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Immunomodulatory properties of human adult and fetal multipotent mesenchymal stem cells

Pei-Min Chen, Men-Luh Yen, Ko-Jiunn Liu and 2 more

Journal of Biomedical Science · 2011 · Review

doi:10.1186/1423-0127-18-49

Abstract

In recent years, a large number of studies have contributed to our understanding of the immunomodulatory mechanisms used by multipotent mesenchymal stem cells (MSCs). Initially isolated from the bone marrow (BM), MSCs have been found in many tissues but the strong immunomodulatory properties are best studied in BM MSCs. The immunomodulatory effects of BM MSCs are wide, extending to T lymphocytes and dendritic cells, and are therapeutically useful for treatment of immune-related diseases including graft-versus-host disease as well as possibly autoimmune diseases. However, BM MSCs are very rare cells and require an invasive procedure for procurement. Recently, MSCs have also been found in fetal-stage embryo-proper and extra-embryonic tissues, and these human fetal MSCs (F-MSCs) have a higher proliferative profile, and are capable of multilineage differentiation as well as exert strong immunomodulatory effects. As such, these F-MSCs can be viewed as alternative sources of MSCs. We review here the current understanding of the mechanisms behind the immunomodulatory properties of BM MSCs and F-MSCs. An increase in our understanding of MSC suppressor mechanisms will offer insights for prevalent clinical use of these versatile adult stem cells in the near future.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 26, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Mesenchymal stem cells: Definition and functional capacity

Human mesenchymal stem cells (MSCs) are a population of multilineage progenitor cells with the ability to differentiate into multiple mesenchymal lineages such as chondrocytes, osteoblasts, or adipocytes. The initial isolation of MSCs was from the bone marrow (BM) based on plastic adherence of the cells as opposed BM hematopoieitic cells which can be cultured in suspension. Increasingly, MSCs have been reported to be isolated from a number of other organs in the adult and fetal-stage tissue. Due to the difficulty in comparing the various methods used to isolate BM and tissue MSCs, a recent movement to define these progenitor cells have proposed a minimal criteria for MSCs in terms of trilineage mesodermal differentiation capacity and expression of a specific panel of cell surface marker including being positive for CD73, CD90, and CD105; and negative for hematopoietic markers such as CD14 or CD11b, CD34, CD45, and CD19 or CD79a. The ease of isolation of MSCs along with reports of differentiation into extra-mesodermal cell types has made MSCs a popular choice for cell therapy for pre-clinical and clinical trials of a variety of diseases.

2. Immunomodulatory Properties of Adult and Fetal-stage MSCs

One important reason for the abundant number of clinical studies using adult BMMSCs is the immunomodulatory properties of these cells. As with organ transplantation, a critical issue in stem cell therapy is the rejection resulting from immune incompatibility between donor and recipient. BMMSCs' immunomodulatory properties appear to obviate this major obstacle for cell therapy; moreover, these immunosuppressive effects allow for an even wider range of disease indications for these progenitor cells, including use for immune-related diseases. BMMSCs appear to be poorly immunogenic, since they constitutively express low levels of major histocompatibility complex (MHC) class I molecules and no MHC class II molecules. Moreover, BMMSCs do not express co-stimulatory molecules such as CD40, CD80, or CD86 which are involved in the activation of T cell for transplant rejection. Several studies show that differentiated and undifferentiated BMMSCs have suppressive effects on alloantigen- and mitogen-stimulated lymphocyte proliferation in in vitro studies using mixed lymphocyte reactions (MLR), with a concomitant reduction in the production of proinflammatory cytokines such as interferon-γ (IFN-γ) and tumor necrosis factor-α (TNF-α). Thus, the clinical indications for human BMMSCs are considerably wider than other human stem cells, ranging from cell replacement for degenerative diseases--common indications for stem cell therapy--as well as immune-related diseases including autoimmune diseases and transplantation rejection.

While the differentiation plasticity and immunomodulatory properties of adult BMMSCs have brought much excitement in terms of prevalent clinical use for these progenitor cells, the fact remains that these cells are very rare, with cell numbers and proliferative capacity further decreasing with age. In addition, an invasive procedure in terms of BM aspiration is needed to obtain BMMSCs. Thus, investigators have worked to identify other abundant and easily attainable sources of MSCs for therapeutic use. While many other adult tissues appear to harbor MSCs as well, the problems of requiring invasive procedures to obtain these relatively rare cells remain. A number of labs have thus turned to using discarded post-partum fetal-stage tissue for isolation of progenitor cells, since fetal umbilical cord blood is known to be a good source for the hematopoietic stem cell, one type of highly used stem cells. Known to be important in mediating the fetomaternal tolerance of pregnancy, fetal-stage extra-embryonic tissues are easily accessible sources for isolation of cells since these tissues are discarded at birth, obviating ethical issues as well.

Fetal MSCs (F-MSCs) have been derived from a number of fetal tissues, including fetal liver and bone marrow. Moreover, extra-embryonic structures of fetal origin are also good sources for MSCs since they are discarded after birth, and MSCs isolated from human umbilical cord blood (UCB)(hUCB-MSCs), the Wharton's Jelly (hWJ-MSCs) of the umbilical cord itself, amniotic fluid (AF)(hAF-MSCs), amnion (hA-MSCs), and the placenta (hP-MSCs) have been demonstrated. These increasing reports on the isolation of MSCs from all these fetal-stage tissues demonstrate that F-MSCs can be an abundant and viable source of MSCs.

In addition to multilineage differentiation capacity, F-MSCs have been demonstrated to harbor strong immunomodulatory effects as well. F-MSCs lack or exhibit very low expression of highly polymorphic MHC class I (HLA-A, HLA-B, and HLA-C); furthermore, they do not express surface MHC class II molecules (HLA-DP, HLA-DQ, and HLA-DR) nor co-stimulatory molecules, such as CD40, CD40 ligand, CD80, and CD86. F-MSCs not only fail to induce an allogeneic or xenogeneic immune response in MLR, but also strongly suppress lymphocyte proliferation induced by mitogens or alloantigens, often in a dose-dependent manner. Based on these data, F-MSCs appear to be as least as non-immunogenic as BMMSCs, and in some reports, appear to be even more immunomodulatory than its adult counterpart. This is supported by clinical experience in hematopoietic stem cell transplantation (HSCT), where lower incidences of immune-related consequences are consistently seen after UCB HSCT compared to BM HSCT.

Based on the accumulating data, it appears that both adult-source MSCs--most prominently BMMSCS--and F-MSCs are good candidates for cell therapy for immune-related diseases in addition to degenerative diseases. In general, the overwhelming majority of the data is based on studies with BMMSCs rather than F-MSCs, since F-MSCs are newer sources of MSCs and have been studied only in the past few years. This review focuses on evidence for the immunomodulation of adult BMMSCs and F-MSCs, properties which appear increasingly relevant for clinical use. Interactions of BMMSCs and F-MSCs with subpopulations of leukocytes, and mechanisms of actions--when investigated--are reviewed.

3.1 Interactions with T Lymphocytes

Currently, the interactions of MSCs with T lymphocytes are the best studied. Many reports have shown that BMMSCs affect several properties of T cells, most prominently efficiently suppressing activated CD4+ T helper cell and CD8+ cytotoxic T cell (CTL) proliferation. Activated T cells are arrested by BMMSCs in the G0/G1 phase of the cell cycle, but apoptosis is not induced. Besides their ability to impair the proliferation of activated T cells, BMMSCs can prolong the survival of unstimulated T cells by rescuing the lymphocytes from activation-induced cell death by down-regulation of Fas receptor and Fas ligand on T cells and inhibition of endogenous proteases involved in cell death. Further studies have shown that BMMSCs reduce IFN-γ production by CD4+ Th1 cells and interleukin (IL)-17 release by CD4+ Th17 lymphocytes, whereas IL-4 secretion by CD4+ Th2 cells is augmented. The cytolytic potential of CTLs can also be efficiently impaired by BMMSCs. Recently, several studies investigated the impact of BMMSCs on T regulatory lymphocytes (Tregs), a population of CD4+ CD25high cells which play an important role in the induction of peripheral tolerance and the inhibition of proinflammatory immune responses. Many studies have shown that BMMSCs cultured with stimulated peripheral blood mononuclear cells (PBMCs) can induce the expansion of functional CD4+ CD25high Foxp3+ Tregs. A number of mechanisms have been suggested--both cell-contact dependent and independent mechanisms--but there is no clear consensus as of yet; for example, transforming growth factor-β (TGF-β) has been cited as being involved in one study but not in another study. This discrepancy may be due to the subtle phenotypic variations induced in BMMSCs by the many methods available for isolation of these adult stem cells.

Several studies have attempted to delineate which specific molecules are involved in the immunomodulatory effect of BMMSCs on T-cell proliferation and effector functions. In the human system, the effects of BMMSCs on T cells are mainly mediated through cell-contact independent processes, implicating the importance of secreted factors. These molecules include IL-1β, TGF-β1, hepatocyte growth factor (HGF), prostaglandin E2 (PGE2), indoleamine 2,3-dioxygenase (IDO), heme oxygenase-1 (HO-1), leukemia inhibitory factor (LIF), insulin-like growth factor (IGF), soluble human leukocyte antigen G5 (sHLA-G5), galectin, and Jagged-1. Most of the inhibitory soluble factors are not constitutively secreted, but can be induced by the interaction between activated effector cells and BMMSCs (Table 1).

F-MSCs also have been reported to have strong inhibitory effects on T lymphocytes. hWJ-MSCs display potent immunosuppressive properties on T cell activation in an antigen-independent manner, and can also suppress the proliferation of mitogen-stimulated rat splenocytes (xenograft model) or human PBMCs (allogeneic transplant model) in allogeneic MLR in vitro. Furthermore, CD14+ monocytes promote the immunosuppressive effect of hWJ-MSCs probably via the IL-1β-PGE2 axis. The inflammatory cytokine IL-1β produced by hPBMCs upon activation upregulates the expression of cyclooxygenase-2 (COX-2) and the production of PGE2 by hWJ-MSCs. hP-MSCs can also suppress the proliferation of allogeneic T cells. These effects of hP-MSCs may involve the secretion of soluble factors TGF-β and IL-10. Both hP-MSCs and hUCB-MSCs have been shown to increase the proportion of Tregs, which contributes to the suppression of T cell proliferation(Figure 1).

Interestingly, a number of reports have demonstrated that in in vitro systems, pretreatment of BMMSCs and F-MSCs with the pro-inflammatory cytokine IFN-γ actually enhances their immunomodulation rather than decreases it. Some investigators have postulated that this may explain the in vivo ability of MSCs to be effective against very inflammatory diseases such as graft-versus-host-disease (GVHD), in which the production of such activating cytokines as IFN-γ by T and natural killer lymphocytes (NKs) may actually promote MSC immunomodulation, subsequently suppressing the proliferation of CD4+, CD8+ T cells, and NKs themselves. While this has not been proven in animal studies, pre-clinical and clinical data continues to reveal therapeutic efficacy after MSC administration, giving indirect evidence for this hypothesis. Interestingly, while IFN-γ pre-treatment of adult BMMSCs results in induction of IDO, a strong immunosuppressive enzyme, MHC II molecules--which can elicit inflammatory responses--are induced as well, but this does not appear to change the immunomodulatory effects of BMMSCs. It would be critical to elucidate this paradox to better understand why these progenitors possess such strong immunomodulatory properties inherently.

3.2 Interactions with Dendritic Cells (DCs)

DCs are derived from monocytes and are potent antigen-presenting cells (APCs) that act by internalizing, shuttling, and presenting antigens to naïve T-cells, which then leads to T-cell activation. These key regulators of immunity display an extraordinary capacity to induce T cell responses and secrete a variety of cytokines; the differentiation status of DCs can influence whether its target lymphocyte--often T cells--will mount an effector versus a more immunomodulatory response. As such, studies have shown that BMMSCs inhibit the immunostimulatory capacity of DCs, supporting the development of a more tolerogenic population of DCs. BMMSCs markedly impair PBMCs differentiation into DCs and inhibit endocytosis and the production of IL-12 by DCs. In the presence of BMMSCs, the differentiation of CD14+ monocytes into DCs is impaired, and the monocytes retain high expression of CD14+--a marker of immaturity for DCs--without the upregulation of CD1a, HLA-DR, or co-stimulatory molecules which prevent the DCs to efficiently induce T cell effector responses. In addition, BMMSCs also efficiently suppress the T cell-activating functions of DCs, including stimulation of T-cell proliferation, reduction of naïve CD4+ T lymphocytes polarizing into proinflammatory Th1 cells, and promotion of Th2 responses. BMMSCs can decrease TNF-α secretion by DCs, which then leads to a reduced number of IFN-γ-producing Th1 cells. APCs generated in the presence of BMMSCs express low levels of IL-12, TNF-α, and MHC class II and high levels of IL-1β and IL-10, regardless of CD86 expression. BMMSCs also induce DCs to secrete IL-10, which favors IL-4-producing Th2 cells and Tregs. Furthermore, BMMSCs impair the release of cytokines by activated DCs through PGE2. Both cell-to-cell contact and soluble factors such as IL-6 and macrophage-colony-stimulating factor (M-CSF) mediate the BMMSC-mediated inhibition of differentiation, cytokine production, and T-cell stimulatory capacity of DCs(Table 1).

Interestingly, there are studies which show that BMMSCs itself can function as non-professional APCs. It has been reported that IFN-γ-stimulated BMMSCs can present exogenous antigens through upregulation of MHC class II molecules, which then results in activation of CD4+ T cells. BMMSCs can also cross-present exogenous antigens to induce CD8+ T cell proliferation. A few studies have shown that BMMSCs--similar to DCs--express high levels of toll-like receptors (TLRs), including TLR1, TLR3, TLR4, and TLR5. TLRs are receptors primarily expressed on APCs which recognize conserved pathogen-derived components. Triggering of TLR3, which binds double-stranded RNA, and TLR4, which binds lipopolysaccharide (LPS) and innate self antigens, on BMMSCs has been reported to suppress the immunomodulation of these cells through Notch ⁄ Jagged1 signaling, leading to production of pro-inflammatory mediators such as IL-1β, IL-6, and IL-8. However, another report showed that triggering of TLR on BMMSCs actually induces immunosuppression, which leads to the production of immunosuppressive kynurenines induced by IDO1. IDO1 can be induced by TLR3 and TLR4 signaling and this involves the activation of protein kinase R (PKR), an autocrine IFN-β signaling loop, and the activation of signal transducer and activator of transcription 1 (STAT1)/interferon regulatory factor 1 (IRF-1). These conflicting data regarding BMMSCs suppressing DC maturation and BMMSCs itself being an APC eliciting pro-inflammatory responses will require more research for clarification. One possible reason for these discrepant findings is that there is much heterogeneity between BMMSCs isolated from laboratory to laboratory. While the recent consensus of cell surface profile and tri-lineage mesodermal differentiation requirement has been extremely helpful to unify BMMSC phenotype, there still may exist epigenetic differences due to organ of origin and donor age, just to name a few variables. Moreover, the immunomodulatory properties of MSCs from different organs have not been much investigated, and one comparative study suggests that the MSC niche is unique in each tissue, which can contributes to functional differences. Thus, it appears that studying the immunomodulatory behavior of MSCs derived from different origins would be important, and the accumulation of such data will help to shed more light and clarity on discrepant findings of this field.

Some studies have suggested that F-MSCs are poor APCs due to their low or limited expression of MHC class II and co-stimulatory molecules even after IFN-γ stimulation. Recent studies have also investigated whether F-MSCs modulate DC phenotype and function. hAMSCs exert immunomodulatory effects on APCs, as demonstrated by their capacity to block maturation of monocytes into DCs. They can prevent the expression of the DC lineage-specific marker CD1a and reduce the expression of HLA-DR, CD80, and CD83. This block in the monocyte-DC maturation process also results in impaired allostimulatory ability of these cells on allogeneic T cells. Remarkably, hUCB-MSCs modulate DCs in a different way. hUCB-MSCs suppress the function of mature DCs by driving DCs to an intermediate maturation state and boosting IL-12 production by mature DCs. These inhibitory mechanisms involve both cell-contact dependent as well as secretion of soluble factors(Figure 1).

3.3 Interactions with Natural Killer Lymphocytes (NKs)

NKs are key players of the innate immune system and are important in targeting virus-infected cells and tumor cells. NKs are highly cytotoxic and secrete large amounts of proinflammatory cytokines such as TNF-α and IFN-γ. Part of the innate immune system, these cytotoxic lymphocytes are triggered to recognize and respond to MHC molecules signifying "self" versus "non-self", rather than specific antigens which T and B lymphocytes of the adaptive immune system recognize. A few studies have shown that BMMSCs are able to suppress the proliferation and cytokine production of NKs. The inhibition requires both cell-to-cell contact and soluble factors such as PGE2 and TGF-β. BMMSCs can also modulate the cytotoxicity of NKs, reducing the levels of NK-secreted cytokines such as IFN-γ, IL-10, and TNF-α and this phenomenon also requires cell-cell contact. However, stimulated NKs can efficiently lyse autologous and allogeneic BMMSCs. The activating NK receptors NKp30, NKG2D, and DNAM-1 were involved in NK-mediated cytotoxicity against BMMSCs. IFN-γ-stimulated BMMSCs, on the other hand, were less susceptible to NK cell lysis as a consequence of the up-regulation of MHC class I molecules at the MSC surface. Moreover, the secretion of soluble HLA-G (sHLA-G) by BMMSCs plays an important role in the inhibition of NK cytotoxicity and IFN-γ release. First identified in choriocarcinoma and migratory trophoblasts, HLA-G (non-classical MHC I molecule) is thought to confer for the fetus a protective effect against the maternal immune system, including directly suppressing maternal NK cytotoxicity. HLA-G can exist in several forms, with the best characterized being the complete transmembrane form (HLA-G1)--the predominant in vivo form--and one of the three soluble, truncated forms (HLA-G5 or sHLA-G). Unlike most MHC I molecules, HLA-G has very low polymorphism and its expression in the adult is highly restricted; however, in certain pathologic states including cancer and inflammatory diseases, expression can be induced. The receptors for HLA-G include ILT-2, ILT-4, and CD94 and these receptors can be found on a number of leukocytes, most prominently being NKs(Table 1).

F-MSCs can express surface molecule HLA-G, indicating potential tolerance-inducing properties. We found that hP-MSCs are more resistant to stimulated-NK cytotoxicity than BMMSCs; moreover, hP-MSCs demonstrate enhanced suppressive effects towards NK in the presence of IFN-γ, and this is partially mediated through surface expression of HLA-G on hP-MSCs but not adult BMMSCs. The placenta is known to have unique immunomodulatory interactions with maternal uterine NKs, which also have a different effector profile than peripheral blood NKs. Thus, interactions of F-MSCs with NKs may be quite different than that found with BMMSCs, since NKs are one of the most important and predominant lymphocyte populations found during pregnancy. While such data is still scarce, research on F-MSCs interactions with this population of innate lymphocytes should yield interesting data, and perhaps even shed light on maternal-fetal immune mechanisms (Figure 1).

4. Clinical applications of adult and F-MSCs for GVHD

The majority of data on the immunomodulation of MSCs are in vitro in nature, however, a number of studies have been in vivo. One of the potentially lethal consequences after allogeneic HSCT is GVHD in which recipient cytotoxic T cells attack donor tissue, resulting in an immune-related complication which is associated with high morbidity and mortality. Animal models of GVHD are one of the most commonly used disease models to validate BMMSC immune function in vivo, and these studies have demonstrated that BMMSCs do remain immunomodulatory in vivo. Recent data has shown that the combination of BMMSCs and immunosuppressive drugs can prolong organ allograft survival. Because of the profound immunomodulatory effect of BMMSCs shown in vitro and in vivo, co-transplantation of ex vivo-expanded BMMSCs with HSCs for GVHD has been recommended. In addition, cytokines released by BMMSCs may promote homing or proliferation of HSCs and enhance HSCs engraftment. Thus, based on the accumulated in vitro and animal studies, a number of clinical trials have been started to evaluate the potential of BMMSCs for the treatment of GVHD.

While there are in general fewer studies using F-MSCs as a cell therapy source, some pre-clinical studies have been conducted. Several animal studies show the prolonged survival of hAMSCs with no evidence of immunological rejection after xenogeneic transplantation into immunocompetent animals including rats and swine. Moreover, hAF-MSCs appear to be relatively resistant to rejection by the recipient--even with allogenic cell transplantation--due to the expression of immunosuppressive factors such as CD59 (protectin) and HLA-G. Co-transplantation of UCBHSCs along with F-MSCs can reduce potential GVHD in recipients, as well as enhance UCB cell engraftment and homing of CD34+ HSCs. Therefore, F-MSCs appear to be a promising source for stem cell therapy of GVHD and likely other immune-related diseases.

5. Conclusions

MSCs are multilineage progenitors which can be isolated from many adult organs as well as fetal-stage tissues. BMMSCs and F-MSCs have been reported to harbor strong immunomodulatory effects. While the data is still scarce regarding F-MSCs, several differences in the immune-suppressive properties between F-MSCs and adult BMMSCs have been found. Future investigations on the molecular mechanisms underlying the immunomodulatory properties of both F-MSCs and adult BMMSCs would be important since these differences may have functional relevance to therapeutic use of both sources of progenitor cells.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

All authors have read and approved the final manuscript.

Acknowledgements and Funding

This work was supported by the National Science Council of Taiwan (grants NSC-99-3111-B-400-002, NSC 97-2320-B-400-005-MY3, and NSC-99-3112-B-400-006 to B.L.Y.; and NSC-99-3111-B-002-009 to M.L.Y.).

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    Not in our library10.1634/stemcells.2004-0058

  40. 40.

    Chang CJ Yen ML Chen YC Chien CC Huang HI Bai CH Yen BL Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gammaStem Cells2006 241124662477

    Not in our library10.1634/stemcells.2006-0071

  41. 41.

    Chiavegato A Bollini S Pozzobon M Callegari A Gasparotto L Taiani J Piccoli M Lenzini E Gerosa G Vendramin I Human amniotic fluid-derived stem cells are rejected after transplantation in the myocardium of normal, ischemic, immuno-suppressed or immuno-deficient ratJ Mol Cell Cardiol2007 424746759

    Not in our library10.1016/j.yjmcc.2006.12.008

  42. 42.

    Hao L Zhang C Chen XH Zou ZM Zhang X Kong PY Liang X Gao L Peng XG Sun AH Human umbilical cord blood-derived stromal cells suppress xenogeneic immune cell response in vitroCroat Med J2009 504351360

    Not in our library10.3325/cmj.2009.50.351

  43. 43.

    Ilancheran S Michalska A Peh G Wallace EM Pera M Manuelpillai U Stem cells derived from human fetal membranes display multilineage differentiation potentialBiol Reprod2007 773577588

    Not in our library10.1095/biolreprod.106.055244

  44. 44.

    Kim J Lee Y Kim H Hwang KJ Kwon HC Kim SK Cho DJ Kang SG You J Human amniotic fluid-derived stem cells have characteristics of multipotent stem cellsCell Prolif2007 4017590

    Not in our library10.1111/j.1365-2184.2007.00414.x

  45. 45.

    Lu LL Liu YJ Yang SG Zhao QJ Wang X Gong W Han ZB Xu ZS Lu YX Liu D Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentialsHaematologica2006 91810171026

    Not in our library

  46. 46.

    Oh W Kim DS Yang YS Lee JK Immunological properties of umbilical cord blood-derived mesenchymal stromal cellsCell Immunol2008 2512116123

    Not in our library10.1016/j.cellimm.2008.04.003

  47. 47.

    Portmann-Lanz CB Schoeberlein A Huber A Sager R Malek A Holzgreve W Surbek DV Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregenerationAm J Obstet Gynecol2006 1943664673

    Not in our library10.1016/j.ajog.2006.01.101

  48. 48.

    Roubelakis MG Pappa KI Bitsika V Zagoura D Vlahou A Papadaki HA Antsaklis A Anagnou NP Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cellsStem Cells Dev2007 166931952

    Not in our library10.1089/scd.2007.0036

  49. 49.
  50. 50.

    Wang M Yang Y Yang D Luo F Liang W Guo S Xu J The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitroImmunology2009 1262220232

    Not in our library10.1111/j.1365-2567.2008.02891.x

  51. 51.

    Weiss ML Anderson C Medicetty S Seshareddy KB Weiss RJ VanderWerff I Troyer D McIntosh KR Immune properties of human umbilical cord Wharton's jelly-derived cellsStem Cells2008 261128652874

    Not in our library10.1634/stemcells.2007-1028

  52. 52.

    Weiss ML Medicetty S Bledsoe AR Rachakatla RS Choi M Merchav S Luo Y Rao MS Velagaleti G Troyer D Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson's diseaseStem Cells2006 243781792

    Not in our library10.1634/stemcells.2005-0330

  53. 53.

    Li C Zhang W Jiang X Mao N Human-placenta-derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cellsCell Tissue Res2007 3303437446

    Not in our library10.1007/s00441-007-0504-5

  54. 54.

    Wolbank S Peterbauer A Fahrner M Hennerbichler S van Griensven M Stadler G Redl H Gabriel C Dose-dependent immunomodulatory effect of human stem cells from amniotic membrane: a comparison with human mesenchymal stem cells from adipose tissueTissue Eng2007 13611731183

    Not in our library10.1089/ten.2006.0313

  55. 55.

    Magatti M De Munari S Vertua E Gibelli L Wengler GS Parolini O Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilitiesStem Cells2008 261182192

    Not in our library10.1634/stemcells.2007-0491

  56. 56.

    Bailo M Soncini M Vertua E Signoroni PB Sanzone S Lombardi G Arienti D Calamani F Zatti D Paul P Engraftment potential of human amnion and chorion cells derived from term placentaTransplantation2004 781014391448

    Not in our library10.1097/01.tp.0000144606.84234.49

  57. 57.

    Li H Niederkorn JY Neelam S Mayhew E Word RA McCulley JP Alizadeh H Immunosuppressive factors secreted by human amniotic epithelial cellsInvest Ophthalmol Vis Sci2005 463900907

    Not in our library10.1167/iovs.04-0495

  58. 58.

    Aggarwal S Pittenger MF Human mesenchymal stem cells modulate allogeneic immune cell responsesBlood2005 105418151822

    Not in our library10.1182/blood-2004-04-1559

  59. 59.

    Krampera M Cosmi L Angeli R Pasini A Liotta F Andreini A Santarlasci V Mazzinghi B Pizzolo G Vinante F Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cellsStem Cells2006 242386398

    Not in our library10.1634/stemcells.2005-0008

  60. 60.

    Krampera M Glennie S Dyson J Scott D Laylor R Simpson E Dazzi F Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptideBlood2003 101937223729

    Not in our library10.1182/blood-2002-07-2104

  61. 61.

    Glennie S Soeiro I Dyson PJ Lam EW Dazzi F Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cellsBlood2005 105728212827

    Not in our library10.1182/blood-2004-09-3696

  62. 62.

    Benvenuto F Ferrari S Gerdoni E Gualandi F Frassoni F Pistoia V Mancardi G Uccelli A Human mesenchymal stem cells promote survival of T cells in a quiescent stateStem Cells2007 25717531760

    Not in our library10.1634/stemcells.2007-0068

  63. 63.

    Zhou L Chong MM Littman DR Plasticity of CD4+ T cell lineage differentiationImmunity2009 305646655

    Not in our library10.1016/j.immuni.2009.05.001

  64. 64.

    Bai L Lennon DP Eaton V Maier K Caplan AI Miller SD Miller RH Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosisGlia2009 571111921203

    Not in our library10.1002/glia.20841

  65. 65.

    Rafei M Campeau PM Aguilar-Mahecha A Buchanan M Williams P Birman E Yuan S Young YK Boivin MN Forner K Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent mannerJ Immunol2009 1821059946002

    Not in our library10.4049/jimmunol.0803962

  66. 66.

    Ghannam S Pene J Torcy-Moquet G Jorgensen C Yssel H Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotypeJ Immunol2010 1851302312

    Not in our library10.4049/jimmunol.0902007

  67. 67.

    Maccario R Podesta M Moretta A Cometa A Comoli P Montagna D Daudt L Ibatici A Piaggio G Pozzi S Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotypeHaematologica2005 904516525

    Not in our library

  68. 68.

    Riley JL June CH Blazar BR Human T regulatory cell therapy: take a billion or so and call me in the morningImmunity2009 305656665

    Not in our library10.1016/j.immuni.2009.04.006

  69. 69.

    Shevach EM Mechanisms of foxp3+ T regulatory cell-mediated suppressionImmunity2009 305636645

    Not in our library10.1016/j.immuni.2009.04.010

  70. 70.

    Itoh M Takahashi T Sakaguchi N Kuniyasu Y Shimizu J Otsuka F Sakaguchi S Thymus and autoimmunity: production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-toleranceJ Immunol1999 162953175326

    Not in our library

  71. 71.

    English K Ryan JM Tobin L Murphy MJ Barry FP Mahon BP Cell contact, prostaglandin E2 and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25Highforkhead box P3+ regulatory T cellsClin Exp Immunol2009 1561149160

    Not in our library10.1111/j.1365-2249.2009.03874.x

  72. 72.

    Prevosto C Zancolli M Canevali P Zocchi MR Poggi A Generation of CD4+ or CD8+ regulatory T cells upon mesenchymal stem cell-lymphocyte interactionHaematologica2007 927881888

    Not in our library10.3324/haematol.11240

  73. 73.

    Di Ianni M Del Papa B De Ioanni M Moretti L Bonifacio E Cecchini D Sportoletti P Falzetti F Tabilio A Mesenchymal cells recruit and regulate T regulatory cellsExp Hematol2008 363309318

    Not in our library10.1016/j.exphem.2007.11.007

  74. 74.

    Selmani Z Naji A Zidi I Favier B Gaiffe E Obert L Borg C Saas P Tiberghien P Rouas-Freiss N Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cellsStem Cells2008 261212222

    Not in our library10.1634/stemcells.2007-0554

  75. 75.

    Batten P Sarathchandra P Antoniw JW Tay SS Lowdell MW Taylor PM Yacoub MH Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: relevance to tissue engineering human heart valvesTissue Eng2006 12822632273

    Not in our library10.1089/ten.2006.12.2263

  76. 76.

    Rasmusson I Immune modulation by mesenchymal stem cellsExp Cell Res2006 3121221692179

    Not in our library10.1016/j.yexcr.2006.03.019

  77. 77.

    Groh ME Maitra B Szekely E Koc ON Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cellsExp Hematol2005 338928934

    Not in our library10.1016/j.exphem.2005.05.002

  78. 78.

    Rasmusson I Ringden O Sundberg B Le Blanc K Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanismsExp Cell Res2005 30513341

    Not in our library10.1016/j.yexcr.2004.12.013

  79. 79.

    Ryan JM Barry F Murphy JM Mahon BP Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cellsClin Exp Immunol2007 1492353363

    Not in our library10.1111/j.1365-2249.2007.03422.x

  80. 80.

    Meisel R Zibert A Laryea M Gobel U Daubener W Dilloo D Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradationBlood2004 1031246194621

    Not in our library10.1182/blood-2003-11-3909

  81. 81.

    Plumas J Chaperot L Richard MJ Molens JP Bensa JC Favrot MC Mesenchymal stem cells induce apoptosis of activated T cellsLeukemia2005 19915971604

    Not in our library10.1038/sj.leu.2403871

  82. 82.

    Chabannes D Hill M Merieau E Rossignol J Brion R Soulillou JP Anegon I Cuturi MC A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cellsBlood2007 1101036913694

    Not in our library10.1182/blood-2007-02-075481

  83. 83.

    Nasef A Mazurier C Bouchet S Francois S Chapel A Thierry D Gorin NC Fouillard L Leukemia inhibitory factor: Role in human mesenchymal stem cells mediated immunosuppressionCell Immunol2008 2531-21622

    Not in our library10.1016/j.cellimm.2008.06.002

  84. 84.

    Gieseke F Schutt B Viebahn S Koscielniak E Friedrich W Handgretinger R Muller I Human multipotent mesenchymal stromal cells inhibit proliferation of PBMCs independently of IFNgammaR1 signaling and IDO expressionBlood2007 110621972200

    Not in our library10.1182/blood-2007-04-083162

  85. 85.

    Nasef A Mathieu N Chapel A Frick J Francois S Mazurier C Boutarfa A Bouchet S Gorin NC Thierry D Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-GTransplantation2007 842231237

    Not in our library10.1097/01.tp.0000267918.07906.08

  86. 86.

    Gieseke F Bohringer J Bussolari R Dominici M Handgretinger R Muller I Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cellsBlood2010 1161937703779

    Not in our library10.1182/blood-2010-02-270777

  87. 87.

    Sioud M Mobergslien A Boudabous A Floisand Y Mesenchymal stem cell-mediated T cell suppression occurs through secreted galectinsInt J Oncol2011 382385390

    Not in our library10.3892/ijo.2010.869

  88. 88.

    Liotta F Angeli R Cosmi L Fili L Manuelli C Frosali F Mazzinghi B Maggi L Pasini A Lisi V Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signalingStem Cells2008 261279289

    Not in our library10.1634/stemcells.2007-0454

  89. 89.

    Wang D Chen K Du WT Han ZB Ren H Chi Y Yang SG Bayard F Zhu D Han ZC CD14+ monocytes promote the immunosuppressive effect of human umbilical cord matrix stem cellsExp Cell Res2010 3161524142423

    Not in our library10.1016/j.yexcr.2010.04.018

  90. 90.

    Cutler AJ Limbani V Girdlestone J Navarrete CV Umbilical cord-derived mesenchymal stromal cells modulate monocyte function to suppress T cell proliferationJ Immunol2010 1851166176623

    Not in our library10.4049/jimmunol.1002239

  91. 91.

    Chen K Wang D Du WT Han ZB Ren H Chi Y Yang SG Zhu D Bayard F Han ZC Human umbilical cord mesenchymal stem cells hUC-MSCs exert immunosuppressive activities through a PGE2-dependent mechanismClin Immunol2010 1353448458

    Not in our library10.1016/j.clim.2010.01.015

  92. 92.

    Girdlestone J Limbani VA Cutler AJ Navarrete CV Efficient expansion of mesenchymal stromal cells from umbilical cord under low serum conditionsCytotherapy2009 116738748

    Not in our library10.3109/14653240903079401

  93. 93.

    Zhang Y Li C Jiang X Zhang S Wu Y Liu B Tang P Mao N Human placenta-derived mesenchymal progenitor cells support culture expansion of long-term culture-initiating cells from cord blood CD34+ cellsExp Hematol2004 327657664

    Not in our library10.1016/j.exphem.2004.04.001

  94. 94.

    Roelen DL van der Mast BJ in't Anker PS Kleijburg C Eikmans M van Beelen E de Groot-Swings GM Fibbe WE Kanhai HH Scherjon SA Differential immunomodulatory effects of fetal versus maternal multipotent stromal cellsHum Immunol2009 7011623

    Not in our library10.1016/j.humimm.2008.10.016

  95. 95.
  96. 96.

    Jones EY Fugger L Strominger JL Siebold C MHC class II proteins and disease: a structural perspectiveNat Rev Immunol2006 64271282

    Not in our library10.1038/nri1805

  97. 97.

    Steinman RM Pack M Inaba K Dendritic cells in the T-cell areas of lymphoid organsImmunol Rev1997 1562537

    Not in our library10.1111/j.1600-065x.1997.tb00956.x

  98. 98.

    Jiang XX Zhang Y Liu B Zhang SX Wu Y Yu XD Mao N Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cellsBlood2005 1051041204126

    Not in our library10.1182/blood-2004-02-0586

  99. 99.

    Spaggiari GM Abdelrazik H Becchetti F Moretta L MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2Blood2009 1132665766583

    Not in our library10.1182/blood-2009-02-203943

  100. 100.

    Beyth S Borovsky Z Mevorach D Liebergall M Gazit Z Aslan H Galun E Rachmilewitz J Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsivenessBlood2005 105522142219

    Not in our library10.1182/blood-2004-07-2921

  101. 101.

    Li YP Paczesny S Lauret E Poirault S Bordigoni P Mekhloufi F Hequet O Bertrand Y Ou-Yang JP Stoltz JF Human mesenchymal stem cells license adult CD34+ hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathwayJ Immunol2008 180315981608

    Not in our library10.4049/jimmunol.180.3.1598

  102. 102.

    Chan WK Lau AS Li JC Law HK Lau YL Chan GC MHC expression kinetics and immunogenicity of mesenchymal stromal cells after short-term IFN-gamma challengeExp Hematol2008 361115451555

    Not in our library10.1016/j.exphem.2008.06.008

  103. 103.

    Stagg J Pommey S Eliopoulos N Galipeau J Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cellBlood2006 107625702577

    Not in our library10.1182/blood-2005-07-2793

  104. 104.

    Chan JL Tang KC Patel AP Bonilla LM Pierobon N Ponzio NM Rameshwar P Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gammaBlood2006 1071248174824

    Not in our library10.1182/blood-2006-01-0057

  105. 105.

    Francois M Romieu-Mourez R Stock-Martineau S Boivin MN Bramson JL Galipeau J Mesenchymal stromal cells cross-present soluble exogenous antigens as part of their antigen-presenting cell propertiesBlood2009 1141326322638

    Not in our library10.1182/blood-2009-02-207795

  106. 106.

    Morandi F Raffaghello L Bianchi G Meloni F Salis A Millo E Ferrone S Barnaba V Pistoia V Immunogenicity of human mesenchymal stem cells in HLA-class I-restricted T-cell responses against viral or tumor-associated antigensStem Cells2008 26512751287

    Not in our library10.1634/stemcells.2007-0878

  107. 107.

    Romieu-Mourez R Francois M Boivin MN Bouchentouf M Spaner DE Galipeau J Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotypeJ Immunol2009 1821279637973

    Not in our library10.4049/jimmunol.0803864

  108. 108.

    Pevsner-Fischer M Morad V Cohen-Sfady M Rousso-Noori L Zanin-Zhorov A Cohen S Cohen IR Zipori D Toll-like receptors and their ligands control mesenchymal stem cell functionsBlood2007 109414221432

    Not in our library10.1182/blood-2006-06-028704

  109. 109.

    Tomchuck SL Zwezdaryk KJ Coffelt SB Waterman RS Danka ES Scandurro AB Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responsesStem Cells2008 26199107

    Not in our library10.1634/stemcells.2007-0563

  110. 110.

    Opitz CA Litzenburger UM Lutz C Lanz TV Tritschler I Koppel A Tolosa E Hoberg M Anderl J Aicher WK Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase RStem Cells2009 274909919

    Not in our library10.1002/stem.7

  111. 111.

    Kern S Eichler H Stoeve J Kluter H Bieback K Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissueStem Cells2006 24512941301

    Not in our library10.1634/stemcells.2005-0342

  112. 112.

    Parolini O Alviano F Bagnara GP Bilic G Buhring HJ Evangelista M Hennerbichler S Liu B Magatti M Mao N Isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem CellsStem Cells2008 262300311

    Not in our library10.1634/stemcells.2007-0594

  113. 113.

    Magatti M De Munari S Vertua E Nassauto C Albertini A Wengler GS Parolini O Amniotic mesenchymal tissue cells inhibit dendritic cell differentiation of peripheral blood and amnion resident monocytesCell Transplant2009 188899914

    Not in our library10.3727/096368909x471314

  114. 114.

    Kronsteiner B Peterbauer-Scherb A Grillari-Voglauer R Redl H Gabriel C van Griensven M Wolbank S Human mesenchymal stem cells and renal tubular epithelial cells differentially influence monocyte-derived dendritic cell differentiation and maturationCell Immunol2011 26713038

    Not in our library10.1016/j.cellimm.2010.11.001

  115. 115.

    van den Berk LC Roelofs H Huijs T Siebers-Vermeulen KG Raymakers RA Kogler G Figdor CG Torensma R Cord blood mesenchymal stem cells propel human dendritic cells to an intermediate maturation state and boost interleukin-12 production by mature dendritic cellsImmunology2009 1284564572

    Not in our library10.1111/j.1365-2567.2009.03142.x

  116. 116.

    Moretta A Locatelli F Moretta L Human NK cells: from HLA class I-specific killer Ig-like receptors to the therapy of acute leukemiasImmunol Rev2008 2245869

    Not in our library10.1111/j.1600-065x.2008.00651.x

  117. 117.

    Caligiuri MA Human natural killer cellsBlood2008 1123461469

    Not in our library10.1182/blood-2007-09-077438

  118. 118.

    Sotiropoulou PA Perez SA Gritzapis AD Baxevanis CN Papamichail M Interactions between human mesenchymal stem cells and natural killer cellsStem Cells2006 2417485

    Not in our library10.1634/stemcells.2004-0359

  119. 119.

    Spaggiari GM Capobianco A Abdelrazik H Becchetti F Mingari MC Moretta L Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2Blood2008 111313271333

    Not in our library10.1182/blood-2007-02-074997

  120. 120.

    Poggi A Zocchi MR Antigen presenting cells and stromal cells trigger human natural killer lymphocytes to autoreactivity: evidence for the involvement of natural cytotoxicity receptors (NCR) and NKG2DClin Dev Immunol2006 132-4325336

    Not in our library10.1080/17402520600578194

  121. 121.

    Spaggiari GM Capobianco A Becchetti S Mingari MC Moretta L Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferationBlood2006 107414841490

    Not in our library10.1182/blood-2005-07-2775

  122. 122.

    Rouas-Freiss N Goncalves RM Menier C Dausset J Carosella ED Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysisProc Natl Acad Sci USA1997 94211152011525

    Not in our library10.1073/pnas.94.21.11520

  123. 123.

    Apps R Gardner L Moffett A A critical look at HLA-GTrends Immunol2008 297313321

    Not in our library10.1016/j.it.2008.02.012

  124. 124.

    Carosella ED Favier B Rouas-Freiss N Moreau P Lemaoult J Beyond the increasing complexity of the immunomodulatory HLA-G moleculeBlood2008 1111048624870

    Not in our library10.1182/blood-2007-12-127662

  125. 125.

    LeMaoult J Zafaranloo K Le Danff C Carosella ED HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cellsFASEB J2005 196662664

    Not in our library10.1096/fj.04-1617fje

  126. 126.

    La Rocca G Anzalone R Corrao S Magno F Loria T Lo Iacono M Di Stefano A Giannuzzi P Marasa L Cappello F Isolation and characterization of Oct-4+/HLA-G+ mesenchymal stem cells from human umbilical cord matrix: differentiation potential and detection of new markersHistochem Cell Biol2009 1312267282

    Not in our library10.1007/s00418-008-0519-3

  127. 127.

    Liu KJ Wang JC Chang CJ Hu HI Hsu PJ Wu YC Bai CH Sytwu HK Yen BL Surface expression of HLA-G is involved in mediating immunomodulatory effects of placenta-derived multipotent cells (PDMCs) towards natural killer lymphocytesCell Transplant2011 in press

    Not in our library10.3727/096368911x580590

  128. 128.

    Gaunt G Ramin K Immunological tolerance of the human fetusAm J Perinatol2001 186299312

    Not in our library10.1055/s-2001-17861

  129. 129.

    Moffett-King A Natural killer cells and pregnancyNat Rev Immunol2002 29656663

    Not in our library10.1038/nri886

  130. 130.

    Deeg HJ How I treat refractory acute GVHDBlood2007 1091041194126

    Not in our library10.1182/blood-2006-12-041889

  131. 131.

    Aksu AE Horibe E Sacks J Ikeguchi R Breitinger J Scozio M Unadkat J Feili-Hariri M Co-infusion of donor bone marrow with host mesenchymal stem cells treats GVHD and promotes vascularized skin allograft survival in ratsClin Immunol2008 1273348358

    Not in our library10.1016/j.clim.2008.02.003

  132. 132.

    Zhou HP Yi DH Yu SQ Sun GC Cui Q Zhu HL Liu JC Zhang JZ Wu TJ Administration of donor-derived mesenchymal stem cells can prolong the survival of rat cardiac allograftTransplant Proc2006 38930463051

    Not in our library10.1016/j.transproceed.2006.10.002

  133. 133.

    Yanez R Lamana ML Garcia-Castro J Colmenero I Ramirez M Bueren JA Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host diseaseStem Cells2006 241125822591

    Not in our library10.1634/stemcells.2006-0228

  134. 134.

    Kim DW Chung YJ Kim TG Kim YL Oh IH Cotransplantation of third-party mesenchymal stromal cells can alleviate single-donor predominance and increase engraftment from double cord transplantationBlood2004 103519411948

    Not in our library10.1182/blood-2003-05-1601

  135. 135.

    Ge W Jiang J Baroja ML Arp J Zassoko R Liu W Bartholomew A Garcia B Wang H Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft toleranceAm J Transplant2009 9817601772

    Not in our library10.1111/j.1600-6143.2009.02721.x

  136. 136.

    Popp FC Eggenhofer E Renner P Slowik P Lang SA Kaspar H Geissler EK Piso P Schlitt HJ Dahlke MH Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolateTranspl Immunol2008 201-25560

    Not in our library10.1016/j.trim.2008.08.004

  137. 137.

    von Bonin M Stolzel F Goedecke A Richter K Wuschek N Holig K Platzbecker U Illmer T Schaich M Schetelig J Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysate-containing mediumBone Marrow Transplant2009 433245251

    Not in our library10.1038/bmt.2008.316

  138. 138.

    Fang B Song Y Liao L Zhang Y Zhao RC Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host diseaseTransplant Proc2007 391033583362

    Not in our library10.1016/j.transproceed.2007.08.103

  139. 139.

    Muller I Kordowich S Holzwarth C Isensee G Lang P Neunhoeffer F Dominici M Greil J Handgretinger R Application of multipotent mesenchymal stromal cells in pediatric patients following allogeneic stem cell transplantationBlood Cells Mol Dis2008 4012532

    Not in our library10.1016/j.bcmd.2007.06.021

  140. 140.

    Lazarus HM Koc ON Devine SM Curtin P Maziarz RT Holland HK Shpall EJ McCarthy P Atkinson K Cooper BW Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patientsBiol Blood Marrow Transplant2005 115389398

    Not in our library10.1016/j.bbmt.2005.02.001

  141. 141.

    Ning H Yang F Jiang M Hu L Feng K Zhang J Yu Z Li B Xu C Li Y The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rate in hematologic malignancy patients: outcome of a pilot clinical studyLeukemia2008 223593599

    Not in our library10.1038/sj.leu.2405090

  142. 142.

    Taupin P OTI-010 Osiris Therapeutics/JCR PharmaceuticalsCurr Opin Investig Drugs2006 75473481

    Not in our library

  143. 143.

    Vianello F Dazzi F Mesenchymal stem cells for graft-versus-host disease: a double edged sword?Leukemia2008 223463465

    Not in our library10.1038/leu.2008.25

  144. 144.

    Sundin M Ringden O Sundberg B Nava S Gotherstrom C Le Blanc K No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipientsHaematologica2007 92912081215

    Not in our library10.3324/haematol.11446

  145. 145.

    Le Blanc K Ringden O Immunobiology of human mesenchymal stem cells and future use in hematopoietic stem cell transplantationBiol Blood Marrow Transplant2005 115321334

    Not in our library10.1016/j.bbmt.2005.01.005

  146. 146.

    Eliopoulos N Stagg J Lejeune L Pommey S Galipeau J Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient miceBlood2005 1061340574065

    Not in our library10.1182/blood-2005-03-1004

  147. 147.

    Bensidhoum M Chapel A Francois S Demarquay C Mazurier C Fouillard L Bouchet S Bertho JM Gourmelon P Aigueperse J Homing of in vitro expanded Stro-1- or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34 cell engraftmentBlood2004 103933133319

    Not in our library10.1182/blood-2003-04-1121

  148. 148.

    Ball LM Bernardo ME Roelofs H Lankester A Cometa A Egeler RM Locatelli F Fibbe WE Cotransplantation of ex vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem-cell transplantationBlood2007 110727642767

    Not in our library10.1182/blood-2007-04-087056

  149. 149.

    Behre G Theurich S Weber T Christopeit M Ning, et alReply to 'The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rates in hematologic malignancy patients: outcome of a pilot clinical study'Leukemia2009 231178author reply 179-180

    Not in our library10.1038/leu.2008.150

  150. 150.

    Le Blanc K Samuelsson H Gustafsson B Remberger M Sundberg B Arvidson J Ljungman P Lonnies H Nava S Ringden O Transplantation of mesenchymal stem cells to enhance engraftment of hematopoietic stem cellsLeukemia2007 21817331738

    Not in our library10.1038/sj.leu.2404777

  151. 151.

    in 't Anker PS Noort WA Kruisselbrink AB Scherjon SA Beekhuizen W Willemze R Kanhai HH Fibbe WE Nonexpanded primary lung and bone marrow-derived mesenchymal cells promote the engraftment of umbilical cord blood-derived CD34+ cells in NOD/SCID miceExp Hematol2003 3110881889

    Not in our library10.1016/s0301-472x(03)00202-9

  152. 152.

    Ringden O Remberger M Svahn BM Barkholt L Mattsson J Aschan J Le Blanc K Gustafsson B Hassan Z Omazic B Allogeneic hematopoietic stem cell transplantation for inherited disorders: experience in a single centerTransplantation2006 815718725

    Not in our library10.1097/01.tp.0000181457.43146.36

  153. 153.

    Kong XY Cai Z Pan L Zhang L Shu J Dong YL Yang N Li Q Huang XJ Zuo PP Transplantation of human amniotic cells exerts neuroprotection in MPTP-induced Parkinson disease miceBrain Res2008 1205108115

    Not in our library10.1016/j.brainres.2008.02.040

  154. 154.

    Zhao P Ise H Hongo M Ota M Konishi I Nikaido T Human amniotic mesenchymal cells have some characteristics of cardiomyocytesTransplantation2005 795528535

    Not in our library10.1097/01.tp.0000149503.92433.39

  155. 155.

    Kubo M Sonoda Y Muramatsu R Usui M Immunogenicity of human amniotic membrane in experimental xenotransplantationInvest Ophthalmol Vis Sci2001 42715391546

    Not in our library

  156. 156.

    Walther G Gekas J Bertrand OF Amniotic stem cells for cellular cardiomyoplasty: promises and premisesCatheter Cardiovasc Interv2009 737917924

    Not in our library10.1002/ccd.22016

  157. 157.

    Prather WR Toren A Meiron M Placental-derived and expanded mesenchymal stromal cells (PLX-I) to enhance the engraftment of hematopoietic stem cells derived from umbilical cord bloodExpert Opin Biol Ther2008 8812411250

    Not in our library10.1517/14712598.8.8.1241

  158. 158.

    Hiwase SD Dyson PG To LB Lewis ID Cotransplantation of placental mesenchymal stromal cells enhances single and double cord blood engraftment in nonobese diabetic/severe combined immune deficient miceStem Cells2009 27922932300

    Not in our library10.1002/stem.157

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