Pigment epithelial cells isolated from human peripheral iridectomies have limited properties of retinal stem cells

Acta Ophthalmologica

Volumn 89, Issue 8, 2011, Pages

  Frøen, Rebecca C ^a   Johnsen, Erik O ^a   Petrovski, Goran ^b   Berényi, Erika ^b   Facskõ, Andrea ^b   Berta, András ^b   Nicolaissen, Bjørn ^a   Moe, Morten C ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

adult human; ciliary body; iris pigment epithelium; peripheral iridectomy; progenitor cell; retinal stem cell

Indexed keywords

BETA3 TUBULIN; CLAUDIN; CYTOKERATIN 19; MEMBRANE PROTEIN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; RHODOPSIN; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CILIARY BODY EPITHELIUM; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; IRIDECTOMY; MELANOSOME; MONOLAYER CULTURE; NERVE CELL DIFFERENTIATION; PIGMENT CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CELL; RETINA STEM CELL; STEM CELL;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BIOLOGICAL MARKERS; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; CILIARY BODY; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLAUCOMA; HUMANS; IRIDECTOMY; IRIS; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; PIGMENT EPITHELIUM OF EYE; RETINAL PIGMENT EPITHELIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 82155167663     PISSN: 1755375X     EISSN: 17553768     Source Type: Journal    
DOI: 10.1111/j.1755-3768.2011.02198.x     Document Type: Article

References (49)

1. Abe T, Yoshida M, Yoshioka Y, Wakusawa R, Tokita-Ishikawa Y, Seto H, Tamai M, &, Nishida K, (2007): Iris pigment epithelial cell transplantation for degenerative retinal diseases. Prog Retin Eye Res 26: 302-321. (Pubitemid 46498799)
2. Akagi T, Akita J, Haruta M, et al., (2005): Iris-derived cells from adult rodents and primates adopt photoreceptor-specific phenotypes. Invest Ophthalmol Vis Sci 46: 3411-3419. (Pubitemid 44264332)
3. Asami M, Sun G, Yamaguchi M, &, Kosaka M, (2007): Multipotent cells from mammalian iris pigment epithelium. Dev Biol 304: 433-446. (Pubitemid 46399698)
4. Aymerich MS, Alberdi EM, Martinez A, &, Becerra SP, (2001): Evidence for pigment epithelium-derived factor receptors in the neural retina. Invest Ophthalmol Vis Sci 42: 3287-3293. (Pubitemid 33740692)
5. Belecky-Adams T, Tomarev S, Li HS, Ploder L, McInnes RR, Sundin O, &, Adler R, (1997): Pax-6, Prox 1, and Chx10 homeobox gene expression correlates with phenotypic fate of retinal precursor cells. Invest Ophthalmol Vis Sci 38: 1293-1303. (Pubitemid 27278548)
6. Bhatia B, Singhal S, Lawrence JM, Khaw PT, &, Limb GA, (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.
7. Bilak MM, Becerra SP, Vincent AM, Moss BH, Aymerich MS, &, Kuncl RW, (2002): Identification of the neuroprotective molecular region of pigment epithelium-derived factor and its binding sites on motor neurons. J Neurosci 22: 9378-9386. (Pubitemid 35356181)
8. Carter DA, Mayer EJ, &, Dick AD, (2007): The effect of postmortem time, donor age and sex on the generation of neurospheres from adult human retina. Br J Ophthalmol 91: 1216-1218. (Pubitemid 47344902)
9. Cicero SA, Johnson D, Reyntjens S, et al., (2009): Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proc Natl Acad Sci U S A 106: 6685-6690.
10. Coles BL, Angenieux B, Inoue T, Del Rio-Tsonis 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 U S A 101: 15772-15777. (Pubitemid 39473563)
11. Das AV, James J, Rahnenfuhrer J, Thoreson WB, Bhattacharya S, Zhao X, &, Ahmad I, (2005): Retinal properties and potential of the adult mammalian ciliary epithelium stem cells. Vision Res 45: 1653-1666. (Pubitemid 40403826)
12. Das AV, Mallya KB, Zhao X, Ahmad F, Bhattacharya S, Thoreson WB, Hegde GV, &, Ahmad I, (2006): Neural stem cell properties of Muller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 299: 283-302. (Pubitemid 44550105)
13. Davis N, Yoffe C, Raviv S, et al., (2009): Pax6 dosage requirements in iris and ciliary body differentiation. Dev Biol 333: 132-142.
14. Dawson DW, Volpert OV, Gillis P, Crawford SE, Xu H, Benedict W, &, Bouck NP, (1999): Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285: 245-248. (Pubitemid 29329995)
15. Fischer AJ, Zelinka C, &, Scott MA, (2010): Heterogeneity of glia in the retina and optic nerve of birds and mammals. PLoS ONE 5: e10774.
16. Furuse M, Fujita K, Hiiragi T, Fujimoto K, &, Tsukita S, (1998): Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141: 1539-1550. (Pubitemid 28309169)
17. Gage FH, (2000): Mammalian neural stem cells. Science 287: 1433-1438. (Pubitemid 30127128)
18. Gualdoni S, Baron M, Lakowski J, Decembrini S, Smith AJ, Pearson RA, Ali RR, &, Sowden JC, (2010): Adult ciliary epithelial cells, previously identified as retinal stem cells with potential for retinal repair, fail to differentiate into new rod photoreceptors. Stem Cells 28: 1048-1059.
19. Haruta M, Kosaka M, Kanegae Y, et al., (2001): Induction of photoreceptor-specific phenotypes in adult mammalian iris tissue. Nat Neurosci 4: 1163-1164. (Pubitemid 33135615)
20. Inoue T, Coles BL, Dorval K, et al., (2010): Maximizing functional photoreceptor differentiation from adult human retinal stem cells. Stem Cells 28: 489-500.
21. Jomary C, Jones SE, &, Lotery AJ, (2010): Generation of light-sensitive photoreceptor phenotypes by genetic modification of human adult ocular stem cells with Crx. Invest Ophthalmol Vis Sci 51: 1181-1189.
22. Klassen H, Sakaguchi DS, &, Young MJ, (2004): Stem cells and retinal repair. Prog Retin Eye Res 23: 149-181. (Pubitemid 38496399)
23. Kohno R, Ikeda Y, Yonemitsu Y, et al., (2006): Sphere formation of ocular epithelial cells in the ciliary body is a reprogramming system for neural differentiation. Brain Res 1093: 54-70. (Pubitemid 43946398)
24. Lamba DA, McUsic A, Hirata RK, Wang PR, Russell D, &, Reh TA, (2010): Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PLoS ONE 5: e8763.
25. 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: 2033-2043. (Pubitemid 47258181)
26. Lendahl U, Zimmerman LB, &, McKay RD, (1990): CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
27. Liu IS, Chen JD, Ploder L, Vidgen D, van der Kooy D, Kalnins VI, &, McInnes RR, (1994): Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron 13: 377-393. (Pubitemid 24275095)
28. Livesey FJ, &, Cepko CL, (2001): Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2: 109-118. (Pubitemid 33673365)
29. MacLaren RE, Pearson RA, MacNeil A, et al., (2006): Retinal repair by transplantation of photoreceptor precursors. Nature 444: 203-207. (Pubitemid 44722060)
30. 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 25: 2430-2438. (Pubitemid 47582735)
31. Mannello F, &, Tonti GA, (2007): Concise review: no breakthroughs for human mesenchymal and embryonic stem cell culture: conditioned medium, feeder layer, or feeder-free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells 25: 1603-1609. (Pubitemid 47121836)
32. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, &, Gruss P, (2001): Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105: 43-55. (Pubitemid 32323915)
33. Mayer EJ, Carter DA, Ren Y, Hughes EH, Rice CM, Halfpenny CA, Scolding NJ, &, Dick AD, (2005): Neural progenitor cells from postmortem adult human retina. Br J Ophthalmol 89: 102-106. (Pubitemid 40040248)
34. Moe MC, Varghese M, Danilov AI, et al., (2005): Multipotent progenitor cells from the adult human brain: neurophysiological differentiation to mature neurons. Brain 128: 2189-2199. (Pubitemid 41253285)
35. Moe MC, Kolberg RS, Sandberg C, Vik-Mo E, Olstorn H, Varghese M, Langmoen IA, &, Nicolaissen B, (2009): A comparison of epithelial and neural properties in progenitor cells derived from the adult human ciliary body and brain. Exp Eye Res 88: 30-38.
36. Nakayama A, Nguyen MT, Chen CC, Opdecamp K, Hodgkinson CA, &, Arnheiter H, (1998): Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech Dev 70: 155-166. (Pubitemid 28116490)
37. Olstorn H, Moe MC, Roste GK, Bueters T, &, Langmoen IA, (2007): Transplantation of stem cells from the adult human brain to the adult rat brain. Neurosurgery 60: 1089-1098. discussion 1098-1089. (Pubitemid 46849857)
38. Perron M, &, Harris WA, (2000): Retinal stem cells in vertebrates. Bioessays 22: 685-688. (Pubitemid 30613299)
39. Reh TA, (2002): Neural stem cells: form and function. Nat Neurosci 5: 392-394. (Pubitemid 34454239)
40. Reynolds BA, &, Weiss S, (1992): Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
41. Rowan S, &, Cepko CL, (2004): Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev Biol 271: 388-402. (Pubitemid 38833669)
42. Schlotzer-Schrehardt U, &, Kruse FE, (2005): Identification and characterization of limbal stem cells. Exp Eye Res 81: 247-264. (Pubitemid 41208160)
43. Schraermeyer U, &, Heimann K, (1999): Current understanding on the role of retinal pigment epithelium and its pigmentation. Pigment Cell Res 12: 219-236. (Pubitemid 129686284)
44. Slettedal JK, Lyberg T, Ramstad H, Beraki K, &, Nicolaissen B, (2007): Regeneration of the epithelium in organ-cultured donor corneas with extended post-mortem time. Acta Ophthalmol Scand 85: 371-376. (Pubitemid 46901480)
45. Sun G, Asami M, Ohta H, Kosaka J, &, Kosaka M, (2006): Retinal stem/progenitor properties of iris pigment epithelial cells. Dev Biol 289: 243-252. (Pubitemid 41804102)
46. 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. (Pubitemid 30158683)
47. Xu H, Sta Iglesia DD, Kielczewski JL, Valenta DF, Pease ME, Zack DJ, &, Quigley HA, (2007a): Characteristics of progenitor cells derived from adult ciliary body in mouse, rat, and human eyes. Invest Ophthalmol Vis Sci 48: 1674-1682. (Pubitemid 351261353)
48. Xu S, Sunderland ME, Coles BL, et al., (2007b): The proliferation and expansion of retinal stem cells require functional Pax6. Dev Biol 304: 713-721. (Pubitemid 46527572)
49. Yamamoto N, Tanikawa A, &, Horiguchi M, (2010): Basic study of retinal stem/progenitor cell separation from mouse iris tissue. Med Mol Morphol 43: 139-144.