Müller glial cells induce stem cell properties in retinal progenitors in vitro and promote their further differentiation into photoreceptors

Journal of Neuroscience Research

Volumn 90, Issue 2, 2012, Pages 407-421

  Simón, María V ^a,b   De Genaro, Pablo ^a,b   Abrahan, Carolina E ^a,b   de los Santos, Beatriz ^a   Rotstein, Nora P ^a,b   Politi, Luis E ^a,b  

^a Instituto de Investigaciones Bioquimicas Bahia Blanca   (Argentina)

^b UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

Photoreceptor differentiation; Progenitors; Regeneration; Retina stem cells

Indexed keywords

CYCLIC GMP; GLUTAMIC ACID; OPSIN; PERIPHERIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; GLIA CELL; MUELLER CELL; NEWBORN; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RAT; RETINA DEVELOPMENT; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; PHOTORECEPTOR CELLS; RATS; RATS, WISTAR; RETINA; STEM CELLS;

EID: 83155175204     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22747     Document Type: Article

References (62)

1. Abrahan CE, Insua MF, Politi LE, German OL, Rotstein NP. 2009. Oxidative stress promotes proliferation and dedifferentiation of retina glial cells in vitro. J Neurosci Res 87: 964-977.
2. Adler R. 1982. Regulation of neurite growth in purified retina neuronal cultures: effects of PNPF, a substratum-bound, neurite-promoting factor. J Neurosci Res 8: 165-177.
3. Adler R, Hatlee M. 1989. Plasticity and differentiation of embryonic retinal cells after terminal mitosis. Science 243: 391-393.
4. Barbour B, Brew H, Attwell D. 1988. Electrogenic glutamate uptake in glial cells is activated by intracellular potassium. Nature 335: 433-435.
5. Barnstable CJ. 1980. Monoclonal antibodies which recognize different cell types in the rat retina. Nature 286: 231-235.
6. Bernardos RL, Barthel LK, Meyers JR, Raymond PA. 2007. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 27: 7028-7040.
7. Brew H, Attwell D. 1987. Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327: 707-709.
8. Cameron DA. 2000. Cellular proliferation and neurogenesis in the injured retina of adult zebrafish. Vis Neurosci 17: 789-797.
9. Capovilla M, Cervetto L, Torre V. 1982. Antagonism between steady light and phosphodiesterase inhibitors on the kinetics of rod photoresponses. Proc Natl Acad Sci U S A 79: 6698-6702.
10. Chen S, Wang QL, Nie Z, Sun H, Lennon G, Copeland NG, Gilbert DJ, Jenkins NA, Zack DJ. 1997. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19: 1017-1030.
11. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65: 1-105.
12. Das AV, Mallya KB, Zhao X, Ahmad F, Bhattacharya S, Thoreson WB, Hegde GV, Ahmad I. 2006. Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 299: 283-302.
13. Derouiche A. 1996. Possible role of the Müller cell in uptake and metabolism of glutamate in the mammalian outer retina. Vis Res 36: 3875-3878.
14. Fischer AJ, Reh TA. 2003. Potential of Müller glia to become neurogenic retinal progenitor cells. Glia 43: 70-76.
15. Fontaine V, Kinkl N, Sahel J, Dreyfus H, Hicks D. 1998. Survival of purified rat photoreceptors in vitro is stimulated directly by fibroblast growth factor-2. J Neurosci 18: 9662-9672.
16. Furukawa T, Morrow EM, Cepko CL. 1997. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91: 531-541.
17. Fykse EM, Fonnum F. 1996. Amino acid neurotransmission: dynamics of vesicular uptake. Neurochem Res 21: 1053-1060.
18. Garelli A, Rotstein NP, Politi LE. 2006. Docosahexaenoic acid promotes photoreceptor differentiation without altering Crx expression. Invest Ophthalmol Vis Sci 47: 3017-3027.
19. Harada T, Harada C, Kohsaka S, Wada E, Yoshida K, Ohno S, Mamada H, Tanaka K, Parada LF, Wada K. 2002. Microglia-Müller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci 22: 9228-9236.
20. Harada T, Harada C, Nakamura K, Quah HM, Okumura A, Namekata K, Saeki T, Aihara M, Yoshida H, Mitani A, Tanaka K. 2007. The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. J Clin Invest 117: 1763-1770.
21. Haynes T, Del Rio-Tsonis K. 2004. Retina repair, stem cells and beyond. Curr Neurovasc Res 1: 231-239.
22. Hicks D, Barnstable CJ. 1987. Different rhodopsin monoclonal antibodies reveal different binding patterns on developing and adult rat retina. J Histochem Cytochem 35: 1317-1328.
23. Hicks D, Courtois Y. 1990. The growth and behaviour of rat retinal Müller cells in vitro. 1. An improved method for isolation and culture. Exp Eye Res 51: 119-129.
24. Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND. 1991. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354: 522-525.
25. Hitchcock P, Ochocinska M, Sieh A, Otteson D. 2004. Persistent and injury-induced neurogenesis in the vertebrate retina. Prog Ret Eye Res 23: 183-194.
26. Ikegami Y, Mitsuda S, Araki M. 2002. Neural cell differentiation from retinal pigment epithelial cells of the newt: an organ culture model for the urodele retinal regeneration. J Neurobiol 50: 209-220.
27. Insua MF, Garelli A, Rotstein NP, German OL, Arias A, Politi LE. 2003. Cell cycle regulation in retinal progenitors by glia-derived neurotrophic factor and docosahexaenoic acid. Invest Ophthalmol Vis Sci 44: 2235-2244.
28. Insua MF, Simon MV, Garelli A, de Los SB, Rotstein NP, Politi LE. 2008. Trophic factors and neuronal interactions regulate the cell cycle and Pax6 expression in Müller stem cells. J Neurosci Res 86: 1459-1471.
29. Jomary C, Jones SE. 2008. Induction of functional photoreceptor phenotype by exogenous Crx expression in mouse retinal stem cells. Invest Ophthalmol Vis Sci 49: 429-437.
30. Kanai Y, Stelzner M, Nussberger S, Khawaja S, Hebert SC, Smith CP, Hediger MA. 1994. The neuronal and epithelial human high affinity glutamate transporter. Insights into structure and mechanism of transport. J Biol Chem 269: 20599-20606.
31. Karl MO, Reh TA. 2010. Regenerative medicine for retinal diseases: activating endogenous repair mechanisms. Trends Mol Med 16: 193-202.
32. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA. 2008. Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A 105: 19508-19513.
33. Kirn JR, Nottebohm F. 1993. Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 13: 1654-1663.
34. Kljavin IJ, Reh TA. 1991. Müller cells are a preferred substrate for in vitro neurite extension by rod photoreceptor cells. J Neurosci 11: 2985-2994.
35. Laemmli UK, Beguin F, Gujer-Kellenberger G. 1970. A factor preventing the major head protein of bacteriophage T4 from random aggregation. J Mol Biol 47: 69-85.
36. Liang L, Yan RT, Ma W, Zhang H, Wang SZ. 2006. Exploring RPE as a source of photoreceptors: differentiation and integration of transdifferentiating cells grafted into embryonic chick eyes. Invest Ophthalmol Vis Sci 47: 5066-5074.
37. Lolley RN, Farber DB, Rayborn ME, Hollyfield JG. 1977. Cyclic GMP accumulation causes degeneration of photoreceptor cells: simulation of an inherited disease. Science 196: 664-666.
38. Lolley RN, Craft CM, Lee RH. 1992. Photoreceptors of the retina and pinealocytes of the pineal gland share common components of signal transduction. Neurochem Res 17: 81-89.
39. Moore KA, Lemischka IR. 2006. Stem cells and their niches. Science 311: 1880-1885.
40. Naito S, Ueda T. 1983. Adenosine triphosphate-dependent uptake of glutamate into protein I-associated synaptic vesicles. J Biol Chem 258: 696-699.
41. Nickerson PE, Da SN, Myers T, Stevens K, Clarke DB. 2008. Neural progenitor potential in cultured Müller glia: effects of passaging and exogenous growth factor exposure. Brain Res 1230: 1-12.
42. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M. 2004. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 101: 13654-13659.
43. Poitry S, Poitry-Yamate C, Ueberfeld J, Macleish PR, Tsacopoulos M. 2000. Mechanisms of glutamate metabolic signaling in retinal glial (Müller) cells. J Neurosci 20: 1809-1821.
44. Poitry-Yamate CL, Poitry S, Tsacopoulos M. 1995. Lactate released by Müller glial cells is metabolized by photoreceptors from mammalian retina. J Neurosci 15: 5179-5191.
45. Politi LE, Adler R. 1986. Generation of enriched populations of cultured photoreceptor cells. Invest Ophthalmol Vis Sci 27: 656-665.
46. Politi L, Adler R. 1988. Selective failure of long-term survival of isolated photoreceptors from both homozygous and heterozygous rd (retinal degeneration) mice. Exp Eye Res 47: 269-282.
47. Politi LE, Bouzat C, los Santos EB, Barrantes FJ. 1996. Heterologous retinal cultured neurons and cell adhesion molecules induce clustering of acetylcholine receptors and polynucleation in mouse muscle BC3H-1 clonal cell line. J Neurosci Res 43: 639-651.
48. Politi LE, Rotstein NP, Carri NG. 2001. Effect of GDNF on neuroblast proliferation and photoreceptor survival: additive protection with docosahexaenoic acid. Invest Ophthalmol Vis Sci 42: 3008-3015.
49. Raymond PA, Reifler MJ, Rivlin PK. 1988. Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol 19: 431-463.
50. Reh TA, Fischer AJ. 2001. Stem cells in the vertebrate retina. Brain Behav Evol 58: 296-305.
51. Rotstein NP, Aveldano MI, Barrantes FJ, Politi LE. 1996. Docosahexaenoic acid is required for the survival of rat retinal photoreceptors in vitro. J Neurochem 66: 1851-1859.
52. Rotstein NP, Aveldano MI, Barrantes FJ, Roccamo AM, Politi LE. 1997. Apoptosis of retinal photoreceptors during development in vitro: protective effect of docosahexaenoic acid. J Neurochem 69: 504-513.
53. Rotstein NP, Politi LE, Aveldano MI. 1998. Docosahexaenoic acid promotes differentiation of developing photoreceptors in culture. Invest Ophthalmol Vis Sci 39: 2750-2758.
54. Sakaguchi DS, Janick LM, Reh TA. 1997. Basic fibroblast growth factor (FGF-2) induced transdifferentiation of retinal pigment epithelium: generation of retinal neurons and glia. Dev Dyn 209: 387-398.
55. Scadden DT. 2006. The stem-cell niche as an entity of action. Nature 441: 1075-1079.
56. Schmitt A, Asan E, Lesch KP, Kugler P. 2002. A splice variant of glutamate transporter GLT1/EAAT2 expressed in neurons: cloning and localization in rat nervous system. Neuroscience 109: 45-61.
57. Stenkamp DL, Cameron DA. 2002. Cellular pattern formation in the retina: retinal regeneration as a model system. Mol Vis 8: 280-293.
58. Tabb JS, Ueda T. 1991. Phylogenetic studies on the synaptic vesicle glutamate transport system. J Neurosci 11: 1822-1828.
59. Tackenberg MA, Tucker BA, Swift JS, Jiang C, Redenti S, Greenberg KP, Flannery JG, Reichenbach A, Young MJ. 2009. Müller cell activation, proliferation and migration following laser injury. Mol Vis 15: 1886-1896.
60. van der Kooy D, Weiss S. 2000. Why stem cells? Science 287: 1439-1441.
61. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
62. Vergara MN, Del Rio-Tsonis K. 2009. Retinal regeneration in the Xenopus laevis tadpole: a new model system. Mol Vis 15: 1000-1013.