Human müller glia with stem cell characteristics differentiate into retinal ganglion cell (RGC) precursors in vitro and partially restore RGC function in vivo following transplantation

Stem Cells Translational Medicine

Volumn 1, Issue 3, 2012, Pages 188-199

  Singhal, Shweta ^a   Bhatia, Bhairavi ^a   Jayaram, Hari ^a   Becker, Silke ^a   Jones, Megan F ^a   Cottrill, Phillippa B ^a   Khaw, Peng T ^a   Salt, Thomas E ^b   Astrid Limb, G ^a  

^a Division of Pharmacology and Therapeutics   (United Kingdom)

^b MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

Adult stem cells; Cell transplantation; Differentiation; Tissue specific stem cells

Indexed keywords

AZATHIOPRINE; CALCIUM ION; CYCLOSPORIN A; FIBROBLAST GROWTH FACTOR 2; GAMMA SECRETASE INHIBITOR; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; N METHYL DEXTRO ASPARTIC ACID; NEUROTRANSMITTER; NOTCH RECEPTOR; PHENYLEPHRINE; PREDNISOLONE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR POU4F2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL TRANSPLANTATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPORATION; ELECTRORETINOGRAPHY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GLIA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MUELLER CELL; NEURITE; NONHUMAN; PROTEIN EXPRESSION; RAT; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME LAPSE IMAGING; WESTERN BLOTTING; ADULT; ANIMAL; CELL MOTION; CYTOLOGY; GENETICS; GLIA; METABOLISM; PHYSIOLOGY; REGENERATION; RETINA NERVE CELL; STEM CELL; STEM CELL TRANSPLANTATION;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; ELECTRORETINOGRAPHY; GREEN FLUORESCENT PROTEINS; HUMANS; NEURITES; NEUROGLIA; RATS; REGENERATION; RETINAL GANGLION CELLS; RETINAL NEURONS; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSCRIPTION FACTOR BRN-3B;

EID: 84866088266     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2011-0005     Document Type: Article

References (44)

1. Raymond PA, Barthel LK, Bernardos RL et al. Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol 2006;6:36.
2. Karl MO, Hayes S, Nelson BR et al. Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A 2008;105:19508-19513.
3. Randlett O, Norden C, Harris WA. The vertebrate retina: A model for neuronal polarization in vivo. Dev Neurobiol 2010.
4. Dahlmann-Noor A, Vijay S, Jayaram H et al. Current approaches and future prospects for stem cell rescue and regeneration of the retina and optic nerve. Can J Ophthalmol 2010;45: 333-341.
5. 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.
6. Rapaport DH, Dorsky RI. Inductive competence, its significance in retinal cell fate determination and a role for Delta-Notch signaling. Semin Cell Dev Biol 1998;9:241-247.
7. MacLaren RE, Pearson RA, MacNeil A et al. Retinal repair by transplantation of photoreceptor precursors. Nature 2006;444:203-207.
8. Karlstetter M, Ebert S, Langmann T. Microglia in the healthy and degenerating retina: Insights from novel mouse models. Immunobiology 2010;215:685-691.
9. Sellés-Navarro I, Ellezam B, Fajardo R et al. Retinal ganglion cell and nonneuronal cell responses to a microcrush lesion of adult rat optic nerve. Exp Neurol 2001;167:282-289.
10. Singhal S, Lawrence JM, Bhatia B et al. Chondroitin sulfate proteoglycans and microglia prevent migration and integration of grafted Müller stem cells into degenerating retina. STEM CELLS 2008;26:1074-1082.
11. Xiang M, Zhou L, Nathans J. Similarities and differences among inner retinal neurons revealed by the expression of reporter transgenes controlled by Brn-3a, Brn-3b, and Brn-3c promotor sequences. Vis Neurosci 1996;13: 955-962.
12. Mao W, Yan RT, Wang SZ. Reprogramming chick RPE progeny cells to differentiate towards retinal neurons by ash1. Mol Vis 2008; 14:2309-2320.
13. Bui BV, Edmunds B, Cioffi GA et al. The gradient of retinal functional changes during acute intraocular pressure elevation. Invest Ophthalmol Vis Sci 2005;46:202-213.
14. Bui BV, Fortune B. Ganglion cell contributions to the rat full-field electroretinogram. J Physiol 2004;555:153-173.
15. Xiang M. Requirement for Brn-3b in early differentiation of postmitotic retinal ganglion cell precursors. Dev Biol 1998;197: 155-169.
16. Liu W, Khare SL, Liang X et al. All Brn3 genes can promote retinal ganglion cell differentiation in the chick. Development 2000;127: 3237-3247.
17. Pan L, Deng M, Xie X et al. ISL1 and BRN3B co-regulate the differentiation of murine retinal ganglion cells. Development 2008; 135:1981-1990.
18. Ekström P, Johansson K. Differentiation of ganglion cells and amacrine cells in the rat retina: Correlation with expression of HuC/D and GAP-43 proteins. Brain Res Dev Brain Res 2003;145:1-8.
19. Yang HJ, Silva AO, Koyano-Nakagawa N et al. Progenitor cell maturation in the developing vertebrate retina. Dev Dyn 2009;238: 2823-2836.
20. Gan L, Wang SW, Huang Z et al. POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev Biol 1999; 210:469-480.
21. Yang Z, Ding K, Pan L et al. Math5 determines the competence state of retinal ganglion cell progenitors. Dev Biol 2003;264: 240-254.
22. Lamba DA, Karl MO, Ware CB et al. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc Natl Acad Sci U S A 2006;103:12769-12774.
23. Puro DG, Yuan JP, Sucher NJ. Activation of NMDA receptor-channels in human retinal Müller glial cells inhibits inward-rectifying potassium currents. Vis Neurosci 1996;13: 319-326.
24. Limb GA, Salt TE, Munro PM et al. In vitro characterization of a spontaneously immortalized human Müller cell line (MIO-M1). Invest Ophthalmol Vis Sci 2002;43:864-869.
25. Kubrusly RC, da Cunha MC, Reis RA et al. Expression of functional receptors and transmitter enzymes in cultured Müller cells. Brain Res 2005;1038:141-149.
26. Matter JM, Matter-Sadzinski L, Ballivet M. Activity of the 3 nicotinic receptor promoter is a marker of neuron fate determination during retina development. J Neurosci 1995;15:5919-5928.
27. Pearson R, Catsicas M, Becker D et al. Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J Neurosci 2002;22: 7569-7579.
28. Wakakura M, Utsunomiya-Kawasaki I, Ishikawa S. Rapid increase in cytosolic calcium ion concentration mediated by acetylcholine receptors in cultured retinal neurons and Müller cells. Graefes Arch Clin Exp Ophthalmol 1998;236:934-939.
29. Masland RH, Ames A 3rd. Responses to acetylcholine of ganglion cells in an isolated mammalian retina. J Neurophysiol 1976;39: 1220-1235.
30. Strang CE, Amthor FR, Keyser KT. Rabbit retinal ganglion cell responses to nicotine can be mediated by 2-containing nicotinic acetylcholine receptors. Vis Neurosci 2003;20:651-662.
31. Tsutsui-Kimura I, Ohmura Y, Izumi T et al. Endogenous acetylcholine modulates impulsive action via 4 2nicotinicacetylcholinere-ceptors in rats. Eur J Pharmacol 2010;641:148-153.
32. Aoki H, Hara A, Niwa M et al. An in vitro mouse model for retinal ganglion cell replacement therapy using eye-like structures differentiated from ES cells. Exp Eye Res 2007;84: 868-875.
33. Lam TT, Abler AS, Kwong JM et al. N-Methyl-D-aspartate (NMDA)-induced apopto-sis in rat retina. Invest Ophthalmol Vis Sci 1999; 40:2391-2397.
34. Kelly CM, Precious SV, Scherf C et al. Neonatal desensitization allows long-term survival of neural xenotransplants without immunosuppression. Nat Methods 2009;6:271-273.
35. Imayoshi I, Sakamoto M, Yamaguchi M et al. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 2010;30: 3489-3498.
36. Ronchini C, Capobianco AJ. Induction of cyclin D1 transcription and CDK2 activity by Notch(ic): Implication for cell cycle disruption in transformation by Notch(ic). Mol Cell Biol 2001;21:5925-5934.
37. Austin CP, Feldman DE, Ida JA Jr. et al. Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 1995;121:3637-3650.
38. Nelson BR, Gumuscu B, Hartman BH et al. Notch activity is downregulated just prior to retinal ganglion cell differentiation. Dev Neurosci 2006;28:128-141.
39. Bao ZZ, Cepko CL. The expression and function of Notch pathway genes in the developing rat eye. J Neurosci 1997;17:1425-1434.
40. Cicero SA, Johnson D, Reyntjens S et al. Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proc Natl Acad Sci U S A 2009;106:6685-6690.
41. Newman E, Reichenbach A. The Müller cell: A functional element of the retina. Trends Neurosci 1996;19:307-312.
42. Atluri P, Fleck MW, Shen Q et al. Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev Biol 2001;240:143-156.
43. Lecchi M, McIntosh JM, Bertrand S et al. Functional properties of neuronal nicotinic acetylcholine receptors in the chick retina during development. Eur J Neurosci 2005;21: 3182-3188.
44. Briggman KL, Helmstaedter M, Denk W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 2011;471:183-188.