Differential expression of neuronal genes in müller glia in two- and three-dimensional cultures

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 3, 2011, Pages 1439-1449

  Joseph Phillips, M ^a   Otteson, Deborah C ^b  

^a UNIVERSITY OF HOUSTON   (United States)

^b University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MIGRATION; CELL STIMULATION; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CULTURE MEDIUM; GENE; GENE EXPRESSION; GLIA; HYDROGEL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; INTERMETHOD COMPARISON; MOUSE; MUELLER CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURONAL GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RETINA NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; RETINAL NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPHEROIDS, CELLULAR; TISSUE SCAFFOLDS;

EID: 79955932358     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6400     Document Type: Article

References (68)

1. Baker PS, Brown GC. Stem-cell therapy in retinal disease. Curr Opin Ophthalmol. 2009;20:175-181.
2. Limb GA, Daniels JT. Ocular regeneration by stem cells: present status and future prospects. Br Med Bull. 2008;85:47-61.
3. Enzmann V, Yolcu E, Kaplan HJ, Ildstad ST. Stem cells as tools in regenerative therapy for retinal degeneration. Arch Ophthalmol. 2009;127:563-571.
4. Ohta K, Ito A, Tanaka H. Neuronal stem/progenitor cells in the vertebrate eye. Dev Growth Differ. 2008;50:253-259.
5. Amabile G, Meissner A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med. 2009;15:59-68.
6. Bernardos RL, Barthel LK, Meyers JR, Raymond PA. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci. 2007;27:7028-7040.
7. Reh TA, Fischer AJ. Stem cells in the vertebrate retina. Brain Behav Evol. 2001;58:296-305.
8. Ooto S, Akagi T, Kageyama R, et al. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A. 2004;101:13654-13659.
9. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA. Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A. 2008;105:19508-19513.
10. Bhatia B, Singhal S, Lawrence JM, Khaw PT, Limb GA. Distribution of Müller stem cells within the neural retina: evidence for the existence of a ciliary margin-like zone in the adult human eye. Exp Eye Res. 2009;89:373-382.
11. Takeda M, Takamiya A, Jiao JW, et al. alpha-Aminoadipate induces progenitor cell properties of Müller glia in adult mice. Invest Ophthalmol Vis Sci. 2008;49:1142-1150.
12. Nickerson PE, Da Silva N, Myers T, Stevens K, Clarke DB. Neural progenitor potential in cultured Müller glia: effects of passaging and exogenous growth factor exposure. Brain Res. 2008;1230:1-12.
13. Florian C, Langmann T, Weber BH, Morsczeck C. Murine Müller cells are progenitor cells for neuronal cells and fibrous tissue cells. Biochem Biophys Res Commun. 2008;374:187-191.
14. Lawrence JM, Singhal S, Bhatia B, et al. MIO-M1 cells and similar Müller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells. 2007;25:2033-2043.
15. Das AV, Mallya KB, Zhao X, et al. Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol. 2006;299:283-302.
16. Levenberg S, Huang NF, Lavik E, Rogers AB, Itskovitz-Eldor J, Langer R. Differentiation of human embryonic stem cells on threedimensional polymer scaffolds. Proc Natl Acad Sci U S A. 2003; 100:12741-12746.
17. Gelain F, Bottai D, Vescovi A, Zhang S. Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures. PLoS ONE. 2006;1:e119.
18. Holmes TC, de Lacalle S, Su X, Liu G, Rich A, Zhang S. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci U S A. 2000;97:6728-6733.
19. Lavik EB, Klassen H, Warfvinge K, Langer R, Young MJ. Fabrication of degradable polymer scaffolds to direct the integration and differentiation of retinal progenitors. Biomaterials. 2005;26:3187-3196.
20. Tomita M, Lavik E, Klassen H, Zahir T, Langer R, Young MJ. Biodegradable polymer composite grafts promote the survival and differentiation of retinal progenitor cells. Stem Cells. 2005;23: 1579-1588.
21. Redenti S, Neeley WL, Rompani S, et al. Engineering retinal progenitor cell and scrollable poly(glycerol-sebacate) composites for expansion and subretinal transplantation. Biomaterials. 2009;30: 3405-3414.
22. Neeley WL, Redenti S, Klassen H, et al. A microfabricated scaffold for retinal progenitor cell grafting. Biomaterials. 2008;29:418-426.
23. Otteson DC, Phillips MJ. A conditional immortalized mouse Müller glial cell line expressing glial and retinal stem-cell genes. Invest Ophthalmol Vis Sci. 2010;51:5991-6000.
24. Yokoi H, Kinoshita T, Zhang S. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc Natl Acad Sci U S A. 2005;102: 8414-8419.
25. Gelain F, Horii A, Zhang S. Designer self-assembling peptide scaffolds for 3-d tissue cell cultures and regenerative medicine. Macromolecular Biosci. 2007;7:544-551.
26. Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15:378-386.
27. Vukicevic S, Kleinman HK, Luyten FP, Roberts AB, Roche NS, Reddi AH. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp Cell Res. 1992;202:1-8.
28. Jat PS, Noble MD, Ataliotis P, et al. Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc Natl Acad Sci U S A. 1991;88:5096-5100.
29. Simpson DA, Feeney S, Boyle C, Stitt AW. Retinal VEGF mRNA measured by SYBR green I fluorescence: a versatile approach to quantitative PCR. Mol Vis. 2000;6:178-183.
30. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30:e36.
31. Merhi-Soussi F, Angenieux B, Canola K, et al. High yield of cells committed to the photoreceptor fate from expanded mouse retinal stem cells. Stem Cells. 2006;24:2060-2070.
32. Haeseleer F, Sokal I, Verlinde CL, et al. Five members of a novel Ca(2+)-binding protein (CABP) subfamily with similarity to calmodulin. J Biol Chem. 2000;275:1247-1260.
33. Dhingra A, Lyubarsky A, Jiang M, et al. The light response of ON bipolar neurons requires G[alpha]o. J Neurosci. 2000;20:9053-9058.
34. Stoeckli ET, Landmesser LT. Axon guidance at choice points. Curr Opin Neurobiol. 1998;8:73-79
35. Bjartmar L, Huberman AD, Ullian EM, et al. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci. 2006;26:6269-6281.
36. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wassle H. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci. 1998;18:10136-10149.
37. Fujita T, Maturana AD, Ikuta J, et al. Axonal guidance protein FEZ1 associates with tubulin and kinesin motor protein to transport mitochondria in neurites of NGF-stimulated PC12 cells. Biochem Biophys Res Commun. 2007;361:605-610.
38. Chen C, Li M, Chai H, Yang H, Fisher WE, Yao Q. Roles of neuropilins in neuronal development, angiogenesis, and cancers. World J Surg. 2005;29:271-275.
39. Pellet-Many C, Frankel P, Jia H, Zachary I. Neuropilins: structure, function and role in disease. Biochem J. 2008;411:211-226.
40. Deleyrolle LP, Reynolds BA. Isolation, expansion, and differentiation of adult mammalian neural stem and progenitor cells using the neurosphere assay. Methods Mol Biol. 2009;549:91-101.
41. Reynolds BA, Tetzlaff W, Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci. 1992;12:4565-4574.
42. Monnin J, Morand-Villeneuve N, Michel G, Hicks D, Versaux-Botteri C. Production of neurospheres from mammalian Müller cells in culture. Neurosci Lett. 2007;421:22-26.
43. Todorova MG, Soria B, Quesada I. Gap junctional intercellular communication is required to maintain embryonic stem cells in a non-differentiated and proliferative state. J Cell Physiol. 2008;214: 354-362.
44. Duval N, Gomes D, Calaora V, Calabrese A, Meda P, Bruzzone R. Cell coupling and Cx43 expression in embryonic mouse neural progenitor cells. J Cell Sci. 2002;115:3241-3251.
45. Trimarchi JM, Stadler MB, Cepko CL. Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS ONE. 2008;3:e1588.
46. Blackshaw S, Harpavat S, Trimarchi J, et al. Genomic analysis of mouse retinal development. PLoS Biol. 2004;2:E247.
47. Livesey FJ, Young TL, Cepko CL. An analysis of the gene expression program of mammalian neural progenitor cells. Proc Natl Acad Sci U S A. 2004;101:1374-1379.
48. Bazan E, Alonso FJ, Redondo C, et al. In vitro and in vivo characterization of neural stem cells. Histol Histopathol. 2004;19:1261-1275.
49. Zhang L, Mathers PH, Jamrich M. Function of rx, but not pax6, is essential for the formation of retinal progenitor cells in mice. Genesis. 2000;28:135-142.
50. Roesch K, Jadhav AP, Trimarchi JM, et al. The transcriptome of retinal Müller glial cells. J Comp Neurol. 2008;509:225-238.
51. Fischer AJ, Reh TA. Potential of Müller glia to become neurogenic retinal progenitor cells. Glia. 2003;43:70-76.
52. Lin YP, Ouchi Y, Satoh S, Watanabe S. Sox2 plays a role in the induction of amacrine and Müller glial cells in mouse retinal progenitor cells. Invest Ophthalmol Vis Sci. 2009;50:68-74.
53. Calinescu AA, Vihtelic TS, Hyde DR, Hitchcock PF. Cellular expression of midkine-a and midkine-b during retinal development and photoreceptor regeneration in zebrafish. J Comp Neurol. 2009;514:1-10.
54. Dee CT, Hirst CS, Shih YH, Tripathi VB, Patient RK, Scotting PJ. Sox3 regulates both neural fate and differentiation in the zebrafish ectoderm. Dev Biol. 2008;320:289-301.
55. Li H, Radford JC, Ragusa MJ, et al. Transcription factor MEF2C influences neural stem/progenitor cell differentiation and maturation in vivo. Proc Natl Acad Sci U S A. 2008;105:9397-9402.
56. Hocking JC, Hehr CL, Chang RY, Johnston J, McFarlane S. TGFbeta ligands promote the initiation of retinal ganglion cell dendrites in vitro and in vivo. Mol Cell Neurosci. 2008;37:247-260.
57. Kerrison JB, Lewis RN, Otteson DC, Zack DJ. Bone morphogenetic proteins promote neurite outgrowth in retinal ganglion cells. Mol Vis. 2005;11:208-215.
58. Yanagisawa H, Komuta Y, Kawano H, Toyoda M, Sango K. Pleiotrophin induces neurite outgrowth and upregulates growth-associated protein (GAP)-43 mRNA through the ALK/GSK3beta/betacatenin signaling in developing mouse neurons. Neurosci Res. 2009;66:111-116.
59. Amaratunga A, Abraham CR, Edwards RB, Sandell JH, Schreiber BM, Fine RE. Apolipoprotein E is synthesized in the retina by Müller glial cells, secreted into the vitreous, and rapidly transported into the optic nerve by retinal ganglion cells. J Biol Chem. 1996;271:5628-5632.
60. Rogers JT, Weeber EJ. Reelin and apoE actions on signal transduction, synaptic function and memory formation. Neuron Glia Biol. 2008;4:259-270.
61. Fletcher EL, Hack I, Brandstatter JH, Wassle H. Synaptic localization of NMDA receptor subunits in the rat retina. J Comp Neurol. 2000;420:98-112.
62. Hennig AK, Peng GH, Chen S. Regulation of photoreceptor gene expression by Crx-associated transcription factor network. Brain Res. 2008;1192:114-133.
63. Chen CK. Recoverin and rhodopsin kinase. Adv Exp Med Biol. 2002;514:101-107.
64. Furukawa T, Morrow EM, Li T, Davis FC, Cepko CL. Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat Genet. 1999;23:466-470.
65. 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.
66. Ng L, Hurley JB, Dierks B, et al. A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet. 2001;27:94-98.
67. Wan J, Zheng H, Chen ZL, Xiao HL, Shen ZJ, Zhou GM. Preferential regeneration of photoreceptor from Müller glia after retinal degeneration in adult rat. Vision Res. 2008;48:223-234.
68. Steedman M, Tao S, Klassen H, Desai T. Enhanced differentiation of retinal progenitor cells using microfabricated topographical cues. Biomed Microdevices. 12:363-369