The transcriptome of retinal Müller glial cells

Abstract

Müller glial cells are the major type of glia in the mammalian retina. To identify the molecular machinery that defines Müller glial cell identity and function, single cell gene expression profiling was performed on Affymetrix microarrays. Identification of a cluster of genes expressed at high levels suggests a Müller glia core transcriptome, which likely underlies many of the functions of Müller glia. Expression of components of the cell cycle machinery and the Notch pathway, as well as of growth factors, chemokines, and lipoproteins might allow communication between Müller glial cells and the neurons that they support, including modulation of neuronal activity. This approach revealed a set of transcripts that were not previously characterized in (Müller) glia; validation of the expression of some of these genes was performed by in situ hybridization. Genes expressed exclusively by Müller glia were identified as novel markers. In addition, a novel BAC transgenic mouse that expresses Cre in Müller glia cells was generated. The molecular fingerprint of Müller glia provides a foundation for further studies of Müller glia development and function in normal and diseased states. J. Comp. Neurol. 509:225–238, 2008. © 2008 Wiley‐Liss, Inc.

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References 87

1. 1.

   Amaratunga A, Abraham CR, Edwards RB, Sandell JH, Schreiber BM, Fine RE. Apolipoprotein E is synthesized in the retina by Muller glial cells, secreted to the vitreous, and rapidly transported into the optic nerve by retinal ganglion cells. J Biol Chem. 1996;271:5628-5632.

   Not in our library10.1074/jbc.271.10.5628

2. 2.

   Anezary L, Medina JI, Sanchez-Nogueiro J, Lopez-Gallardo M, Prada C. Shape diversity among chick retina Müller cells and their postnatal differentiation. J Comp Neurol. 2001;438:32-49.

   Not in our library10.1002/cne.1300

3. 3.

   Awasaki T, Tatsumi R, Takahashi K, Arai K, Nakanishi Y, Ueda R, Ito K. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during rosophila metamorphosis. Neuron. 2006;50:855-867.

   Not in our library10.1016/j.neuron.2006.04.027

4. 4.

   Bao ZZ, Cepko CL. The expression and function of Notch pathway genes in the developing rat eye. J Neurosci. 1997;15:1425-1434.

   Not in our library10.1523/jneurosci.17-04-01425.1997

5. 5.

   Bachoo RM, Kim RS, Ligon KL, Maher EA, Brennan C, Billings N, Chan S, Li C, Rowitch DH, Wong WH, DePinho RA. Molecular diversity of astrocytes with implications for neurological disorders. Proc Natl Acad Sci U S A. 2004;101:8384-8389.

   Not in our library10.1073/pnas.0402140101

6. 6.

   Blackshaw S, Fraioli RE, Furukawa T, Cepko CL. Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell. 2001;107:579-589.

   Not in our library10.1016/s0092-8674(01)00574-8

7. 7.
   Genomic Analysis of Mouse Retinal Development · 2004

   No notice
8. 8.

   Brady G, Iscove NN. Construction of cDNA libraries from single cells. Methods Enzymol. 1993;225:611-623.

   Not in our library10.1016/0076-6879(93)25039-5

9. 9.

   Bringmann A, Skatchkov SN, Pannicke T, Biedermann B, Wolburg H, Orkand RK, Reichenbach A. Müller glial cells in anuran retina. Microsc Res Tech. 2000;50:384-393.

   Not in our library10.1002/1097-0029(20000901)50:5<384::aid-jemt7>3.0.co;2-w

10. 10.

    Cai L, Morrow EM, Cepko CL. Misexpression of basic helix-loop-helix genes in the murine cerebral cortex affects cell fate choices and neuronal survival. Development. 2000;127:3021-3030.

    Not in our library10.1242/dev.127.14.3021

11. 11.

    Chang ML, Wu CH, Jiang-Shieh YF, Shieh JY, Wen CY. Reactive changes of retinal astrocytes and Muller glial cells in kainate-induced neuroexcitotoxicity. J Anat. 2007;210:54-65.

    Not in our library10.1111/j.1469-7580.2006.00671.x

12. 12.

    Chan-ling T. Glial, neuronal and vascular interactions in the mammalian retina. Prog Ret Eye Res. 1994;13:357-389.

    Not in our library

13. 13.

    Che S, Ginsberg SD. Amplification of RNA transcripts using terminal continuation. Lab Invest. 2004;84:131-137.

    Not in our library10.1038/labinvest.3700005

14. 14.

    Chen CM, Cepko CL. Expression of Chx10 and Chx10–1 in the developing chicken retina. Mech Dev. 2000;90:293-297.

    Not in our library10.1016/s0925-4773(99)00251-8

15. 15.

    Chojnacki A, Shimazaki T, Gregg C, Weinmaster G, Weiss S. Glycoprotein 130 regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci. 2003;23:1730-1741.

    Not in our library10.1523/jneurosci.23-05-01730.2003

16. 16.

    Davis JA, Reed RR. Role of Olf-1 and Pax-6 transcription factors in neurodevelopment. J Neurosci. 1996;16:5082-5094.

    Not in our library10.1523/jneurosci.16-16-05082.1996

17. 17.

    De Melo, Qiu X, Du G, Cristante L, Eisenstat DD. Dlx1, Dlx2, Pax6, Brn3b and Chx10 homeobox gene expression defines the retinal ganglion and inner nuclear layers of the developing and adult mouse retina. J Comp Neurol. 2003;461:187-204.

    Not in our library10.1002/cne.10674

18. 18.

    Dulac C, Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell. 1995;83:195-206.

    Not in our library10.1016/0092-8674(95)90161-2

19. 19.

    Dyer MA, Cepko CL. Control of Müller glial cell proliferation and activation following retinal injury. Nat Neurosci. 2000;3:873-880.

    Not in our library10.1038/78774

20. 20.

    Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998;95:14863-14868.

    Not in our library10.1073/pnas.95.25.14863

21. 21.

    Farago AF, Awatramani RB, Dymecki SM. Assembly of the brain stem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron. 2006;50:205-218.

    Not in our library10.1016/j.neuron.2006.03.014

22. 22.

    Fischer AJ, Reh TA. Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci. 2001;4:247-252.

    Not in our library10.1038/85090

23. 23.

    Fischer AJ, Reh TA. Potential of Müller glia to become neurogenic retinal progenitor cells. Glia. 2003;43:70-76.

    Not in our library10.1002/glia.10218

24. 24.

    Francke M, Makarov F, Kacza J, Seeger J, Wendt S, Gartner U, Faude F, Wiedemann P, Reichenbach A. Retinal pigment epithelium melanin granules are phagocytozed by Müller glial cells in experimental retinal detachment. J Neurocytol. 2001;30:131-136.

    Not in our library10.1023/a:1011987107034

25. 25.

    Franze K, Grosche J, Skatchkov SN, Schinkinger S, Foja C, Schild D, Uckermann O, Travis K, Reichenbach A, Guck J. Müller cells are living optical fibers in the vertebrate retina. Proc Natl Acad Sci U S A. 2007;104:8287-8292.

    Not in our library10.1073/pnas.0611180104

26. 26.

    Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL. rax, Hes1, and notch1 promote the formation of Müller glia by postnatal retinal progenitor cells. Neuron. 2000;26:383-394.

    Not in our library10.1016/s0896-6273(00)81171-x

27. 27.

    Gaiano N, Fishell G. The role of Notch in promoting glial and neural stem cell fates. Annu Rev Neurosci. 2002;25:471-490.

    Not in our library10.1146/annurev.neuro.25.030702.130823

28. 28.

    Glaser T, Walton DS, Maas RL. Genomic structure, evolutionary conservation and aniridia mutations in the human Pax6 gene. Nat Genet. 1992;2:232-239.

    Not in our library10.1038/ng1192-232

29. 29.

    Greenberg KP, Geller SF, Schaffer DV, Flannery JG. Targeted transgene expression in Müller glia of normal and diseased retinas. Invest Ophthalmol Vis Sci. 2007;48:1844-1852.

    Not in our library10.1167/iovs.05-1570

30. 30.

    Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, van Heyningen V. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature. 1991;354:522-525.

    Not in our library10.1038/354522a0

31. 31.

    Hojo M, Ohtsuka T, Hashimoto N, Gradwohl G, Guillemot F, Kageyama R. Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development. 2000;127:2515-2522.

    Not in our library10.1242/dev.127.12.2515

32. 32.

    Ikeda T, Puro DG. Nerve growth factor: a mitogenic signal for retinal Müller glial cells. Brain Res. 1994;649:260-264.

    Not in our library10.1016/0006-8993(94)91072-3

33. 33.

    Inoue T, Hojo M, Bessho Y, Tano Y, Lee JE, Kageyama R. Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development. 2002;129:831-842.

    Not in our library10.1242/dev.129.4.831

34. 34.

    Iscove NN, Barbara M, Gu M, Gibson M, Modi C, Winegarden N. Representation is faithfully preserved in global cDNA amplified exponentially from sub-picogram quantities of mRNA. Nat Biotechnol. 2002;20:940-943.

    Not in our library10.1038/nbt729

35. 35.

    Ivanov D, Dvoriantchikova G, Nathanson L, McKinnon SJ, Shestopalov VI. Microarray analysis of gene expresssion in adult retinal ganglion cells. FEBS Lett. 2006;580:331-335.

    Not in our library10.1016/j.febslet.2005.12.017

36. 36.

    Jadhav AP, Cho SH, Cepko CL. Notch activity permits retinal stem cells to progress through multiple progenitor states and acquire stem cell property. Proc Natl Acad Sci U S A. 2006a;103:18998-19003.

    Not in our library10.1073/pnas.0608155103

37. 37.

    Jadhav AP, Mason HA, Cepko CL. Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development. 2006b;133:913-923.

    Not in our library10.1242/dev.02245

38. 38.

    Jenne DE, Tschopp J. Clusterthe intriguing guises of a widely expressed glycoprotein. Trends Biochem Sci. 1992;17:154-159.

    Not in our library10.1016/0968-0004(92)90325-4

39. 39.

    Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci. 2006;9:173-179.

    Not in our library10.1038/nn1620

40. 40.

    Kwan CT, Tsang SL, Krumlauf R, Shaw MH. Regulatory analysis of the mouse Hoxb3 gene: multiple elements work in concert to direct temporal and spatial patterns of expression. Dev Biol. 2001;232:176-190.

    Not in our library10.1006/dbio.2001.0157

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