following TBI for example, is thought to promote survival as pericytes remaining in their vascular location show signs of degenerative activity. Migration from the vessel involves upregulation of cell surface proteases. Newly-forming vessels both in adult angiogenesis and neovascularization are characterized by increased leakiness. This is transient under normal circumstances but is abnormal in conditions such as pathological angiogenesis. During angiogenesis there is co-migration of pericytes with EC sprouts and concomitant proliferation of migrated cells before renewed pericyte coverage and termination of angiogenesis. Pericytes may also be recruited from the bone marrow in adult mice and may have a role in initiation as well as termination of angiogenesis. Renewed pericyte coverage restores vascular integrity. These observations are supported by data derived using in vitro models of angiogenesis. Lack of pericyte termination of angiogenesis alters vascular function and may promote vascular leakiness in part by structural problems with tight junctions. Pericytes may also be essential to regulation of transport mechanisms. Taken together it is easy to speculate that loss of pericyte function may result in the induction of edema and inflammation.

Is there a role for astrocytes in maintenance of BBB function? Certainly the astrocytes provide a structural barrier that helps promote vascular integrity. As discussed, microvessels from the GFAP knockout mouse that have no astrocyte end-feet have a tendency to form micro-hemorrhages despite the presence of normal tight junctions. The interaction of astrocytes with the capillary appears to have an ordered structure as seen in Figure 2a in wild type capillaries. GFAP staining seems to have a fish net orientation that may assist in promoting vascular integrity. Heterozygous animals display a very disordered GFAP staining (Figure 2b). Capillaries from GFAP-/- mice display no staining pattern (Figure 2c). We have found that, to compensate for the loss of astrocyte end-feet, pericytes proliferate. Pericyte to EC ratios are much higher than those observed for wild type mice and for GFAP+/- heterozygotes (Figure 3; Table 1). This is in contrast to data by others using PDGF deficient animals. The presence of astrogliosis may also alter pericyte function.

The integral association of PDGF/PDGFR signaling in maintenance of pericyte function, makes it easy to speculate that astrocytes may be able to regulate pericyte function by the modulation of PDGFβ signaling. Controlled synthesis of astrocyte H2O2 alters PDGF signaling and is neuroprotective in conditions of oxidative stress. The expression of truncated PDGFβR inhibits PDGF signaling. Inhibition is also seen with upregulation of PDGFαR. Heparan sulphate controls the diffusion, and thus the availability of PDGFβ. Perlecan, a heparin sulfate proteoglycan, has been reported to modulate the BBB and is produced by astrocytes during the stress response. Astrocyte modulation of pericyte function is seen in the injured retina.

4. Pericyte-astrocyte communication and disease

Under normal conditions, the pericyte is relatively quiescent and is essential for vascular stability. Under conditions of stress or injury, the pericyte undergoes phenotypic and functional changes that may include migration, proliferation or differentiation. How these events that include pericyte reprogramming are coordinated at the molecular level needs to be determined. However, it is clear that pericyte dysfunction or the loss of pericytes is likely to play an important role in the pathogenesis of disease.

Pericyte loss or a reduced pericyte-to-EC ratio may be achieved through: 1) migration of pericytes from their microvascular location under pathological or physiological conditions, 2) pericyte death, 3) reduced pericyte turnover or maintenance, and 4) selective alteration of pericyte recruitment to EC that may be associated with dysregulation of angiogenesis and abnormal PDGFβ signaling. Loss of pericytes with reduced pericyte-to-EC ratios results in a focal increase in permeability. This can be normal as seen in the transient decrease in pericyte-to-EC ratios due to migration of pericytes during endogenous adaptation to chronic mild hypoxia or may be abnormal as observed in a number of pathophysiological diseases. Migration may also play a pathogenic role such as that observed in diabetic retinopathy. Decreased pericyte-to-EC ratios have been observed following TBI (20) and stroke, multiple sclerosis, brain tumors, diabetic retinopathy, aging, and in a variety of angiopathies. Pericyte loss may also play a role in Alzheimer's disease, however; enhanced pericyte coverage of some vessels suggests that increased proliferation of pericytes is an adaptation to focal loss of bioenergetic homeostasis. Pericyte loss due to cellular degeneration/apoptosis has been shown in hypertrophic scars, keloids, early diabetic retinopathy, brain tumors, liver cancer hyperglycemia, and during development. Premature infants have decreased pericyte coverage. A decreased pericyte-to-EC ratio also observed during vascular regression.

Increased pericyte coverage may also be an indicator of vascular dysfunction. Pericyte proliferation has been associated with development of muscularization during pulmonary hypertension and is thought to be due to platelet activating factor. Cochlear pericytes in the stria vascularis are markedly affected by acoustic trauma. Levels of the pericyte structural protein, desmin, substantially increase after noise exposure with a corresponding increase in pericyte coverage of vessels. Increased expression levels of desmin were associated with the induction of hypoxia-inducible factor (HIF)-1alpha and the upregulation of vascular endothelial growth factor (VEGF). Inhibition of HIF-1alpha activity decreased VEGF expression levels. Blockade of VEGF activity with SU1498, a VEGF receptor inhibitor, significantly attenuated the expression of desmin in pericytes and may have altered the adaptive process to acoustic stress. Increased pericyte-to-EC ratios are also observed in response to over expression of PDGFβ. The percentage of vessels covered by pericytes is nearly doubled in myelofibrotic bone marrow.

Direct evidence for astrocyte augmentation of pericyte coverage is lacking. However, indirect observations suggest that astrocytes may help augment pericyte proliferation through augmentation of PDGFβ levels or release of inflammatory mediators that enhance gliosis. In patients with glaucoma, enhanced proliferation is modest but restricted to NG2+ pericytes. Astrocytes and pericytes both express estrogen receptors. Astrocytes have been shown to be a source of estrogen following neuronal injury due to an upregulation of aromatase. Estrogens attenuate PDGFβ signaling in vascular smooth muscle cells.

On a more subtle level pericyte stem cell activity may be a target for astrocyte modulation. Pericytes have been shown to be multipotent adult stem cells in a number of tissues. Primary CNS pericytes are capable of differentiating along both the mesenchymal and neural lineages depending on the culture conditions [, as reviewed]. In the absence of serum in the presence of basic fibroblast growth factor (bFGF) cultured adult pericytes form immature NG2+ astrocytes/radial glial cells, NG2+ oligodendrocyte progenitor-like cells and neurons. Thus in response to injury pericytes may undergo neurogenesis. Astrocyte-generated signaling molecules have been shown to augment neurogenesis and differentiation of oligodendrocyte progenitor cells (OPC). Radial glial cells also retain neurogenic potential. During injury responses in the kindled animal, astrocyte activation and induction of neurogenesis is due in part to augmentation of nestin expression in pericytes. Following TBI, Wnt/beta-catenin signaling occurs in quiescent NG2 progenitors in the cortex, in subcallosal zone (SCZ) progenitors, and in subependymal cells surrounding the central canal. Initially after TBI, beta-catenin signaling was predominantly increased in a subset of NG2+ progenitors in the cortex. One week following injury, the majority of beta-catenin signaling appeared in reactive astrocytes but not other glial cells. Interestingly, cells with beta-catenin signaling were not generated following spinal cord injury. This suggests that although augmentation of pericyte generated stem cell activity and differentiation may be essential to tissue plasticity in adult animals responses may be tissue specific. Further, differentiations within microvascular locations, as well as other abnormal pericyte responses to injury, are likely to be highly deleterious.

5. Pericytes here and now

After its identification by Rouget in the late 1800s, relatively little was published about the pericyte until 1902 when the presence of this intriguing cell was confirmed. The development of tissue culture techniques, as well as genetically-manipulated transgenic models in which pericyte coverage is absent or diminished has stimulated considerable interest and provided invaluable tools needed to study pericyte biology. However, while genetically-modified animals can be an important tool some caution should be used when attributing functional roles from observations derived in knockout animals. Adaptive responses to a genetic modification may also confound the interpretation. One must also consider that the phenotype is a function both of the planned genetic manipulation and of potential adaptive responses to the change. There are a number of examples in the literature that uniquely illustrated this point. Pericytes are integral to the regulation of vascular function as shown in PDGFβ knockouts. However, PDGFα knockout is also embryonic lethal and displays a similar phenotype, and together with PDGFβ is also integral to postnatal development. In the future more targeted manipulations as well as fate mapping will likely clarify the functional role of pericytes in many tissues.

Conclusions

In this review we discussed evidence that pericytes and astrocytes undergo direct cell-to-cell communication. We also discuss indirect evidence that suggests that astrocytes and pericytes coordinate BBB function. It is clear that this communication is needed for the maintenance of vascular function and must be integral to endogenous adaptation to injury in the adult neurovascular unit. Loss of pericyte function and/or loss of proper astrocyte contact with the BBB can result in pericyte dysfunction and development of disease. A better understanding of the mechanisms by which pericytes communicate with other cells and how altered communication may result in disease pathology is likely to yield exciting new insights as well as the development of a new therapeutic target in CNS disorders.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

PDD had primary responsibility for the design of experiments discussed within the review and for the organization and conception of the article. RB performed experiments detailed in the figures and tables as well as development of concepts discussed within. VK conducted experiments to provide some of the data within the manuscript as well as helped with its preparation. DB collected and secured data and interpreted material utilized for the review. AB discussed the organization of the review and possible concepts to be included. All authors have reviewed and approved the final version of the manuscript.

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    Du R Petritsch C Lu K Liu P Haller A Ganss R Song H Vandenberg S Bergers G Matrix metalloproteinase-2 regulates vascular patterning and growth affecting tumor cell survival and invasion in GBMNeuro Oncol2008 10254264

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  22. 22.

    Diaz-Flores L Gutierrez R Varela H Angiogenesis: an updateHistol Histopathol1994 9807843

    Not in our library

  23. 23.

    Nehls V Herrmann R Huhnken M Guide migration as a novel mechanism of capillary network remodeling is regulated by basic fibroblast growth factorHistochem Cell Biol1998 109319329

    Not in our library10.1007/s004180050232

  24. 24.

    Nehls V Schuchardt E Drenckhahn D The effect of fibroblasts, vascular smooth muscle cells, and pericytes on sprout formation of endothelial cells in a fibrin gel angiogenesis systemMicrovasc Res1994 48349363

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  26. 26.

    Wollburg H Noell S Mask A Wolburg-Buchholz K Fallier-Becker P Brain endothelial cells and the glio-vascular complexCell Tissue Res2009 3357596

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  27. 27.

    del Zoppo GJ Milner R Integrin-matrix interactions in the cerebral microvasculatureArterioscler Thromb Vasc Biol2006 2619661975

    Not in our library10.1161/01.atv.0000232525.65682.a2

  28. 28.

    Stratman AN Schwindt AE Malotte KM Davis GE Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilizationBlood2010 11647204730

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  29. 29.

    Kalimo H Lehto M Nanto-Salonen K Jalkanen M Risteli L Risteli J Narva EV Characterization of the perivascular reticulin network in a case of primary brain lymphoma. Immunohistochemical demonstration of collagen types I, III, IV, and V; laminin; and fibronectinActa Neuropathol1985 66299305

    Not in our library10.1007/bf00690962

  30. 30.

    Canfield AE Schor AM Loskutoff DJ Schor SL Grant ME Plasminogen activator inhibitor-type I is a major biosynthetic product of retinal microvascular endothelial cells and pericytes in cultureBiochem J1989 259529535

    Not in our library10.1042/bj2590529

  31. 31.

    Mandarino LJ Sundarraj N Finlayson J Hassel HR Regulation of fibronectin and laminin synthesis by retinal capillary endothelial cells and pericytes in vitroExp Eye Res1993 57609621

    Not in our library10.1006/exer.1993.1166

  32. 32.

    Jeon H Ono M Kumagai C Miki K Morita A Kitagawa Y Pericytes from microvessels fragment produce type IV collagen and multiple laminin isoformsBiosci Biotechnol Biochem1996 60856861

    Not in our library10.1271/bbb.60.856

  33. 33.

    Díaz-Flores L Gutiérrez R Madrid JF Varela H Valladares F Acosta E Martín-Vasallo P Díaz-Flores L Jr Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell nicheHistol Histopathol2009 24909969

    Not in our library10.14670/hh-24.909

  34. 34.

    Gonul E Duz B Kahraman S Kayali H Kubar A Timurkaynak E Early pericyte response to brain hypoxia in cats: an ultrastructural studyMicrovasc Res2002 64116119

    Not in our library10.1006/mvre.2002.2413

  35. 35.

    Arismendi-Morillo G Castellano A Tumoral micro-blood vessels and vascular microenvironment in human astrocytic tumors. A transmission electron microscopy studyJ Neurooncol2005 73211217

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  36. 36.

    Wiley LA Rupp GR Steinle JJ Sympathetic innervation regulates basement membrane thickening and pericyte number in rat retinaInvest Ophthalmol Vis Sci2005 46744748

    Not in our library10.1167/iovs.04-1023

  37. 37.

    Nielson BS Sehested M Kjeldsen L Borregaard N Rygaard J Dan K Expression of matrix metalloprotease-9 in vascular pericytes in human breast cancerLab Invest1997 77345355

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  38. 38.

    Arihiro S Ohtani H Hiwatashi N Torii A Sorsa T Nagura H Vascular smooth muscle cells and pericytes express MMP-1, MMP-9, TIMP-1 and type I procollagen in inflammatory bowel diseaseHistopathology2001 395059

    Not in our library10.1046/j.1365-2559.2001.01142.x

  39. 39.

    Zozulya A Weidenfeller C Galla HJ Pericyte-endothelial cell interaction increases MMP-9 secretion at the blood brain barrier in vitroBrain Res2008 1189111

    Not in our library10.1016/j.brainres.2007.10.099

  40. 40.

    Xing C Arai K Park KP Lo EH Induction of vascular endothelial growth factor and matrix metalloproteinase-9 via CD47 signaling in neurovascular cellsNeurochem Res2010 3510921097

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  41. 41.

    Thanabalasundaram G Pieper C Lischper M Galla HJ Regulation of the blood-brain barrier integrity by pericytes via matrix metalloproteinases mediated activation of vascular endothelial growth factor in vitroBrain Res2010 1347110

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  42. 42.

    Hughes SJ Wall N Scholfield CN McGeown JG Gardiner TA Stitt AW Curtis TM Advanced glycation end product modified basement membrane attenuates endothelin-1 induced [Ca2+]i signaling and contraction in retinal microvascular pericytesMol Vis2004 109961004

    Not in our library

  43. 43.

    McCarty JH Monahan-Earley RA Brown LF Keller M Gerhardt H Rubin K Shani M Dvorak HF Wolburg H Bader BL Dvorak AM Hynes RO Defective associations between blood vessels and brain parenchyma lead to cerebral hemorrhage in mice lacking alphav integrinsMol Cell Biol2002 2276677677

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  44. 44.

    McCarty JH Cell biology of the neurovascular unit: implications for drug delivery across the blood-brain barrierAssay Drug Dev Technol2005 38995

    Not in our library10.1089/adt.2005.3.89

  45. 45.

    Hayden MR Sowers JR Tyagi SC The central role of vascular extracellular matrix and basement membrane remodeling in metabolic syndrome and type 2 diabetes: the matrix preloadedCardiovasc Diabetol2005 49

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  46. 46.

    Ryan US Ryan JW Whitaker C How do kinins affect vascular tone?Adv Exp Med Biol1979 120A375391

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  47. 47.

    Filipovich-Rimon T Fleisher-Berkovich S Protein synthesis dependent effects of kinins on astrocyte prostaglandin synthesisPeptides2010 31651656

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  48. 48.

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  49. 49.

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    Not in our library

  50. 50.

    Larson DM Haudenschild CC Beyer EC Gap junction messenger RNA expression by vascular wall cellsCirc Res1990 6610741080

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  51. 51.

    Cuevas P Gutierrez-Diaz JA Reimers D Dujovny M Diaz FG Ausman JI Pericyte endothelial gap junctions in human cerebral capillariesAnat Embryol (Berl)1984 170155159

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  53. 53.

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  54. 54.

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  55. 55.

    Castejón OJ Electron microscopic study of capillary wall in human cerebral edemaJ Neuropathol Exp Neurol1980 39296328

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  56. 56.

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    Not in our library

  57. 57.

    Kawamura H Oku H Li Q Sakagami K Puro DG Endothelin-induced changes in the physiology of retinal pericytesInvest Ophthalmol Vis Sci2002 43882888

    Not in our library

  58. 58.

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  59. 59.

    Dore-Duffy P LaManna JC Physiologic angiodynamics in the brainAntioxid Redox Signal2007 913631371

    Not in our library10.1089/ars.2007.1713

  60. 60.

    Fruttiger M Development of the mouse retinal vasculature: angiogenesis versus vasculogenesisInvest Ophthalmol Vis Sci2002 43522527

    Not in our library

  61. 61.

    Canfield AE Allen TD Grant ME Schor SL Schor AM Modulation of extracellular matrix biosynthesis by bovine retinal pericytes in vitro: effects of the substratum and cell densityJ Cell Sci1990 96159169

    Not in our library10.1242/jcs.96.1.159

  62. 62.

    Jiang B Liou GI Behzadian MA Caldwell RB Astrocytes modulate retinal vasculogenesis: effects on fibronectin expressionJ Cell Sci1994 10724992508

    Not in our library10.1242/jcs.107.9.2499

  63. 63.

    Plate KH Mechanisms of Angiogenesis in the BrainJ Neuropath Exp Neurol1999 58313320

    Not in our library10.1097/00005072-199904000-00001

  64. 64.

    Gardner TW Lieth E Khin SA Barber AJ Bonsall DJ Lesher T Rice K Brennan WA Jr Astrocytes increase barrier properties and ZO-1 expression in retinal vascular endothelial cellsArterioscler Thromb Vasc Bio2006 5524012411

    Not in our library

  65. 65.

    Hori S Ohtsuki S Hosoya K Nakashima E Terasaki TA Pericyte-derived angiopoietin-1 multimeric complex induces occludin gene expression in brain capillary endothelial cells through Tie-2 activation in vitroJ Neurochem2007 89503513

    Not in our library10.1111/j.1471-4159.2004.02343.x

  66. 66.

    Haseloff RF Blasig IE Bauer HC Bauer H In search of the astrocytic factor(s) modulating blood-brain barrier functions in brain capillary endothelial cells in vitroCell Mol Neurobiol2005 252539

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  67. 67.

    Kim JH Kim JH Yu YS Kim DH Kim KWJ Recruitment of pericytes and astrocytes is closely related to the formation of tight junction in developing retinal vesselsNeurosci Res2009 87653659

    Not in our library10.1002/jnr.21884

  68. 68.

    Benner M Kisseberth WS Su Y Besnard K Messing A GFAP promoter direct astrocyte-specific expression in transgenic miceJ Neurosci1994 1410301037

    Not in our library10.1523/jneurosci.14-03-01030.1994

  69. 69.

    Delaney CL Brenner M Messing A Conditional ablation of cerebellar astrocytes in postnatal transgenic miceJ Neurosci1996 1669086918

    Not in our library10.1523/jneurosci.16-21-06908.1996

  70. 70.

    McCall MA Gregg RG Behringer RR Brenner M Delaney CL Galbreath EJ Zhang CL Pearce RA Chiu SY Messing A Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiologyProc Natl ACad Sci USA1996 9363616366

    Not in our library10.1073/pnas.93.13.6361

  71. 71.

    Nawashiro H Messing A Azzam N Brenner M Mice lacking GFAP are hypersensitive to traumatic cerebrospinal injuryNeuroreport1998 916911696

    Not in our library10.1097/00001756-199806010-00004

  72. 72.

    Bertossi M Girolamo F Errede M Virgintino D Roncali L Effects of 6-aminonicotinamide gliotoxin on blood-brain barrier differentiation in the chick embryo cerebellumAnat Embryol2003 207209219

    Not in our library10.1007/s00429-003-0335-4

  73. 73.

    Nakagawa S Deli MA Kawaguchi H Shimizudani T Shimono T Kittel A Tanaka K Niwa M A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytesNeurochem Int2009 54253263

    Not in our library10.1016/j.neuint.2008.12.002

  74. 74.

    Al Ahmad A Gassmann M Ogunshola OO Maintaining blood-brain barrier integrity: pericytes perform better than astrocytes during prolonged oxygen deprivationJ Cell Physiol2009 218612622

    Not in our library10.1002/jcp.21638

  75. 75.

    Nakagawa S Deli MA Nakao S Honda M Hayashi K Nakaoke R Kataoka Y Niwa M Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cellsCell Mol Neurobiol2007 27687694

    Not in our library10.1007/s10571-007-9195-4

  76. 76.

    Bryan BA D'Amore PA Pericytes isolation and use in endothelial/pericyte co-culture modelsMethods Enzymol2008 443315331

    Not in our library10.1016/s0076-6879(08)02016-8

  77. 77.

    Wolburg H Noell S Wolburg-Buchholz K Mack A Fallier-Becker P Agrin, aquaporin-4, and astrocyte polarity as an important feature of the blood-brain barrierNeuroscientist2009 15180193

    Not in our library10.1177/1073858408329509

  78. 78.

    Mendelson K Swendeman S Saftig P Blobel CP Stimulation of platelet-derived growth factor receptor beta (PDGFRbeta) activates ADAM17 and promotes metalloproteinase-dependent cross-talk between the PDGFRbeta and epidermal growth factor receptor (EGFR) signaling pathwaysJ Biol Chem2010 2852502425032

    Not in our library10.1074/jbc.m110.102566

  79. 79.

    Fukushi J Makagiansar IT Stallcup WB NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrinMol Biol Cell2004 1535803590

    Not in our library10.1091/mbc.e04-03-0236

  80. 80.

    Hurtado O Lizasoain I Fernández-Tomé P Alvarez-Barrientos A Leza JC Lorenzo P Moro MA TACE/ADAM17-TNF-alpha pathway in rat cortical cultures after exposure to oxygen-glucose deprivation or glutamateJ Cereb Blood Flow Metab2002 22576585

    Not in our library10.1097/00004647-200205000-00009

  81. 81.

    Van Hinsbergh VW Koolwijk P Endothelial sprouting and angiogenesis: matrix metalloproteinases in the leadCardiovasc Res2008 78203212

    Not in our library10.1093/cvr/cvm102

  82. 82.

    Risau W Drexler H Mironov V Smits A Siegbahn A Funa K Heldin CH Platelet-derived growth factor is angiogenic in vivoGrowth Factors1992 7261266

    Not in our library10.3109/08977199209046408

  83. 83.

    Darland DC D'Amore PA TGF beta is required for the formation of capillary-like structures in three-dimensional cocultures of 10T1/2 and endothelial cellsAngiogenesis2001 41120

    Not in our library10.1023/a:1016611824696

  84. 84.

    Hellstrom M Kalen M Lindahl P Abramsson A Betsholtz C Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessels formation in the mouseDevelopment1999 12630473055

    Not in our library10.1242/dev.126.14.3047

  85. 85.

    Lindblom P Gerhardt H Leibner S Abramsson A Enge M Hellstrom M Backstrom G Fredriksson S Landegren U Nystrom HC Bergstrom G Dejana e Ostman A Lindahl P Betsholtz C Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wallGenes Dev2003 1718351840

    Not in our library10.1101/gad.266803

  86. 86.

    Armulik A Abramsson A Betsholtz C Endothelial/pericyte interactionsCirc Res2005 97512523

    Not in our library10.1161/01.res.0000182903.16652.d7

  87. 87.

    Bjarnegard M Enge M Norlin j Gustafsdottir S Fredriksson S Abramsson A Takemoto M Gustafsson E Fassler R Betsholtz C Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalitiesDevelopment2004 31318471857

    Not in our library10.1242/dev.01080

  88. 88.

    Steinach E Kahn BH Echte Contractilität und motorische Innervation der BlutcapillarenPflügers Archiv1903 97195[German]

    Not in our library

  89. 89.

    Ni TG The active response of capillaries of frogs, tadpoles, fish, bats, and men to various forms of excitationAmer J Phys1922 62282309

    Not in our library

  90. 90.

    Peppiatt CM Howarth C Mobbs P Attwell D Bidirectional control of CNS capillary diameter by pericytesNature2006 443700704

    Not in our library10.1038/nature05193

  91. 91.

    Hamilton NB Attwell D Hall CN Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and diseaseFront Neuroenergetics2010 25

    Not in our library10.3389/fnene.2010.00005

  92. 92.

    Bell RD Winkler EA Sagare AP Singh I Larue B Deane R Zlokovic BV Pericytes Control Key Neurovascular Functions and Neuronal Phenotype in the Adult Brain and during Brain AgingNeuron2010 68409412

    Not in our library10.1016/j.neuron.2010.09.043

  93. 93.

    Quignard JF Harley EA Duhault J Vanhoutte PM Félétou M K+ channels in cultured bovine retinal pericytes: effects of beta-adrenergic stimulationJ Cardiovasc Pharmacol2003 42379388

    Not in our library10.1097/00005344-200309000-00009

  94. 94.

    Cao C Goo JH Lee-Kwon W Pallone TL Vasa recta pericytes express a strong inward rectifier K+ conductanceAm J Physiol Regul Integr Comp Physiol2006 290R16011607

    Not in our library10.1152/ajpregu.00877.2005

  95. 95.

    Jackson WF Potassium channels in the peripheral microcirculationMicrocirculation2005 12113127

    Not in our library10.1080/10739680590896072

  96. 96.

    Bondjers C He L Takemoto M Norlin J Asker N Hellström M Lindahl P Betsholtz C Microarray analysis of blood microvessels from PDGF-B and PDGF-Rbeta mutant mice identifies novel markers for brain pericytesFASEB J2006 2017031705

    Not in our library10.1096/fj.05-4944fje

  97. 97.

    Kelley C D'Amore P Hechtman HB Shepro D Vasoactive hormones and cAMP affect pericyte contraction and stress fibres in vitroJ Muscle Res Cell Motil1988 9184194

    Not in our library10.1007/bf01773740

  98. 98.

    Das A Frank RN Weber ML Kennedy A Reidy CA Mancini MA ATP causes retinal pericytes to contract in vitroExp Eye Res1988 46349362

    Not in our library10.1016/s0014-4835(88)80025-3

  99. 99.

    Matthew KE Herman IM The pericyte: Cellular regulation of microvascular blood flowMicrovasc Res2009 77235246

    Not in our library10.1016/j.mvr.2009.01.007

  100. 100.

    Anderson DR Glaucoma, capillaries and pericytes. 1. Blood flow regulationOphthalmologica1996 210257262

    Not in our library10.1159/000310722

  101. 101.

    Edelman DA Jiang Y Tyburski J Wilson RF Steffes C Pericytes and their role in microvasculature homeostasisJ Surg Res135305311

    Not in our library10.1016/j.jss.2006.06.010

  102. 102.

    Hughes S Gardiner T Hu P Baxter L Rosinova E Chan-Ling T Altered pericyte-endothelial relations in the rat retina during aging: implications for vessel stabilityNeurobiol Aging2006 2718381847

    Not in our library10.1016/j.neurobiolaging.2005.10.021

  103. 103.

    Kelley C D'Amore P Hechtman HB Shepro D Vasoactive hormones and cAMP affect pericyte contraction and stress fibres in vitroJ Muscle Res Cell Motil1988 9184194

    Not in our library10.1007/bf01773740

  104. 104.

    Filosa JA Nelson MT Gonzales Bosc LV Activity-dependent NFATc3 nuclear accumulation in pericytes from cortical parenchymal microvesselsJ Physiol Cell Physiol2007 29317971805

    Not in our library10.1152/ajpcell.00554.2006

  105. 105.

    Liebner S Plate KH Differentiation of the brain vasculature: the answer came blowing by the WntJ Angiogenes Res2010 21

    Not in our library10.1186/2040-2384-2-1

  106. 106.

    Lee HS Han J Bai HJ Kim KW Brain angiogenesis in developmental and pathological processes: regulation, molecular and cellular communication at the neurovascular interfaceFEBS J2009 27646224635

    Not in our library10.1111/j.1742-4658.2009.07174.x

  107. 107.

    Stenman JM Rajagopal J Carroll TJ Ishibashi M McMahon J McMahon AP Canonical WNT Signaling regulates organ-specific assembly and differentiation of CNS vasculatureScience2008 32212471250

    Not in our library10.1126/science.1164594

  108. 108.

    Daneman R Agalliu D Zhou L Kuhnert F Kuo CJ Barres BA Wnt/beta-catenin signaling is required for CNS, but not-CNS, angiogenesisProc Natl Acad Sci USA2009 106641646

    Not in our library10.1073/pnas.0805165106

  109. 109.

    White BD Nathe RJ Maris DO Nguyen NK Goodson JM Moon RT Horner PJ Beta-catenin signaling increases in proliferating NG2+progenitors and astrocytes during post-traumatic gliogenesis in the adult brainStem Cells2010 28297307

    Not in our library10.1002/stem.268

  110. 110.

    Leveen P Pekny M Gebre-Medhin S Swolin B Larsson E Betsholtz C Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalitiesGenes Dev1994 818751887

    Not in our library10.1101/gad.8.16.1875

  111. 111.

    Siegfried G Basak A Prichett-Pejic W Scamuffa N Ma L Benjannet S Veinot JP Calvo F Seidah N Khatib AM Regulation of the stepwise proteolytic cleavage and secretion of PDGF-B by the proprotein convertasesOncogene2005 2469256935

    Not in our library10.1038/sj.onc.1208838

  112. 112.

    Zlokovic BV The blood-brain barrier in health and chronic neurodegenerative disordersNeuron2008 57178201

    Not in our library10.1016/j.neuron.2008.01.003

  113. 113.

    Danema R Zhou L Amanuel A Kebede Barres BA Pericytes are required for blood-brain barrier integrity during embryogenesisNature2010 468223231

    Not in our library10.1038/nature09612

  114. 114.

    Armulik A Genove G Mae M Nisancioglu MN Wallgard E Niaudet C Liqun H Norlin J Lindblom P Strittmatter K Johansson BR Betsholtz C Pericytes regulate the blood-brain barrierNature2010 468557561

    Not in our library10.1038/nature09522

  115. 115.

    Girolamo F Virgintino D Errede M Capobianco C Bernandini N Bertossi M Roncali L Involvement of metalloprotease-2 in the development of human brain microvesselsHistochem Cell Biol2004 122261270

    Not in our library10.1007/s00418-004-0705-x

  116. 116.

    Diaz-Flores L Gutierrez R Valladares F Varela H Perez M Intense vascular sprouting from rat femoral vein induced by prostaglandins E1 and E2Anat Rec1994 2386876

    Not in our library10.1002/ar.1092380109

  117. 117.

    Nehls V Denzer K Drenckhahn D Pericyte involvement in capillary sprouting during angiogenesis in situCell Tissue Res1992 270469474

    Not in our library10.1007/bf00645048

  118. 118.

    Virgintino D Ozerdem U Girolamo F Roncali L Stallcup WB Perris R Reversal of cellular roles in angiogenesis: implications for anti-angiogenic therapyJ Vasc Res2008 4512931

    Not in our library10.1159/000109965

  119. 119.

    Diaz-Flores L Gutierrez R Madrid JF Varela H Valladares F Acosta E Martin-Vasallo P Diaz-Flores L Jr Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell nicheHistol Histopathol2009 24909969

    Not in our library10.14670/hh-24.909

  120. 120.

    Kokovay E Li L Cunningham LA Angiogenetic recruitment of pericytes from bone marrow after strokeJ Cereb Blood Flow Metab2006 26545555

    Not in our library10.1038/sj.jcbfm.9600214

  121. 121.

    Minakawa T Bready J Berliner J Fisher M Cancilla PA In vitro interaction of astrocytes and pericytes with capillary-like structures of brain microvessels oendotheliumLab Invest1991 653240

    Not in our library

  122. 122.

    Lai CH Kuo KH The critical component to establish in vitro BBB model: PericyteBrain Res Brain Res Rev2005 50258265

    Not in our library10.1016/j.brainresrev.2005.03.007

  123. 123.

    Ahmad AA Taboada CB Gassmann M Ogunshola OO Astrocytes and pericytes differentially modulate blood-brain barrier characteristics during development and hypoxic insultJ Cereb Blood Flow Metab2010 1010381045

    Not in our library10.1038/jcbfm.2010.148

  124. 124.

    Haskew RE Mongin AA Kimelberg HK Peroxynitrite enhances astrocytic volume-sensitive excitatory amino acid release via a src tyrosine kinase-dependent mechanismJ Neurochem2002 82903912

    Not in our library10.1046/j.1471-4159.2002.01037.x

  125. 125.

    Hede SM Hansson I Afink GB Eriksson A Nazarenko I Andrae J Genove G Westermark B Nister M GFAP promoter driven transgenic exprassion of PDGFB in the mouse brain leads to glioblastoma in a Tro53 null backgroundGlia2009 5711431153

    Not in our library10.1002/glia.20837

  126. 126.

    Tagami M Yamagata K Fujino H Kubota A Nara Y Yamory Y Morphological differentiation of endothelial cells co-cultured with astrocytes on type-I or type IV collagenCell Tissue Res1992 268225232

    Not in our library10.1007/bf00318790

  127. 127.

    Choi MH Lee IK Kim GW Kim BU Han YH Yu DY Park HS Kim KY Lee JS Choi C Bae YS Lee BI Rhee SG Kang SW Regulation of PDGF signaling and vascular remodeling by peroxiredoxin IINature2005 435347353

    Not in our library10.1038/nature03587

  128. 128.

    Haskew-Layton RE Payappilly JB Smirnova NA Ma TC Chan KK Murphy TH Guo H Langley B Sultana B Butterfield DA Santagata S Alldred MJ Gazaryan IG Bell GW Ginsberg SD Ratan RR Controlled enzymatic production of astrocytic hydrogen peroxide protects neurons from oxidative stress via an Nrf2-independent pathwayProc Natl Acad Sci USA2010 1071738517390

    Not in our library10.1073/pnas.1003996107

  129. 129.

    Ueno H Colbert H Escobedo JA Williams LT Inhibition of PDGF beta receptor signal transduction by coexpression of a truncated receptorScience1991 252844848

    Not in our library10.1126/science.1851331

  130. 130.

    Zhou T Liu H Zhang P Luo C Effect of truncated PDGF-Alpha receptor on cellular cycle and proliferation for vascular cells of pulmonary arterySichuan Da Xue Xue Bao Yi Xue Ban2003 34313

    Not in our library

  131. 131.

    Kurup S Abramsson A Li JP Lindahl U Kjellen L Betsholtz C Genhardt H Spillmann D Heparin Sulphate requirement in platelet-derived growth factor B-mediated pericyte recruitmentBiochem Soc Trans2006 34454455

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  132. 132.

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    Szpak GM Lewandowska E Wierzba-Bobrowicz T Bertrand E Pasennik E Mendel T Stepien T Leszczynska A Rafalowska J Small cerebral vessel disease in familial amyloid and non-amyloid angiopathies: FAD-PS-1 (P117L) mutation and CADASIL. Immunohistochemical and ultrastructural studiesFolia Neuropathol2007 45192204

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    Vermeulen PB Colpaert C Salgado R Royers R Hellemans H Van Den Heuvel E Goovaerts G Dirix LY Van ME Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasiaJ Pathol2001 195336342

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    Li W Liu X Yanoff M Cohen S Ye X Cultured retinal capillary pericytes die by apoptosis after an abrupt fluctuation from high to low glucose levels: a comparative study with retinal capillary endothelial cellsDiabetologia1996 39537547

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    Khoury J Langleben D Platelet-activating factor stimulates lung pericyte growth in vitroAm J Physiol1996 270L298304

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    Shi X Cochlear pericyte responses to acoustic trauma and involvement of hypoxia-inducible factor-1 alpha and vascular endothelial growth factorAm J Pathol2009 17416921704

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    Song N Huang Y Shi H Yuan S Ding Y Song X Fu Y Luo Y Overexpression of platelet-derived growth factor-BB increases tumor pericyte content via stromal-derived factor-1 alpha/CXCR4 axisCancer Res2009 69605764

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    Zetterberg E Alessandro MV Migliaccio AR Vainchenker W Tulliez M Dickie R Hasselbalch H Rogers R Palmblad J Pericyte coverage of abnormal blood vessels in myelofibrotic bone marrowsHaematologica2007 92597604

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    Vinukonda G Dummula K Malik S Hu F Thompson CI Csiszar A Ungvari Z Ballabh Effect of prenatal glucocorticoids on cerebral vasculature of the developing brainStroke2010 4117661773

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    Fioravanzo l Venturini M Di Liddo R Marchi F Grandi C Parnigotto PP Folin M Involvement of Rat Hippocampal Astrocytes in β-Amyloid - Induced Angiogenesis and NeuroinflammationCurr Alzheimer Res2010

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    Sortino MA Platania P Chisari M Merlo S Copani A Catania MV A major role for astrocytes in the neuroprotective effect of estrogenDrug Dev Res2006 66126135

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    Inman DM Horner PJ Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucomaGlia2007 55942953

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    Bukovsky A Cekanova M Caudle MR Wimalasena J Foster JS Henley DC Elder RF Expression and localization of estrogen receptor-alpha protein in normal and abnormal term placentae and stimulation of trophoblast differentiation by estradiolReprod Biol Endocrinol2003 113

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    Kappert k Caglayan E Huntgeburth M Baumer AT Sparwel J Uebel M Rosenkranz S 17Beta-estradiol attenuates PDGF signaling in vascular smooth muscle cells at the postreceptor levelAm J Physiol Heart Circ Physiol2006 290H538546

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    Bonnie J Korach D Korach KS Estrogen receptors and human diseaseJ Clin Invest2006 116561570

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    Gaughwin PM Caldwell MA Anderson JM Schwiening CJ Fawcett JW Compston DAS Chandran S Astrocytes promote neurogenesis from oligodendrocyte precursor cellsEur J Neurosci2006 23945956

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    Mori T Buffo A Gotz M The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesisCurr Top Dev Biol2005 696799

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    Zheng T Marshal LL Laywell ED Steindler DA Neurogenic astrocytes transplanted into the adult mouse lateral ventricle contribute to olfactory neurogenesis, and reveal a novel intrinsic subependymal neuronJ Neuroscience2006 142175185

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    Kraev IV Godukhin OV Patrushev IV Davies HA Popov VI Stewart MG Partial kindling induces neurogenesis, activates astrocytes and alters synaptic morphology in the dentate gyrus of freely moving adult ratsJ Neurosci2009 162254267

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    Nakagawa T Miyamoto O Janjua NA Auer RN Nagao S Itano T Localization of nestin in amygdaloid kindled rat; an immunoelectron microscopic studyCan J Neurol Sci2004 31514519

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    Lindahl P Karlsson L Hellstrom M Gebre-Medhin S Willetts K Health JK Betsholtz C Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung developmentDevelopment1997 12439433953

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    Soriano P The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somitesDevelopment1997 12426912700

    Not in our library10.1242/dev.124.14.2691

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    Betsholtz C Role of platelet-derived growth factors in mouse developmentInt J Dev Biol1995 39817825

    Not in our library

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