Potential application of adult stem cells in retinal repair-challenge for regenerative medicine

Current Eye Research

Volumn 34, Issue 9, 2009, Pages 748-760

  MacHalińska, Anna ^a   Baumert, Bartłomiej ^a   Kuprjanowicz, Leszek ^a   Wiszniewska, Barbara ^a   Karczewicz, Danuta ^a   MacHaliński, Bogusław ^a  

^a POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

Adult stem cells; Bone marrow; Regeneration; Retina; Umbilical cord blood

Indexed keywords

LEUKEMIA INHIBITORY FACTOR; SCATTER FACTOR; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN;

ADULT STEM CELL; BONE MARROW; CELL DIFFERENTIATION; CELL ISOLATION; CELL MIGRATION; CELL POPULATION; CELL REGENERATION; CELL THERAPY; EMBRYO CELL; EX VIVO STUDY; EYE DISEASE; HUMAN; ORGAN DONOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; REGENERATIVE MEDICINE; RETINA; RETINA DEGENERATION; RETINA NEOVASCULARIZATION; RETINA NEUROEPITHELIAL LAYER; REVIEW; TISSUE; UMBILICAL CORD BLOOD; VISUAL DISORDER;

ADULT STEM CELLS; ANIMALS; CELL TRANSPLANTATION; HUMANS; REGENERATION; REGENERATIVE MEDICINE; RETINA; RETINAL DISEASES; TISSUE ENGINEERING;

EID: 70350657322     PISSN: 02713683     EISSN: 14602202     Source Type: Journal    
DOI: 10.1080/02713680903050592     Document Type: Review

References (97)

1. Papayannopoulou T, Lemischka I. Stem cell biology. In: Stamatoyannopoulos G, Majerus PW, Perlmutter RM, Vermus H, eds. The Molecular Basis of Blood Diseases. 3rd ed. Philadelphia: Saunders; 2001:8-25.
2. Ratajczak MZ, Zuba-Surma EK, Machalinski B, Kucia M. Bonemarrow- derived stem cells-Our key to longevity? J Appl Genet 2007;48:307-319.
3. Kucia M, Zhang PY, Wysoczynski M, Rezzoug F, Zuba-Surma E, Machalinski B, Majka M, Reca R, Ildstad S, Ratajczak J, Shields CB, Ratajczak MZ. Neural tissue-committed stem cells (TCSC) reside in the bonemarrow and aremobilized into the peripheral blood following stroke. Leukemia 2006;20:18-28.
4. Da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008;26:2287-2299.
5. Potten CS. Stem cells in gastrointestinal epithelium: Numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci. 1998;353:821-830.
6. Cotsarelis G, Kaur P, Dhouailly D, Hengge U, Bickenbach J. Epithelial stem cells in the skin: Definition, markers, localization and functions. Exp Dermatol. 1999;8:80-88.
7. Das AV, James J, Rahnenföuhrer J, ThoresonWB, Bhattacharya S, Zhao X, Ahmad I. Retinal properties and potential of the adult mammalian ciliary epithelium stem cells. Vis Res. 2005;45:1653-1666.
8. Coles BL, Anǵenieux B, Inoue T, Del Rio-Tsonis K, Spence JR, McInnes RR, Arsenijevic Y, van der Kooy D. Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA 2004;101:15772-15777.
9. Cai J, Rao M. Stem and precursor cells for transplant therapy. In: Halberstadt CR, Emerich DF, eds. Cellular Transplantation: From Laboratory to Clinic. London: Elsevier; 2007:29-42.
10. DasAV, MallyaKB, Zhao X,AhmadF, Bhattacharya S, Thoreson WB, Hegde GV, Ahmad I. Neural stem cell properties ofM̈uller glia in the mammalian retina: Regulation by Notch and Wnt signaling. Dev Biol. 2006;299:283-302.
11. Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E, Czajka R, Wojakowski W, Machalinski B, Ratajczak MZ. Morphological and molecular characterization of novel population of CXCR4+SSEA-1+Oct- 4+ very small embryonic-like cells purified from human cord blood-preliminary report. Leukemia 2007;21:297-303.
12. BeltramiAP, Cesselli D, Bergamin N, Marcon P, Rigo S, Puppato E, D'Aurizio F, Verardo R, Piazza S, Pignatelli A, Poz A, Baccarani U, Damiani D, Fanin R, Mariuzzi L, Finato N, Masolini P, Burelli S, Belluzzi O, Schneider C, Beltrami CA. Multipotent cells can be generated in vitro from several adult human organs (heart, liver, and bone marrow). Blood 2007;110:3438-3446.
13. Zuba-Surma EK, Kucia M, Wu W, Klich I, Lillard JW Jr, Ratajczak J, Ratajczak MZ. Very small embryonic-like stem cells are present in adult murine organs: ImageStream-based morphological analysis and distribution studies.Cytometry A 2008;73A:1116-1127.
14. Ratajczak MZ, Zuba-Surma EK, Machalinski B, Ratajczak J, KuciaM. Very small embryonic-like (VSEL) stem cells: Purification from adult organs, characterization, and biological significance. Stem Cell Rev. 2008;4:89-99.
15. Kucia M, Zuba-Surma EK, Wysoczynski M, Wu W, Ratajczak J, Machalinski B, Ratajczak MZ. Adult marrow-derived very small embryonic-like stem cells and tissue engineering. Expert Opin Biol Ther. 2007;7:1499-1514.
16. Ratajczak MZ, Machalinski B,WojakowskiW,Ratajczak J, Kucia M.Ahypothesis for an embryonic origin of pluripotentOct-4(+) stem cells in adult bone marrow and other tissues. Leukemia 2007;21:860-867.
17. Kucia M, Machalinski B, Ratajczak MZ. The developmental deposition of epiblast/germ cell-line derived cells in various organs as a hypothetical explanation of stem cell plasticity? Acta Neurobiol Exp. 2006;66:331-341.
18. Villaron EM, Almeida J, Ĺopez-Holgado N, Alcoceba M, Śanchez-Abarca LI, Sanchez-Guijo FM, AlbercaM, Ṕerez-Simon JA, San Miguel JF, Del Cãnizo MC. Mesenchymal stem cells are present in peripheral blood and can engraft after allogeneic hematopoietic stem cell transplantation. Haematologica 2004;89:1421-1427.
19. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP. Evidence for circulating bone marrow-derived endothelial cells. Blood 1998;92:362-367.
20. Kucia MJ, Wysoczynski M, Wu W, Zuba-Surma EK, Ratajczak J, Ratajczak MZ. Evidence that very small embryoniclike stem cells are mobilized into peripheral blood. Stem Cells 2008;26:2083-2092.
21. Wojakowski W, Tendera M, Kucia M, Zuba-Surma E, Paczkowska E, Ciosek J, Hałasa M, Kŕ ol M, Kázmierski M, Buszman P,Ocha-la A, Ratajczak J, Machalínski B, Ratajczak MZ.Mobilization of bone marrow-derived Oct-4+SSEA-4+ very small embryonic-like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol. 2009;53:1-9.
22. Paczkowska E, Kucia M, Koziarska D, Hałasa M, Safranow K, Masiuk M, Karbicka A, Nowik M, Nowacki P, Ratajczak MZ, Machalí nski B. Clinical evidence that very small embryonic-like (VSEL) stem cells aremobilized into peripheral blood in patients after stroke. Stroke 2009;40:1237-1244.
23. Kucia M, Wojakowski W, Reca R, Machalinski B, Gozdzik J, Majka M, Baran J, Ratajczak J, Ratajczak MZ. The migration of bone marrow-derived non-hematopoietic tissue-committed stem cells is regulated in an SDF-1-, HGF-, and LIF-dependent manner. Arch Immunol Ther Exp. 2006;54:121-135.
24. Kijowski J, Baj-KrzyworzekaM, Majka M, Reca R, Marquez LA, Christofidou-Solomidou M, Janowska-Wieczorek A, Ratajczak MZ. The SDF-1-CXCR4 axis stimulates VEGF secretion and activates integrins but does not affect proliferation and survival in lymphohematopoietic cells. Stem Cells 2001;19:453-466.
25. Wysoczynski M, Reca R, Ratajczak J, Kucia M, Shirvaikar N, Mills M, Wanzeck J, Honczarenko M, Janowska-Wieczorek A, Ratajczak MZ. Incorporation of CXCR4 into membrane lipid rafts primes homing-related responses of hematopoietic stem cells to an SDF-1 gradient. Blood 2005;105:40-48.
26. Paczkowska E, Larysz B, Rzeuski R, Karbicka A, Ja-lowínski R, Kornacewicz-Jach Z, Ratajczak MZ, Machalínski B. Human hematopoietic stem/progenitor-enriched CD34+cells are mobilized into peripheral blood during stress related to ischemic stroke or acute myocardial infarction. Eur J Haematol. 2005;75:461-467.
27. MacHaliłski B, Paczkowska E, Koziarska D, Ratajczak MZ. Mobilization of human hematopoietic stem/progenitor-enriched CD34+ cells into peripheral blood during stress related to ischemic stroke. Folia Histochem Cytobiol. 2006;44:97-101.
28. Lapidot T, Petit I. Current understanding of stem cell mobilization: The roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Exp Hematol. 2002;30:973-981.
29. Cottler-Fox MH, Lapidot T, Petit I, KolletO,DiPersio JF, Link D, Devin S. Stem cell mobilization. Hematol Am Soc Hematol Educ Prog. 2003:419-437.
30. Szumilas P, Barcew K, Baskiewicz-Masiuk M, Wiszniewska B, Ratajczak MZ, Machalinski B. Effect of stem cell mobilization with cyclophosphamide plus granulocyte colony-stimulating factor on morphology of haematopoietic organs in mice. Cell Prolif. 2005;38:47-61.
31. Ti SE, Anderson D, Touhami A, Kim C, Tseng SC. Factors affecting outcome following transplantation of ex vivo expanded limbal epithelium on amniotic membrane for total limbal defi- ciency in rabbits. Invest Ophthalmol Vis Sci. 2002;43:2584-2592.
32. Tweedell KS. New paths to pluripotent stem cells. Curr Stem Cell Res Ther. 2008;3:151-162.
33. Munsie MJ,Michalska AE,O'Brien CM, TrounsonAO, Pera MF, Mountford PS. Isolation of pluripotent embryonic stem cells from reprogrammed adult mouse somatic cell nuclei. Curr Biol. 2000;10:989-992.
34. Chang CC, Sung LY, Amano T, Tian XC, Yang X, Nagy ZP. Nuclear transfer and oocyte cryopreservation. Reprod Fertil Dev. 2009;21:37-44.
35. Arnhold S, Klein H, Semkova I, Addicks K, Schraermeyer U. Neurally selected embryonic stem cells induce tumor formation after long-term survival following engraftment into the subretinal space. Invest Ophthalmol Vis Sci. 2004;45:4251-4255.
36. Wu DC, Boyd AS, Wood KJ. Embryonic stem cells and their differentiated derivatives have a fragile immune privilege but still represent novel targets of immune attack. Stem Cells 2008;26:1939-1950.
37. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
38. Li Y, Reca RG, Atmaca-Sonmez P, Ratajczak MZ, Ildstad ST, Kaplan HJ, Enzmann V. Retinal pigment epithelium damage enhances expression of chemoattractants and migration of bone marrow-derived stem cells. Invest Ophthalmol Vis Sci. 2006;47:1646-1652.
39. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ. A population of very small embryoniclike (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006;20:857-869.
40. HalasaM, Baskiewicz-MasiukM, Dabkowska E, Machalinski B. An efficient two-step method to purify very small embryoniclike (VSEL) stem cells from umbilical cord blood (UCB). Folia Histochem Cytobiol. 2008;46:239-243.
41. Machalinski B, Kijowski J, Marlicz W, Gontarewicz A, Markiewski M, Paczkowski M, Kopkowski A, Majka M, Ostrowski M, Ratajczak MZ. Heparinized cadaveric organ donors (HCOD)-A potential source of hematopoietic cells for transplantation and gene therapy. Transplantation 2001;71:1003-1007.
42. Machalinski B, Paczkowska E, Halasa M, Pabisiak K, Walczak M, Sienko J, Kozik W, Ostrowski M, Syrenicz A, Sulikowski T, Machalinska A. Expression of stem cell markers on mononuclear cells derived from heparinized cadaveric organ donors before and after disconnection from the respirator. Transplant Proc. 2006;38:16-19.
43. Machalinski B, Baskiewicz-Masiuk M, Pabisiak K, Grymula K, Sienko J, Domanski L, OstrowskiM, Machalinska A. The evaluation of apoptosis and reactive oxygen species in hematopoietic cells derived from heparinized cadaveric organ donors stored short-term at 4 degrees C. Transplant Proc. 2005;37:2281-2284.
44. Machalinski B, Paczkowski M, Kawa M, Paczkowska E, Ostrowski M. An optimization of isolation of early hematopoietic cells from heparinized cadaveric organ donors. Transplant Proc. 2003;35:3096-3100.
45. Vugler A, Carr AJ, Lawrence J, Chen LL, Burrell K, Wright A, Lundh P, Semo M, Ahmado A, Gias C, da Cruz L, Moore H, Andrews P, Walsh J, Coffey P. Elucidating the phenomenon of HESC-derived RPE: Anatomy of cell genesis, expansion, and retinal transplantation. Exp Neurol. 2008;214:347-361.
46. Fisher AJ, Reh TA. Transdifferentiation of pigmented epithelial cells: A source of retinal stem cells? Dev Neurosci. 2001;23:268-276.
47. Carr AJ, Vugler A, Lawrence J, Chen LL, Ahmado A, Chen FK, Semo M, Gias C, da Cruz L, Moore HD, Walsh J, Coffey PJ. Molecular characterization and functional analysis of phagocytosis by human embryonic stem cell-derived RPE cells using a novel human retinal assay. Mol Vis. 2009;15:283-295.
48. Hirami Y, Osakada F, Takahashi K, Okita K, Yamanaka S, Ikeda H, Yoshimura N, Takahashi M. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neurosci Lett. 2009;458:126-131.
49. Coles BL, Angenieux B, Inoue T, Del Rio-Tsonis K, Spence JR, McInnes RR, Arsenijevic Y, van der Kooy D. Facile isolation and the characterization of human retinal stem cells.Proc Natl Acad Sci USA 2004;101:15772-15777.
50. HumayunMS, de Juan E Jr, del Cerro M, Dagnelie G, Radner W, Sadda SR, del Cerro C. Human neural retinal transplantation. Invest Ophthalmol Vis Sci. 2000;41:3100-3106.
51. KelleyMW, Turner JK, Reh TA. Regulation of proliferation and photoreceptor differentiation in fetal human retinal cell cultures. Invest Ophthalmol Vis Sci. 1995;36:1280-1289.
52. Yang P, SeilerMJ, Aramant RB, Whittemore SR. In vitro isolation and expansion of human retinal progenitor cells. Exp Neurol. 2002;177:326-331.
53. Lamba DA, Karl MO, Reh TA. Neural regeneration and cell replacement: A view from the eye. Cell Stem Cells 2008;2:538-549.
54. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR. Retinal repair by transplantation of photoreceptor precursors. Nature 2006;444;203-207.
55. Lamba DA, Gust J, Reh TA. Transplantation of human embryonic stem cell-derived photoreceptors restores somevisual function in Crx-deficient mice. Cell Stem Cells 2009;4:73-79.
56. Kicic A, Shen WY, Wilson AS, Constable IJ, Robertson T, Rakoczy PE. Differentiation of marrow stromal cells into photoreceptors in the rat eye. J Neurosci. 2003;23:7742-7749.
57. Tomita M, Mori T, Maruyama K, Zahir T, Ward M, Umezawa A, Young MJ. A comparison of neural differentiation and retinal transplantation with bone marrow-derived cells and retinal progenitor cells. Stem Cells 2006;24:2270-2278.
58. Chiou SH, Kao CL, Peng CH, Chen SJ, Tarng YW, Ku HH, Chen YC, ShyrYM, LiuRS, HsuCJ, YangDM,HsuWM,KuoCD, Lee CH.Anovel in vitro retinal differentiationmodel by co-culturing adult human bone marrow stem cells with retinal pigmented epithelium cells. Biochem Biophys ResCommun. 2005;326:578-585.
59. Strunk D, Stamm C. Adult stem cell for myocardial tissue repair. In: Battler A, Leor J, eds. Stem Cell and Gene-Based Therapy. Frontiers in Regenerative Medicine. London: Springer; 2006:17-31.
60. Minamino K, Adachi Y, Yamada H, Higuchi A, Suzuki Y, IwasakiM, Nakano K, Koike Y, Mukaide H, Kiriyama N, Shigematsu A, Matsumura M, Ikehara S. Long-term survival of bone marrow-derived retinal nerve cells in the retina. Neuroreport 2005;16:1255-1259.
61. Takahashi M, Palmer TD, Takahashi J, Gage FH. Widespread integration and survival of adult-derived neural progenitor cells in the developing optic retina. Mol Cell Neurosci. 1998;12:340-348.
62. Tomita M, Adachi Y, Yamada H, Takahashi K, Kiuchi K,Oyaizu H, Ikebukuro K, Kaneda H, Matsumura M, Ikehara S. Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells 2002;20:279-283.
63. Zhang J, ShanQ, Ma P, JiangY,Chen P,Wen J, Zhou Y, QianH, Pei X. Differentiation potential of bone marrow mesenchymal stem cells into retina in normal and laser-injured rat eye. Sci China C Life Sci. 2004;47:241-250.
64. Koike-Kiriyama N, Adachi Y, Minamino K, IwasakiM, Nakano K, Koike Y, Yamada H, Mukaide H, Shigematsu A, Mizokami T, Matsumura M, Ikehara S. Human cord blood cells can differentiate into retinal nerve cells. Acta Neurobiol Exp. 2007;67: 359-365.
65. Jonas JB, Witzens-Harig M, Arseniev L, Ho AD. Intravitreal autologous bone marrow-derived mononuclear cell transplantation: A feasibility report. Acta Ophthalmol. 2008;86: 225-226.
66. Farrar GJ, Kenna PF, Humphries P. On the genetics of retinitis pigmentosa and on mutation-independent approaches to therapeutic intervention. EMBO J. 2002;21:857-864.
67. Chang B, Hawes NL, Davisson MT, Heckenlively JR. Mouse model of RP. In: Tombran-Tink J, Barnstable CJ, eds. Retinal Degenerations: Biology, Diagnostics, and Therapeutics. Totowa, NJ: Humana Press; 2007:149-161.
68. Inoue Y, Iriyama A, Ueno S, Takahashi H, Kondo M, Tamaki Y, Araie M, Yanagi Y. Subretinal transplantation of bone marrow mesenchymal stem cells delays retinal degeneration in the RCS rat model of retinal degeneration. Exp Eye Res. 2007;85:234-241.
69. Arnhold S, Heiduschka P, Klein H, Absenger Y, Basnaoglu S, Kreppel F, Henke-Fahle S, Kochanek S, Bartz-Schmidt KU, Addicks K, Schraermeyer U. Adenovirally transduced bone marrow stromal cells differentiate into pigment epithelial cells and induce rescue effects in RCS rats. Invest Ophthalmol Vis Sci. 2006;47:4121-4129.
70. Arnhold S, Absenger Y, Klein H, Addicks K, Schraermeyer U. Transplantation of bone marrow-derived mesenchymal stem cells rescue photoreceptor cells in the dystrophic retina of the rhodopsin knockout mouse. Graefes Arch Clin Exp Ophthalmol. 2007;245:414-422.
71. Ogilvie JM, Speck JD, Lett JM. Growth factors in combination, but not individually, rescue rd mouse photoreceptors in organ culture. Exp Neurol. 2000;161:676-685.
72. Chen Q, Long Y, Yuan X, Zou L, Sun J, Chen S, Perez-Polo JR, Yang K. Protective effects of bone marrow stromal cell transplantation in injured rodent brain: Synthesis of neurotrophic factors. J Neurosci Res. 2005;80:611-619.
73. Espinosa-Heidmann DG, Reinoso MA, Pina Y, Csaky KG, Caicedo A, Cousins SW. Quantitative enumeration of vascular smoothmuscle cells and endothelial cells derived from bone marrow precursors in experimental choroidal neovascularization. Exp Eye Res. 2005;80:369-378.
74. Espinosa-Heidmann DG, Caicedo A,Hernandez EP, Csaky KG, Cousins SW. Bone marrow-derived progenitor cells contribute to experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:4914-4919.
75. Chan-Ling T, Baxter L, Afzal A, Sengupta N, Caballero S, Rosinova E, Grant MB. Hematopoietic stem cells provide repair functions after laser-induced Bruch'smembrane rupture model of choroidal neovascularization. Am J Pathol. 2006;168:1031-1044.
76. Otani A, Dorrell MI, Kinder K,Moreno SK, Nusinowitz S, Banin E, Heckenlively J, Friedlander M. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineagenegative hematopoietic stem cells. J Clin Invest. 2004;114:765-774.
77. Kociok N. Can the injection of the patient's own bone marrowderived stem cells preserve cone vision in retinitis pigmentosa and other diseases of the eye? Graefes Arch Clin Exp Ophthalmol. 2005;243:187-188.
78. Smith LE. Bone marrow-derived stem cells preserve cone vision in retinitis pigmentosa. J Clin Invest. 2004;114:755-757.
79. Gilgun-Sherki Y, Streifler JY. Cell replacement therapy in acute stroke: Current state. In: Battler A, Leor J, eds. Stem Cell and Gene-Based Therapy. Frontiers in Regenerative Medicine. London: Springer; 2006:123-132.
80. Donati G. Emerging therapies for neovascular age-related macular degeneration: State of the art. Ophthalmologica. 2007;221:366-377.
81. Tomita M, Yamada H, Adachi Y, Cui Y, Yamada E, Higuchi A, Minamino K, Suzuki Y, Matsumura M, Ikehara S. Choroidal neovascularization is provided by bonemarrow cells. Stem Cells 2004;22:21-26.
82. Grant MB, May WS, Caballero S, Brown GA, Guthrie SM, Mames RN, Byrne BJ, Vaught T, Spoerri PE, Peck AB, Scott EW. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med. 2002;8:607-612.
83. Otani A, Kinder K, Ewalt K, Otero FJ, Schimmel P, Friedlander M. Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med. 2002;8:1004-1010.
84. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. NatMed. 2003;9:702-712.
85. Prater DN, Case J, Ingram DA, Yoder MC.Working hypothesis to redefine endothelial progenitor cells. Leukemia 2007;21:1141-1149.
86. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007;109:1801-1809.
87. Ritter MR, Banin E, Moreno SK, Aguilar E, Dorrell MI, Friedlander M. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest. 2006;116:3266-3276.
88. Dorrell MI, Otani A, Aguilar E, Moreno SK, Friedlander M. Adult bone marrow-derived stem cells use R-cadherin to target sites of neovascularization in the developing retina. Blood 2004;103:3420-3427.
89. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, Chimenti S, Landsman L, Abramovitch R, Keshet E. VEGFinduced adult neovascularization: Recruitment, retention, and role of accessory cells. Cell 2006;124:175-189.
90. Crane IJ, Wallace CA, McKillop-Smith S, Forrester JV. CXCR4 receptor expression on human retinal pigment epithelial cells from the blood-retina barrier leads to chemokine secretion and migration in response to stromal cell-derived factor 1 alpha. J Immunol. 2000;165:4372-4378.
91. Butler JM, Guthrie SM, Koc M, Afzal A, Caballero S, Brooks HL, Mames RN, Segal MS, Grant MB, Scott EW. SDF-1 is both necessary and sufficient to promote proliferative retinopathy. J Clin Invest. 2005;115:86-93.
92. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-864.
93. Harris JR, Fisher R, Jorgenssen M, Kaushal S, Scott EW. CD133 progenitor cells from the bonemarrow contribute to retinal pigment epithelium repair. Stem Cells 2009;27:457-466.
94. Sun G, Asami M, Ohta H, Kosaka J, Kosaka M. Retinal stem/progenitor properties of iris pigment epithelial cells. Dev Biol. 2006;289:243-252.
95. Nishida A, Takahashi M, Tanihara H, Nakano I, Takahashi JB, Mizoguchi A, Ide C, Honda Y. Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Invest Ophthalmol Vis Sci. 2000;41:4268-4274.
96. Guo Y, Saloupis P, Shaw SJ, Rickman DW. Engraftment of adult neural progenitor cells transplanted to rat retina injured by transient ischemia. Invest Ophthalmol Vis Sci. 2003;44:3194-3201.
97. Seigel GM, Sun W, Salvi R, Campbell LM, Sullivan S, Reidy JJ. Human corneal stem cells display functional neuronal properties. Mol Vis. 2003;9:159-163.