Proliferation of the ciliary epithelium with retinal neuronal and photoreceptor cell differentiation in human eyes with retinal detachment and proliferative vitreoretinopathy

Graefe's Archive for Clinical and Experimental Ophthalmology

Volumn 250, Issue 3, 2012, Pages 409-423

  Ducournau, Yvette ^a   Boscher, Claude ^b   Adelman, Ron A ^c   Guillaubey, Colette ^d   Schmidt Morand, Didier ^e   Mosnier, Jean François ^a   Ducournau, Didier ^a  

^a CHU de Nantes   (France)

^b AMERICAN HOSPITAL OF PARIS   (France)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Institut D'Anatomie Pathologie du Forez   (France)

^e LUNAM UNIVERSITÉ   (France)

Author keywords

Ciliary margin; Endoscopic vitreoretinal surgery; Proliferative vitreoretinopathy; Retinal detachment; Retinal progenitor cells; Retinal transplantation

Indexed keywords

CD133 ANTIBODY; EOSIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN ANTIBODY; HEMATOXYLIN; KI67 ANTIBODY; NSE ANTIBODY; PARAFFIN; PROTEIN ANTIBODY; RHODOPSIN ANTIBODY; UNCLASSIFIED DRUG; CD133 ANTIGEN; EGFR PROTEIN, HUMAN; ENOLASE; GLYCOPROTEIN; KI 67 ANTIGEN; LEUKOCYTE ANTIGEN; PEPTIDE; RHODOPSIN;

ADULT; ARTICLE; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CILIARY BODY EPITHELIUM; CONTROLLED STUDY; EMBEDDING; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY; NERVE CELL DIFFERENTIATION; ORBIT TUMOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RETINA DETACHMENT; RETINA NERVE CELL; RETROSPECTIVE STUDY; VITREORETINOPATHY; VITREOUS BODY; CELL DIFFERENTIATION; CELL MOTION; CILIARY BODY; ENZYME IMMUNOASSAY; METABOLISM; MIDDLE AGED; PATHOLOGY; PIGMENT EPITHELIUM;

ADULT; ANTIGENS, CD; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CILIARY BODY; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; KI-67 ANTIGEN; MALE; MIDDLE AGED; PARAFFIN EMBEDDING; PEPTIDES; PHOSPHOPYRUVATE HYDRATASE; PHOTORECEPTOR CELLS, VERTEBRATE; PIGMENT EPITHELIUM OF EYE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RETINAL DETACHMENT; RETINAL NEURONS; RHODOPSIN; VITREORETINOPATHY, PROLIFERATIVE;

EID: 84861118738     PISSN: 0721832X     EISSN: 1435702X     Source Type: Journal    
DOI: 10.1007/s00417-011-1797-3     Document Type: Article

References (55)

1. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ, McInnes RR, Van der Kooy D (2000) Retinal stem cells in the adult mammalian eye. Science 287: 2032-2036
2. Ahmad I, Tang L, Pham H (2000) Identification of neural progenitors in the adult mammalian eye. Biochem Biophys Res Commun 270: 517-521
3. Fischer AJ, Reh TA (2000) Indentification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev Biol 220: 197-210
4. Fischer AJ, Hendrickson A, Reh TA (2001) Immunocytochemical characterization of cysts in the peripheral retina and pars plana of the adult primate. Invest Ophthalmol Vis Sci 42: 3256-3263
5. Moshiri A, Reh TA (2004) Persistent progenitors at the retinal margin of ptc+/- mice. J Neurosci 24: 229-237
6. Das AV, James J, Rahnenführer J, Thoreson WB, Bhattacharya S, Zhao X, Ahmad I (2005) Retinal properties and potential of the adult mammalian ciliary epithelium stem cells. Vision Research 45: 1653-1666
7. Inoue Y, Yanagi Y, Tamaki Y, Uchida S, Kawase Y, Araie M, Okochi H (2005) Clonogenic analysis of ciliary epithelial derived retinal progenitor cells in rabbits. Exp Eye Res 81(4): 437-445
8. Gu P, Harwood LJ, Zhang X, Wylie M, Curry WJ, Cogliati T (2007) Isolation of retinal progenitor and stem cells from the porcine eye. Mol Vis 13: 1045-1057
9. Hollyfield JG (1968) Differential addition of cells to the retina in Rana pipiens tadpoles. Dev Biol 18: 163-179
10. Coles BL, Angénieux B, Inoue T, Del Rio K, Spence JR, McInnes RR, Arsenijevic Y, Van der Kooy D (2004) Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA 101(44): 15772-15777
11. Mayer EJ, Carter DA, Ren Y, Hugues EH, Rice CM, Halfpenny CA, Scolding NJ, Dick AD (2005) Neural progenitor cells from postmortem adult human retina. Br J Ophthalmol 89(1): 102-106
12. Coles BL, Horsford DJ, Mclnnes R, Van der Kooy D (2006) Loss of retinal progenitor cells leads to an increase in the retinal stem cell population in vivo. Eur J Neurosci 23: 75-82
13. Klassen H, Zjaeian B, Kirov I, Young MJ, Schwartz PH (2007) Isolation of retinal progenitor cells from postmortem human tissue and comparison with autologous brain progenitors. J Neurosci Res 77: 334-343
14. Xu H, Drina D, Sta I, Kielczewski JL, Valenta DF, Pease ME, Zack DJ, Quigley HA (2007) Characteristics of progenitor cells derived from adult ciliary body in mouse, rat, and human eyes. Invest Ophthalmol Vis Sci 48: 1674-1682
15. MacNeil A, Pearson RA, MacLaren RE, Smith AJ, Sowden JC, Ali RR (2007) Comparative analysis of progenitor cells isolated from the iris, pars plana, and ciliary body of the adult porcine eye. Stem Cells 10: 2430-2438
16. Wetts R, Serbedzija GN, Fraser SE (1989) Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev Biol 136: 254-263
17. Perron M, Kanekar S, Vetter ML, Harris WA (1998) The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev Biol 199: 185-200
18. MoeM, Kolberg R, Sandberg C, Vilk-Mo E, Olstorn H, Varghese M, Langmoen I, Nicolaissen B (2009) A comparison of epithelial and neural properties in progenitor cells derived from the adult human ciliary body and brain. Experimental Eye Research: 88(1): 30-38
19. Cicero SA, Johnson D, Reyntjens S, Frase S, Connell S, Chow LML, Baker SJ, Sorrentino BP, Dyer MA (2009) Cells previously identified as retinal stem cells are pigmented epithelial cells. PNAS 106(16): 6685-6690
20. Bathia B, Singhal S, Lawrence J, Khaw P, Limb A (2009) Distribution Of Muller stem cells within the neural retina: evidence for the existence of a ciliary margin-like zone in the adult human eye. Exp Eye Res 89: 373-382
21. Boscher C (2007) Endoscopy. In: Kuhn F (ed) Ocular traumatology. Springer, Berlin, pp 473-484, section II, chapter 2.20
22. Boscher C (2001) Endoscopy for anterior proliferative vitreoretinopathy. AAO subspecialty day, Retina: A Retina Odyssey, pp 151-157
23. Bauer N, Fonseca AV, Florek M, Freund D, Jászai J, Bornhäuser M, Fargeas CA, Corbeil D (2008) New insights into the cell biology of hematopoietic progenitors by studying Prominin-1 (CD133). Cells Tissues Organs 188(1-2): 127-138
24. Mizrak D, Brittan M, Alison MR (2008) CD133: molecule of the moment. J Pathol 214(1): 3-9
25. Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti JC, Hutnick L, Krueger RC Jr, Fan G, de Vellis J, Sun YE (2008) CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA 105(3): 1026-1031
26. Carter DA, Dick AD, Mayer EJ (2009) CD 133+ adult human retinal cells remain undifferentiated in Leukaemia Inhibitory Factor (LIF). BMC Opthtalmology 9: 1. doi: 10.1186/1471-2415-9-1
27. Weigmann A, Corbeil D, Hellwig A, Huttner WB (1997) Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalem- mal protrusions of non-epithelial cells. Proc Natl Acad Sci USA 94: 12425-12430
28. Simmons PJ, Peault B, Buck DW, Huttner WB (2000) The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J Biol Chem 275: 5512-5520
29. Corbeil D, Röper K, Fargeas CA, Joester A, Huttner WB (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2: 82-91
30. Fargeas CA, Joester A, Missol-Kolka E, Hellwig A, Huttner WB, Denis Corbeil D (2004) Identification of novel Prominin-1/CD133 splice variants with alternative C-termini and their expression in epididymis and testis. Journal of Cell Science 117: 4301-4311
31. Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC, Bridges RJ, Kumaramanickavel G, John S, Nancarrow D, Röper K, Weigmann A, Huttner WB, Denton MJ (2000) A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 9: 27-34
32. Sun Y, Kong W, Falk A, Hu J, Zhou L, Pollard S, Smith A (2009) CD133 (Prominin) negative human neural stem cells are clonogenic and tripotent. PLoS One 4(5): e5498, Epub 2009 May 11
33. Fischer AJ, Reh TA (2001) Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 4: 247-252
34. Fischer AJ, McGuire CR, Dierks BD, Reh TA (2002) Insulin and fibroblast growth factor 2 activate a neurogenic program in Muller glia of the chicken retina. J Neurosci 22: 9387-9398
35. Wan J, Zheng H, Xiao H, She ZJ, Zhou GM (2007) Sonic hedgehog promotes stem-cell potential of Müller glia in the mammalian retina. Biochem Biophys Res Commun 363(2): 347-354
36. Bernados RL, Barthel LK, Meyers JR, Raymond PA (2007) Latestage neuronal progenitors in the retina are radial müller glia that function as retinal stem cells. J Neurosci 27(26): 7028-7040
37. Monnin J, Morand-Villeneuve N, Michel G, Hicks D, Versaux- Botteri C (2007) Production of neurospheres from mammalian Müller cells in culture. Neurosci Lett 421(1): 22-26
38. Lawrence JM, Singhal S, Bhatia B, Keegan DJ, Reh TA, Luthert PJ, Khaw PT, Limb GA (2007) MIO-M1 cells and similar muller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells 25(8): 2033-2043
39. Draberova E, Del Valle L, Gordon J, Markova V, Smejkalova B, Bertrand L, de Chadarevian JP, Agamanolis DP, Legido A, Khalili K, Dráber P, Katsetos C (2008) Class III beta-tubulin is constitutively coexpressed with glial fibrillary acidic protein and nestin in midgestational human fetal astrocytes: implications for phenotypic identity. J Neuropathol Exp Neurol 67(4): 341-354
40. Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult sub-ventricular zone. J Neurosci 22: 629-634
41. Zhao X, Das AV, Soto-Leon F, Ahmad I (2005) Growth factorresponsive progenitors in the postnatal mammalian retina. Dev Dyn 232(2): 349-358
42. Rapaport DH, Wong LL, Wood ED, Yasumura D, La Vail MM (2004) Timing and topography of cell genesis in the rat retina. J Comp Neurol 474(2): 304-324
43. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444 (7116): 203-207
44. Lamba DA, Karl MO, Ware CB, Reh TA (2006) Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc Natl Acad Sci USA 103: 12769-12774
45. Martins RAP, Pearson RA (2008) Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res 1192: 37-60
46. McFarlane S, Zuber ME, Holt CE (1998) A role for the fibroblast growth factor receptor in cell fate decisions in the developing vertebrate retina. Development 125(20): 3967-3975
47. Fischer AJ, Reh TA (2003) Growth factors induce neurogenesis in the ciliary body. Dev Biol 259: 225-240
48. Giordano F, De Marzo A, Vetrini F, Marigo V (2007) Fibroblast growth factor and epidermal growth factor differently affect differentiation of murine retinal stem cells in vitro. Mol Vis 2(13): 1842-1850
49. Reh TA, Tully T (1986) Regulation of Tyrosine hydroxylasecontaining amacrine cell number in larval frog retina. Dev Biol 114: 463-469
50. Ooto S, Akagi T, Kageyam R, Mandai M, Honda Y, Takahasi M (2004) Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci USA 101: 13654-13659
51. Nickerson PE, Emsley JG, Myers T, Clarke DB (2007) Proliferation and expression of progenitor and mature retinal phenotypes in the adult mammalian ciliary body after retinal ganglion cell injury. Invest Ophthalmol Vis Sci 48(11): 5266-5275
52. Nishiguchi KM, Kaneko H, Nakamura M, Kachi S, Terasaki H (2008) Identification of photoreceptor precursors in the pars plana during ocular development and after retinal injury. Invest Ophthalmol Vis Sci 49(1): 422-428
53. Jens FK, Kiilgaard J, Prause U (2007) Subretinal posterior pole injury induces selective proliferation of RPE cells in the periphery in vivo studies in pigs. Invest Ophthalmol Vis Sci 48(1): 355-360
54. Moe M, Varghese M, Danilov A, Westerlund U, Ram-Pettersen J, Brundin L, Svensson M, Berg-Johnsen J, Langmoen I (2005) Multipotent progenitor cells from the adult human brain: neurophysiological differentiation to mature neurons. Brain 128: 2189-2199
55. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M (2006) Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 129(2): 490-502