Human Müller stem cell (MIO-M1) transplantation in a rat model of glaucoma: Survival, differentiation, and integration

Investigative Ophthalmology and Visual Science

Volumn 49, Issue 8, 2008, Pages 3449-3456

  Bull, Natalie D ^a   Limb, G Astrid ^b   Martin, Keith R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AZATHIOPRINE; BETA TUBULIN; CHONDROITIN ABC LYASE; CYCLOSPORIN; ERYTHROPOIETIN; NERVE CELL ADHESION MOLECULE; PREDNISOLONE; BETA III TUBULIN PROTEIN, HUMAN; BETA III-TUBULIN PROTEIN, HUMAN; ENHANCED GREEN FLUORESCENT PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; IMMUNOSUPPRESSIVE AGENT; NERVE CELL ADHESION MOLECULE L1; POLYSIALYL NEURAL CELL ADHESION MOLECULE; RECOMBINANT ERYTHROPOIETIN; SIALIC ACID DERIVATIVE; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL LINE; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; EXPERIMENTAL MODEL; GLAUCOMA; GLIA; GLIA CELL; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INTRAOCULAR PRESSURE; MACROPHAGE; MICROGLIA; MUELLER CELL; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; RETINA; RETINA NERVE CELL; STEM CELL TRANSPLANTATION; VITREOUS BODY; XENOGRAFT; ADULT STEM CELL; ANIMAL; AQUEOUS HUMOR; CELL MOTION; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; MALE; METABOLISM; PHYSIOLOGY; TRANSPLANTATION; WISTAR RAT;

ADULT STEM CELLS; ANIMALS; AQUEOUS HUMOR; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; CHONDROITIN ABC LYASE; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN, RECOMBINANT; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLAUCOMA; GLIAL FIBRILLARY ACIDIC PROTEIN; GRAFT SURVIVAL; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTRAOCULAR PRESSURE; MALE; NEURAL CELL ADHESION MOLECULE L1; NEUROGLIA; RATS; RATS, WISTAR; RETINA; SIALIC ACIDS; STEM CELL TRANSPLANTATION; TRANSFECTION; TUBULIN;

EID: 49049108522     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-1770     Document Type: Article

References (56)

1. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:262-267.
2. Martin KR, Quigley HA, Valenta D, Kielczewski J, Pease ME. Optic nerve dynein motor protein distribution changes with intraocular pressure elevation in a rat model of glaucoma. Exp Eye Res. 2006;83:255-262.
3. Kumar DM, Agarwal N. Oxidative stress in glaucoma: a burden of evidence. J Glaucoma. 2007;16:334-343.
4. Naskar R, Wissing M, Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci. 2002;43:2962-2968.
5. Coles BL, Angenieux B, Inoue T, et al. Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA. 2004;101:15772-15777.
6. Limb GA, Salt TE, Munro PM, Moss SE, Khaw PT. In vitro characterization of a spontaneously immortalized human Muller cell line (MIO-M1). Invest Ophthalmol Vis Sci. 2002;43:864-869.
7. Meyer JS, Katz ML, Maruniak JA, Kirk MD. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells. 2006;24:274-283.
8. Xu H, Sta Iglesia DD, Kielczewski JL, et al. Characteristics of progenitor cells derived from adult ciliary body in mouse, rat, and human eyes. Invest Ophthalmol Vis Sci. 2007;48:1674-1682.
9. Harrower TP, Tyers P, Hooks Y, Barker RA. Long-term survival and integration of porcine expanded neural precursor cell grafts in a rat model of Parkinson's disease. Exp Neurol. 2006;197:56-69.
10. Kurimoto Y, Shibuki H, Kaneko Y, et al. Transplantation of adult rat hippocampus-derived neural stem cells into retina injured by transient ischemia. Neurosci Lett. 2001;306:57-60.
11. Lee HJ, Kim KS, Park IH, Kim SU. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS ONE. 2007;2:e156.
12. MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature. 2006;444:203-207.
13. Wei P, Liu J, Zhou HL, et al. Effects of engrafted neural stem cells derived from GFP transgenic mice in Parkinson's diseases rats. Neurosci Lett. 2007;419:49-54.
14. Yasuhara T, Matsukawa N, Hara K, et al. Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J Neurosci. 2006;26:12497-12511.
15. Akerud P, Canals JM, Snyder EY, Arenas E. Neuroprotection through delivery of glial cell line-derived neurotrophic factor by neural stem cells in a mouse model of Parkinson's disease. J Neurosci. 2001;21:8108-8118.
16. Hagan M, Wennersten A, Meijer X, Holmin S, Wahlberg L, Mathiesen T. Neuroprotection by human neural progenitor cells after experimental contusion in rats. Neurosci Lett. 2003;351:149-152.
17. Wilkins A, Majed H, Layfield R, Compston A, Chandran S. Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J Neurosci. 2003;23:4967-4974.
18. Yu S, Tanabe T, Dezawa M, Ishikawa H, Yoshimura N. Effects of bone marrow stromal cell injection in an experimental glaucoma model. Biochem Biophys Res Commun. 2006;344:1071-1079.
19. Madhavan L, Ourednik V, Ourednik J. Neural stem/progenitor cells initiate the formation of cellular networks that provide neuroprotection by growth factor-modulated antioxidant expression. Stem Cells. 2008;26:254-265.
20. 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.
21. Chacko DM, Das AV, Zhao X, James J, Bhattacharya S, Ahmad I. Transplantation of ocular stem cells: the role of injury in incorporation and differentiation of grafted cells in the retina. Vision Res. 2003;43:937-946.
22. Nishida A, Takahashi M, Tanihara H, et al. Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Invest Ophthalmol Vis Sci. 2000;41:4268-4274.
23. Gamm DM, Wang S, Lu B, et al. Protection of visual functions by human neural progenitors in a rat model of retinal disease. PLoS ONE. 2007;2:e338.
24. Inoue Y, Iriyama A, Ueno S, et al. 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.
25. Lund RD, Wang S, Lu B, et al. Cells isolated from umbilical cord tissue rescue photoreceptors and visual functions in a rodent model of retinal disease. Stem Cells. 2007;25:602-611.
26. Schraermeyer U, Thumann G, Luther T, et al. Subretinally transplanted embryonic stem cells rescue photoreceptor cells from degeneration in the RCS rats. Cell Transplant. 2001;10:673-680.
27. Young MJ, Ray J, Whiteley SJ, Klassen H, Gage FH. Neuronal differentiation and morphological integration of hippocampal progenitor cells transplanted to the retina of immature and mature dystrophic rats. Mol Cell Neurosci. 2000;16:197-205.
28. Grozdanic SD, Ast AM, Lazic T, et al. Morphological integration and functional assessment of transplanted neural progenitor cells in healthy and acute ischemic rat eyes. Exp Eye Res. 2006;82:597-607.
29. Mellough CB, Cui Q, Spalding KL, et al. Fate of multipotent neural precursor cells transplanted into mouse retina selectively depleted of retinal ganglion cells. Exp Neurol. 2004;186:6-19.
30. Banin E, Obolensky A, Idelson M, et al. Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells. Stem Cells. 2006;24:246-257.
31. Hara A, Niwa M, Kunisada T, et al. Embryonic stem cells are capable of generating a neuronal network in the adult mouse retina. Brain Res. 2004;999:216-221.
32. Lawrence JM, Singhal S, Bhatia B, et al. MIO-M1 cells and similar muller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells. 2007;25:2033-2043.
33. Levkovitch-Verbin H, Quigley HA, Martin KR, Valenta D, Baumrind LA, Pease ME. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest Ophthalmol Vis Sci. 2002;43:402-410.
34. Sigalet DL, Thorne PC, Martin GR, Garola RE, Yatscoff RW. Combined immunosuppression with cyclosporine, rapamycin, and mycophenolate mofetil controls rejection with minimal nutritional impact in experimental small intestinal transplantation. Transplant Proc. 2002;34:1121-1123.
35. Mimouni D, Nousari HC. Inhibitors of purine and pyrimidine synthesis: mycophenolate, azathioprine, and leflunomide. Dermatolog Ther. 2002;15:311-316.
36. Shen WY, Lai MC, Beilby J, et al. Combined effect of cyclosporine and sirolimus on improving the longevity of recombinant adenovirus-mediated transgene expression in the retina. Arch Ophthalmol. 2001;119:1033-1043.
37. Singhal S, Lawrence JM, Bhatia B, et al. Chondroitin Sulphate Proteoglycans and Microglia Prevent Migration and Integration of Grafted Muller Stem Cells Into Degenerating Retina. Stem Cells. 2008;Epub ahead of print.
38. Tsai JC, Wu L, Worgul B, Forbes M, Cao J. Intravitreal administration of erythropoietin and preservation of retinal ganglion cells in an experimental rat model of glaucoma. Curr Eye Res. 2005;30:1025-1031.
39. Chauhan BC, Levatte TL, Garnier KL, et al. Semiquantitative optic nerve grading scheme for determining axonal loss in experimental optic neuropathy. Invest Ophthalmol Vis Sci. 2006;47:634-640.
40. Xue LP, Lu J, Cao Q, Hu S, Ding P, Ling EA. Muller glial cells express nestin coupled with glial fibrillary acidic protein in experimentally induced glaucoma in the rat retina. Neuroscience. 2006;139:723-732.
41. Qiu G, Seiler MJ, Mui C, et al. Photoreceptor differentiation and integration of retinal progenitor cells transplanted into transgenic rats. Exp Eye Res. 2005;80:515-525.
42. Cui Q, Hodgetts SI, Hu Y, Luo JM, Harvey AR. Strain-specific differences in the effects of cyclosporin A and FK506 on the survival and regeneration of axotomized retinal ganglion cells in adult rats. Neuroscience. 2007;146:986-999.
43. Wang L, Zhang ZG, Zhang RL, et al. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci. 2006;26:5996-6003.
44. Suzuki T, Mandai M, Akimoto M, Yoshimura N, Takahashi M. The simultaneous treatment of MMP-2 stimulants in retinal transplantation enhances grafted cell migration into the host retina. Stem Cells. 2006;24:2406-2411.
45. Nickerson PEB, McLeod MC, Myers T, Clarke DB. Phenotypic analysis of proliferating Mueller radial glia: effects of EGF and EPO exposure in the adult mammalian retina. Abstract Viewer/Itinerary Planner. 2005; Washington DC: Society for Neuroscience, 2005. Online: Progam No. 708.9.
46. Rhodes KE, Fawcett JW. Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat. 2004;204:33-48.
47. Crespo D, Asher RA, Lin R, Rhodes KE, Fawcett JW. How does chondroitinase promote functional recovery in the damaged CNS? Exp Neurol. 2007;206:159-171.
48. Ikegami T, Nakamura M, Yamane J, et al. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur J Neurosci. 2005;22:3036-3046.
49. Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci. 2006;26:7405-7415.
50. Kim BG, Dai HN, Lynskey JV, McAtee M, Bregman BS. Degradation of chondroitin sulfate proteoglycans potentiates transplant-mediated axonal remodeling and functional recovery after spinal cord injury in adult rats. J Comp Neurol. 2006;497:182-198.
51. Mooney DJ, Vandenburgh H. Cell delivery mechanisms for tissue repair. Cell Stem Cell. 2008;2:205-213.
52. Horita Y, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. Intravenous administration of glial cell line-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in the adult rat. J Neurosci Res. 2006;84:1495-1504.
53. Liu H, Honmou O, Harada K, et al. Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain. 2006;129:2734-2745.
54. Nomura T, Honmou O, Harada K, Houkin K, Hamada H, Kocsis JD. I.V. infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Neuroscience. 2005;136:161-169.
55. Pineda JR, Rubio N, Akerud P, et al. Neuroprotection by GDNF-secreting stem cells in a Huntington's disease model: optical neuroimage tracking of brain-grafted cells. Gene Ther. 2007;14:118-128.
56. Zhu W, Mao Y, Zhao Y, et al. Transplantation of vascular endothelial growth factor-transfected neural stem cells into the rat brain provides neuroprotection after transient focal cerebral ischemia. Neurosurgery. 2005;57:325-333.