Stem cell treatment of degenerative eye disease

Stem Cell Research

Volumn 14, Issue 3, 2015, Pages 243-257

  Mead, Ben ^a   Berry, Martin ^a   Logan, Ann ^a   Scott, Robert A H ^a   Leadbeater, Wendy ^a   Scheven, Ben A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TISSUE; ADULT STEM CELL; BONE MARROW; CELL DEGENERATION; DEGENERATIVE EYE DISEASE; EMBRYONIC STEM CELL; EYE; GLIA; HUMAN; MESENCHYMAL STEM CELL; NERVE FIBER; NEURAL STEM CELL; OPTIC NERVE; PIGMENT EPITHELIUM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGENERATION; RETINA CELL; RETINA DISEASE; RETINA GANGLION CELL; RETINA NERVE CELL; REVIEW; STEM CELL TRANSPLANTATION; SUBSTITUTION THERAPY; TOOTH PULP; TUMOR CELL INOCULATION; VISION; BIOLOGICAL THERAPY; CYTOLOGY; EYE DISEASES; GRAFT REJECTION; IMMUNOLOGY; INDUCED PLURIPOTENT STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; RETINA; STEM CELL; TRANSPLANTATION;

CELL- AND TISSUE-BASED THERAPY; DENTAL PULP; EMBRYONIC STEM CELLS; EYE DISEASES; GRAFT REJECTION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESENCHYMAL STEM CELL TRANSPLANTATION; NEURAL STEM CELLS; REGENERATION; RETINA; RETINAL GANGLION CELLS; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84924267865     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2015.02.003     Document Type: Review

References (157)

1. Aanismaa R., Hautala J., Vuorinen A., Miettinen S., Narkilahti S. Human dental pulp stem cells differentiate into neural precursors but not into mature functional neurons. Stem Cell Discov. 2012, 2:85-91.
2. Abematsu, M., Tsujimura, K., Yamano, M., Saito, M., Kohno, K., Kohyama, J., Namihira, M.,Komiya S., Nakashima K. Neurons derived from transplanted neural stem cells restore disrupted neuronal circuitry in a mouse model of spinal cord injury. J. Clin. Invest. 2010, 120:3255-3266.
3. Ahmad I., Tang L., Pham H. Identification of neural progenitors in the adult mammalian eye. Biochem. Biophys. Res. Commun. 2000, 270:517-521.
4. Ahmed Z., Kalinski H., Berry M., Almasieh M., Ashush H., Slager N., Brafman A., Spivak I., Prasad N., Mett I., Shalom E., Alpert E., Di Polo A., Feinstein E., Logan A. Ocular neuroprotection by siRNA targeting caspase-2. Cell Death Dis. 2011, 2:e173.
5. Anghileri E., Marconi S., Pignatelli A., Cifelli P., Galie M., Sbarbati A., Krampera M., Belluzzi O., Bonetti B. Neuronal differentiation potential of human adipose-derived mesenchymal stem cells. Stem Cells Dev. 2008, 17:909-916.
6. Arboleda D., Forostyak S., Jendelova P., Marekova D., Amemori T., Pivonkova H., Masinova K., Sykova E. Transplantation of predifferentiated adipose-derived stromal cells for the treatment of spinal cord injury. Cell. Mol. Neurobiol. 2011, 31:1113-1122.
7. 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. Graefe's archive for clinical and experimental ophthalmology=Albrecht von Graefes Archiv fur klinische und experimentelle. Ophthalmologie 2007, 245:414-422.
8. Arthur A., Rychkov G., Shi S., Koblar S.A., Gronthos S. Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 2008, 26:1787-1795.
9. Ballios B.G., Clarke L., Coles B.L.K., Shoichet M.S., Van Der Kooy D. The adult retinal stem cell is a rare cell in the ciliary epithelium whose progeny can differentiate into photoreceptors. Biol. Open 2012, 1(3):237-246.
10. Banin E., Obolensky A., Idelson M., Hemo I., Reinhardtz E., Pikarsky E., Ben-Hur T., Reubinoff B. Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells. Stem Cells 2006, 24:246-257.
11. Barde Y.-A. Trophic factors and neuronal survival. Neuron 1989, 2:1525-1534.
12. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 1994, 14:4368-4374.
13. Berry M., Ahmed Z., Lorber B., Douglas M., Logan A. Regeneration of axons in the visual system. Restor. Neurol. Neurosci. 2008, 26:147-174.
14. Bharti K., Miller S.S., Arnheiter H. The new paradigm: retinal pigment epithelium cells generated from embryonic or induced pluripotent stem cells. Pigment Cell Melanoma Res. 2011, 24:21-34.
15. Bohm M.R.R., Pfrommer S., Chiwitt C., Bruckner M., Melkonyan H., Thanos S. Crystallin-beta-b2-overexpressing NPCs support the survival of injured retinal ganglion cells and photoreceptors in rats. Invest. Ophthalmol. Vis. Sci. 2012, 53:8265-8279.
16. Butowt R., von Bartheld C.S. Connecting the dots: trafficking of neurotrophins, lectins and diverse pathogens by binding to the neurotrophin receptor p75(NTR). Eur. J. Neurosci. 2003, 17:673-680.
17. Canola K., Angénieux B., Tekaya M., Quiambao A., Naash M.I., Munier F.L., Schorderet D.F., Arsenijevic Y. Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Invest. Ophthalmol. Vis. Sci. 2007, 48:446-454.
18. Cao Q.L., Zhang Y.P., Howard R.M., Walters W.M., Tsoulfas P., Whittemore S.R. Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp. Neurol. 2001, 167:48-58.
19. Carr A.J., Vugler A., Lawrence J., Chen L.L., Ahmado A., Chen F.K., Semo M., Gias C., da Cruz L., Moore H.D., Walsh J., Coffey P.J. 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.
20. Carr A.J., Vugler A.A., Hikita S.T., Lawrence J.M., Gias C., Chen L.L., Buchholz D.E., Ahmado A., Semo M., Smart M.J., Hasan S., da Cruz L., Johnson L.V., Clegg D.O., Coffey P.J. Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat. Plos One 2009, 4:e8152.
21. Chacko D.M., Das A.V., 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. Vis. Res. 2003, 43:937-946.
22. Chen H., Weber A.J. Brain-derived neurotrophic factor reduces TrkB protein and mRNA in the normal retina and following optic nerve crush in adult rats. Brain Res. 2004, 1011:99-106.
23. Chen Q., Long Y., Yuan X., Zou L., Sun J., Chen S., Perez-Polo J.R., 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.
24. Chen M., Xiang Z., Cai J. The anti-apoptotic and neuro-protective effects of human umbilical cord blood mesenchymal stem cells (hUCB-MSCs) on acute optic nerve injury is transient. Brain Res. 2013, 1532:63-75.
25. Cho S.-R., Kim Y.R., Kang H.-S., Yim S.H., C-i Park, Min Y.H., Lee B.H., Shin J.C., Lim J.-B. Functional recovery after the transplantation of neurally differentiated mesenchymal stem cells derived from bone barrow in a rat model of spinal cord injury. Cell Transplant. 2009, 18:1359-1368.
26. Clarke L., Ballios B.G., van der Kooy D. Generation and clonal isolation of retinal stem cells from human embryonic stem cells. Eur. J. Neurosci. 2012, 36:1951-1959.
27. Cuenca N., Fernandez-Sanchez L., McGill T.J., Lu B., Wang S.M., Lund R., Huhn S., Capela A. Phagocytosis of photoreceptor outer segments by transplanted human neural stem cells as a neuroprotective mechanism in retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2013, 54:6745-6756.
28. Cummings B.J., Uchida N., Tamaki S.J., Salazar D.L., Hooshmand M., Summers R., Gage F.H., Anderson A.J. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14069-14074.
29. da Cruz L., Chen F.K., Ahmado A., Greenwood J., Coffey P. RPE transplantation and its role in retinal disease. Prog. Retin. Eye Res. 2007, 26:598-635.
30. Dawbarn D., Allen S.J. Neurotrophins and neurodegeneration. Neuropathol. Appl. Neurobiol. 2003, 29:211-230.
31. Del Debbio C.B., Peng X., Xiong H., Ahmad I. Adult ciliary epithelial stem cells generate functional neurons and differentiate into both early and late born retinal neurons under non-cell autonomous influences. BMC Neurosci. 2013, 14:130.
32. Dormady S.P., Bashayan O., Dougherty R., Zhang X.M., Basch R.S. Immortalized multipotential mesenchymal cells and the hematopoietic microenvironment. J. Hematother. Stem Cell Res. 2001, 10:125-140.
33. Dougherty K.D., Dreyfus C.F., Black I.B. Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol. Dis. 2000, 7:574-585.
34. Eiraku M., Takata N., Ishibashi H., Kawada M., Sakakura E., Okuda S., Sekiguchi K., Adachi T., Sasai Y. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 2011, 472:51-56.
35. Fang C.-z., Yang Y.-j., Wang Q.-h., Yao Y., Zhang X.-y., He X.-h. Intraventricular injection of human dental pulp stem cells improves hypoxic-ischemic brain damage in neonatal rats. Plos One 2013, 8:e66748.
36. Faulkner J.R., Herrmann J.E., Woo M.J., Tansey K.E., Doan N.B., Sofroniew M.V. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 2004, 24:2143-2155.
37. Fischer A.J. Neural regeneration in the chick retina. Prog. Retin. Eye Res. 2005, 24:161-182.
38. Flachsbarth K., Kruszewski K., Jung G., Jankwiak W., Riecken K., Wagenfeld L., Richard G., Fehse B., Bartsch U. Neural stem cell-based intraocular administration of ciliary neurotrophic factor attentuates the loss of axotomized ganglion cells in adult mice. Invest. Ophthalmol. Vis. Sci. 2014, 55:7029-7039.
39. Gale Z., Cooper P.R., Scheven B.A.A. Effects of glial cell line-derived neurotrophic factor on dental pulp cells. J. Dent. Res. 2011, 90:1240-1245.
40. Ghorbanian M.T., Haji Ghasem Kashani M., Lashkarblouki T., Hosseinpour L., Mirzaiyan L. Characterization of in vitro cultured bone marrow and adipose tissue-derived mesenchymal stem cells and their ability to express neurotrophic factors. Cell Biol. Int. 2012, 36(12):1239-1249.
41. Gonzalez-Cordero A., West E.L., Pearson R.A., Duran Y., Carvalho L.S., Chu C.J., Naeem A., Blackford S.J.I., Georgiadis A., Lakowski J., Hubank M., Smith A.J., Bainbridge J.W.B., Sowden J.C., Ali R.R. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol. 2013, 31:741-747.
42. Grozdanic S.D., Ast A.M., Lazic T., Kwon Y.H., Kardon R.H., Sonea I.M., Sakaguchi D.S. Morphological integration and functional assessment of transplanted neural progenitor cells in healthy and acute ischemic rat eyes. Exp. Eye Res. 2006, 82:597-607.
43. Gu Y.L., Yin L.W., Zhang Z., Liu J., Liu S.J., Zhang L.F., Wang T.H. Neurotrophin expressions in neural stem cells grafted acutely to transected spinal cord of adult rats linked to functional improvement. Cell. Mol. Neurobiol. 2012, 32:1089-1097.
44. Haddad-Mashadrizeh A., Bahrami A.R., Matin M.M., Edalatmanesh M.A., Zomorodipour A., Gardaneh M., Farshchian M., Momeni-Moghaddam M. Human adipose-derived mesenchymal stem cells can survive and integrate into the adult rat eye following xenotransplantation. Xenotransplantation 2013, 20:165-176.
45. Hambright D., Park K.Y., Brooks M., McKay R., Swaroop A., Nasonkin I.O. Long-term survival and differentiation of retinal neurons derived from human embryonic stem cell lines in un-immunosuppressed mouse retina. Mol. Vis. 2012, 18:920-936.
46. Harper M.M., Grozdanic S.D., Blits B., Kuehn M.H., Zamzow D., Buss J.E., Kardon R.H., Sakaguchi D.S. Transplantation of BDNF-secreting mesenchymal stem cells provides neuroprotection in chronically hypertensive rat eyes. Invest. Ophthalmol. Vis. Sci. 2011, 52:4506-4515.
47. He B.-L., Ba Y.-c., Wang X.-y., Liu S.-j., Ou S., Liu G.-d., Gu Y.-l., Pan X.-h., Wang T.-H. BDNF expression with functional improvement in transected spinal cord treated with neural stem cells in adult rats. Neuropeptides 2012, 47(1):1-7.
48. Hertz J., Qu B., Hu Y., Patel R.D., Valenzuela D.A., Goldberg J.L. Survival and integration of developing and progenitor-derived retinal ganglion cells following transplantation. Cell Transplant. 2014, 23:855-872.
49. Hill A.J., Zwart I., Tam H.H., Chan J., Navarrete C., Jen L.S., Navarrete R. Human umbilical cord blood-derived mesenchymal stem cells do not differentiate into neural cell types or integrate into the retina after intravitreal grafting in neonatal rats. Stem Cells Dev. 2009, 18:399-409.
50. Huang A.H.-C., Snyder B.R., Cheng P.-H., Chan A.W.S. Putative dental pulp-derived stem/stromal cells promote proliferation and differentiation of endogenous neural cells in the hippocampus of mice. Stem Cells 2008, 26:2654-2663.
51. Ikeda H., Osakada F., Watanabe K., Mizuseki K., Haraguchi T., Miyoshi H., Kamiya D., Honda Y., Sasai N., Yoshimura N., Takahashi M., Sasai Y. Generation of Rx+/Pax6+ neural retinal precursors from embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11331-11336.
52. Ishizaka R., Hayashi Y., Iohara K., Sugiyama M., Murakami M., Yamamoto T., Fukuta O., Nakashima M. Stimulation of angiogenesis, neurogenesis and regeneration by side population cells from dental pulp. Biomaterials 2013, 34:1888-1897.
53. Jeong S.W., Chu K., Jung K.H., Kim S.U., Kim M., Roh J.K. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 2003, 34:2258-2263.
54. Jiang L.Q., Streilein J.W. Immune privilege extended to allogeneic tumor cells in the vitreous cavity. Invest. Ophthalmol. Vis. Sci. 1991, 32:224-228.
55. Jiang Y., Ding Q., Xie X., Libby R.T., Lefebvre V., Gan L. Transcription factors SOX4 and SOX11 function redundantly to regulate the development of mouse retinal ganglion cells. J. Biol. Chem. 2013, 288:18429-18438.
56. Johnson T.V., Bull N.D., Hunt D.P., Marina N., Tomarev S.I., Martin K.R. Neuroprotective effects of intravitreal mesenchymal stem cell transplantation in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2010, 51:2051-2059.
57. Johnson T.V., Dekorver N.W., Levasseur V.A., Osborne A., Tassoni A., Lorber B., Heller J.P., Villasmil R., Bull N.D., Martin K.R., Tomarev S.I. Identification of retinal ganglion cell neuroprotection conferred by platelet-derived growth factor through analysis of the mesenchymal stem cell secretome. Brain 2013, 137:503-519.
58. Jones L.L., Oudega M., Bunge M.B., Tuszynski M.H. Neurotrophic factors, cellular bridges and gene therapy for spinal cord injury. J. Physiol. 2001, 533:83-89.
59. Jung G.L., Sun J., Petrowitz B., Riecken K., Kruszewski K., Jankowiak W., Kunst F., Skevas C., Richard G., Fehse B., Bartsch U. Genetically modified neural stem cells for a local and sustained delivery of neuroprotective factors to the dystrophic mouse retina. Stem Cells Transl. Med. 2013, 2:1001-1010.
60. Kalbermatten D.F., Schaakxs D., Kingham P.J., Wiberg M. Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat. Cell Tissue Res. 2011, 344:251-260.
61. Kang S.K., Lee D.H., Bae Y.C., Kim H.K., Baik S.Y., Jung J.S. Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp. Neurol. 2003, 183:355-366.
62. Kang K.N., Kim da Y., Yoon S.M., Lee J.Y., Lee B.N., Kwon J.S., Seo H.W., Lee I.W., Shin H.C., Kim Y.M., Kim H.S., Kim J.H., Min B.H., Lee H.B., Kim M.S. Tissue engineered regeneration of completely transected spinal cord using human mesenchymal stem cells. Biomaterials 2012, 33:4828-4835.
63. Karaoz E., Demircan P.C., Saglam O., Aksoy A., Kaymaz F., Duruksu G. Human dental pulp stem cells demonstrate better neural and epithelial stem cell properties than bone marrow-derived mesenchymal stem cells. Histochem. Cell Biol. 2011, 136:455-473.
64. Kiraly M., Porcsalmy B., Pataki A., Kadar K., Jelitai M., Molnar B., Hermann P., Gera I., Grimm W.D., Ganss B., Zsembery A., Varga G. Simultaneous PKC and cAMP activation induces differentiation of human dental pulp stem cells into functionally active neurons. Neurochem. Int. 2009, 55:323-332.
65. Kiraly M., Kadar K., Horvathy D.B., Nardai P., Racz G.Z., Lacza Z., Varga G., Gerber G. Integration of neuronally predifferentiated human dental pulp stem cells into rat brain in vivo. Neurochem. Int. 2011, 59:371-381.
66. Ko M.L., Hu D.N., Ritch R., Sharma S.C. The combined effect of brain-derived neurotrophic factor and a free radical scavenger in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2000, 41:2967-2971.
67. Ko M.L., Hu D.N., Ritch R., Sharma S.C., Chen C.F. Patterns of retinal ganglion cell survival after brain-derived neurotrophic factor administration in hypertensive eyes of rats. Neurosci. Lett. 2001, 305:139-142.
68. Kode J.A., Mukherjee S., Joglekar M.V., Hardikar A.A. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 2009, 11:377-391.
69. Lamb T.M., Knecht A.K., Smith W.C., Stachel S.E., Economides A.N., Stahl N., Yancopolous G.D., Harland R.M. Neural induction by the secreted polypeptide noggin. Science 1993, 262:713-718.
70. Lamba D.A., Reh T.A. Microarray characterization of human embryonic stem cell-derived retinal cultures. Invest. Ophthalmol. Vis. Sci. 2011, 52:4897-4906.
71. Lamba D.A., Karl M.O., Ware C.B., Reh T.A. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12769-12774.
72. Lamba D.A., Gust J., Reh T.A. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell 2009, 4:73-79.
73. Le Blanc K., Rasmusson I., Sundberg B., Gotherstrom C., Hassan M., Uzunel M., Ringden O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004, 363:1439-1441.
74. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I., Lanino E., Sundberg B., Bernardo M.E., Remberger M., Dini G., Egeler R.M., Bacigalupo A., Fibbe W., Ringden O., DCEGB M. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008, 371:1579-1586.
75. Lee J.Y., Shin J.M., Yeum C.E., Chae G.T., Chun M.H., Oh S.J. Intravitreal delivery of mesenchymal stem cells loaded onto hydrogel affects the regulatory expression of endogenous NGF and BDNF in ischemic rat retina. Tissue Eng. Regen. Med. 2012, 9:249-258.
76. Leong W.K., Henshall T.L., Arthur A., Kremer K.L., Lewis M.D., Helps S.C., Field J., Hamilton-Bruce M.A., Warming S., Manavis J., Vink R., Gronthos S., Koblar S.A. Human adult dental pulp stem cells enhance poststroke functional recovery through non-neural replacement mechanisms. Stem Cells Transl. Med. 2012, 1:177-187.
77. Levkovitch-Verbin H., Sadan O., Vander S., Rosner M., Barhum Y., Melamed E., Offen D., Melamed S. Intravitreal injections of neurotrophic factors secreting mesenchymal stem cells are neuroprotective in rat eyes following optic nerve transection. Invest. Ophthalmol. Vis. Sci. 2010, 51:6394-6400.
78. Li G.R., Deng X.L., Sun H., Chung S.S., Tse H.F., Lau C.P. Ion channels in mesenchymal stem cells from rat bone marrow. Stem Cells 2006, 24:1519-1528.
79. Liao J.L., Yu J., Huang K., Hu J., Diemer T., Ma Z., Dvash T., Yang X.J., Travis G.H., Williams D.S., Bok D., Fan G. Molecular signature of primary retinal pigment epithelium and stem-cell-derived RPE cells. Hum. Mol. Genet. 2010, 19:4229-4238.
80. Liu B., Hunter D.J., Rooker S., Chan A., Paulus Y.M., Leucht P., Nusse Y., Nomoto H., Helms J.A. Wnt signaling promotes Muller cell proliferation and survival after injury. Invest. Ophthalmol. Vis. Sci. 2013, 54:444-453.
81. Logan A., Ahmed Z., Baird A., Gonzalez A.M., Berry M. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 2006, 129:490-502.
82. Lu P., Jones L.L., Snyder E.Y., Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol. 2003, 181:115-129.
83. Lu P., Blesch A., Tuszynski M.H. Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact?. J. Neurosci. Res. 2004, 77:174-191.
84. Lu P., Yang H., Jones L.L., Filbin M.T., Tuszynski M.H. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J. Neurosci. 2004, 24:6402-6409.
85. Lu B., Malcuit C., Wang S., Girman S., Francis P., Lemieux L., Lanza R., Lund R. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 2009, 27:2126-2135.
86. Lu B., Wang S., Girman S., McGill T., Ragaglia V., Lund R. Human adult bone marrow-derived somatic cells rescue vision in a rodent model of retinal degeneration. Exp. Eye Res. 2010, 91:449-455.
87. Lu P., Wang Y., Graham L., McHale K., Gao M., Wu D., Brock J., Blesch A., Rosenzweig E.S., Havton L.A., Zheng B., Conner J.M., Marsala M., Tuszynski M.H. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 2012, 150:1264-1273.
88. Lu B., Morgans C.W., Girman S., Luo J., Zhao J., Du H., Lim S., Ding S., Svendsen C., Zhang K., Wang S. Neural stem cells derived by small molecules preserve vision. Transl. Vis. Sci. Technol. 2013, 2:1.
89. Machalińska A., Kawa M., Pius-Sadowska E., Stepniewski J., Nowak W., Rogińska D., Kaczyńska K., Baumert B., Wiszniewska B., Józkowicz A., Dulak J., Machaliński B. Long-term neuroprotective effects of NT-4-engineered mesenchymal stem cells injected intravitreally in a mouse model of acute retinal injury. Invest. Ophthalmol. Vis. Sci. 2013, 54:8292-8305.
90. Martin P.J., Uberti J.P., Soiffer R.J., Klingemann H., Waller E.K., Daly A., Herrmann R.P., Visani G., Bernardo M.E., Schwerdtfeger R., Kebriaei P. Prochymal (R) improves response rates in patients with steroid-refractory acute graft-versus-host disease involving the liver and gut: results of a randomized, placebo-controlled, multicentre phase III trial in GvHD. Bone Marrow Transplant. 2010, 45:S17.
91. Martino G., Pluchino S. The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 2006, 7:395-406.
92. McGill T.J., Cottam B., Lu B., Wang S., Girman S., Tian C., Huhn S.L., Lund R.D., Capela A. Transplantation of human central nervous system stem cells - neuroprotection in retinal degeneration. Eur. J. Neurosci. 2012, 35:468-477.
93. Mead B., Logan A., Berry M., Leadbeater W., Scheven B.A. Intravitreally transplanted dental pulp stem cells promote neuroprotection and axon regeneration of retinal ganglion cells after optic nerve injury. Invest. Ophthalmol. Vis. Sci. 2013, 54:7544-7556.
94. Mead B., Logan A., Berry M., Leadbeater W., Scheven B.A. Paracrine-mediated neuroprotection and neuritogenesis of axotomised retinal ganglion cells by human dental pulp stem cells: comparison with human bone marrow and adipose-derived mesenchymal stem cells. Plos One 2014, 9:e109305.
95. Mellough C.B., Cui Q., Spalding K.L., Symons N.A., Pollett M.A., Snyder E.Y., Macklis J.D., Harvey A.R. Fate of multipotent neural precursor cells transplanted into mouse retina selectively depleted of retinal ganglion cells. Exp. Neurol. 2004, 186:6-19.
96. Mendel T.A., Clabough E.B., Kao D.S., Demidova-Rice T.N., Durham J.T., Zotter B.C., Seaman S.A., Cronk S.M., Rakoczy E.P., Katz A.J., Herman I.M., Peirce S.M., Yates P.A. Pericytes derived from adipose-derived stem cells protect against retinal vasculopathy. Plos One 2013, 8:e65691.
97. Mey J., Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res. 1993, 602:304-317.
98. Meyer J.S., Katz M.L., Maruniak J.A., Kirk M.D. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells 2006, 24:274-283.
99. Meyer J.S., Shearer R.L., Capowski E.E., Wright L.S., Wallace K.A., McMillan E.L., Zhang S.C., Gamm D.M. Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16698-16703.
100. Morgan-Warren P.J., Berry M., Ahmed Z., Scott R.A., Logan A. Exploiting mTOR signaling: a novel translatable treatment strategy for traumatic optic neuropathy?. Invest. Ophthalmol. Vis. Sci. 2013, 54:6903-6916.
101. Nakano T., Ando S., Takata N., Kawada M., Muguruma K., Sekiguchi K., Saito K., Yonemura S., Eiraku M., Sasai Y. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 2012, 10:771-785.
102. Neuhuber B., Gallo G., Howard L., Kostura L., Mackay A., Fischer I. Reevaluation of in vitro differentiation protocols for bone marrow stromal cells: disruption of actin cytoskeleton induces rapid morphological changes and mimics neuronal phenotype. J. Neurosci. Res. 2004, 77:192-204.
103. Nishida A., Takahashi M., Tanihara H., Nakano I., Takahashi J.B., 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.
104. Nosrat C.A., Fried K., Lindskog S., Olson L. Cellular expression of neurotrophin mRNAs during tooth development. Cell Tissue Res. 1997, 290:569-580.
105. Nosrat I.V., Widenfalk J., Olson L., Nosrat C.A. Dental pulp cells produce neurotrophic factors, interact with trigeminal neurons in vitro, and rescue motoneurons after spinal cord injury. Dev. Biol. 2001, 238:120-132.
106. Ooto S., Akagi T., Kageyama R., Akita J., Mandai M., Honda Y., Takahashi M. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13654-13659.
107. Osakada F., Ooto S., Akagi T., Mandai M., Akaike A., Takahashi M. Wnt signaling promotes regeneration in the retina of adult mammals. J. Neurosci. 2007, 27:4210-4219.
108. Osakada F., Ikeda H., Mandai M., Wataya T., Watanabe K., Yoshimura N., Akaike A., Sasai Y., Takahashi M. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat. Biotechnol. 2008, 26:215-224.
109. Osakada F., Ikeda H., Sasai Y., Takahashi M. Stepwise differentiation of pluripotent stem cells into retinal cells. Nat. Protoc. 2009, 4:811-824.
110. Osakada F., Jin Z.B., Hirami Y., Ikeda H., Danjyo T., Watanabe K., Sasai Y., Takahashi M. In vitro differentiation of retinal cells from human pluripotent stem cells by small-molecule induction. J. Cell Sci. 2009, 122:3169-3179.
111. Pakulska M.M., Ballios B.G., Shoichet M.S. Injectable hydrogels for central nervous system therapy. Biomed. Mater. 2012, 7:024101.
112. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
113. Park S.S., Bauer G., Abedi M., Pontow S., Panorgias A., Jonnal R., Zawadzki R.J., Werner J.S., Nolta J. Intravitreal autologous bone marrow CD34+ cell therapy for ischemic and degenerative retinal disorders: preliminary phase 1 clinical trial findings. Invest. Ophthalmol. Vis. Sci. 2015, 56:81-89.
114. Pera E.M., Wessely O., Li S.Y., De Robertis E.M. Neural and head induction by insulin-like growth factor signals. Dev. Cell 2001, 1:655-665.
115. Phillips M.J., Wallace K.A., Dickerson S.J., Miller M.J., Verhoeven A.D., Martin J.M., Wright L.S., Shen W., Capowski E.E., Percin E.F., Perez E.T., Zhong X., Canto-Soler M.V., Gamm D.M. Blood-derived human iPS cells generate optic vesicle-like structures with the capacity to form retinal laminae and develop synapses. Invest. Ophthalmol. Vis. Sci. 2012, 53:2007-2019.
116. Pierdomenico L., Bonsi L., Calvitti M., Rondelli D., Arpinati M., Chirumbolo G., Becchetti E., Marchionni C., Alviano F., Fossati V., Staffolani N., Franchina M., Grossi A., Bagnara G.P. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 2005, 80:836-842.
117. Puissant N., Barreau C., Bourin P., Clavel C., Corre J., Bousquet C., Taureau C., Cousin B., Abbal M., Laharrague P., Penicaud L., Casteilla L., Blancher A. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Brit. J. Haematol. 2005, 129:118-129.
118. Pyle A.D., Lock L.F., Donovan P.J. Neurotrophins mediate human embryonic stem cell survival. Nat. Biotechnol. 2006, 24:344-350.
119. Reichenbach A., Bringmann A. New functions of Muller cells. Glia 2013, 61:651-678.
120. Reynolds J., Lamba D.A. Human embryonic stem cell applications for retinal degenerations. Exp. Eye Res. 2013, 123:151-160.
121. Richardson P.M., McGuinness U.M., Aguayo A.J. Axons from CNS neurons regenerate into PNS grafts. Nature 1980, 284:264-265.
122. Riess P., Zhang C., Saatman K.E., Laurer H.L., Longhi L.G., Raghupathi R., Lenzlinger P.M., Lifshitz J., Boockvar J., Neugebauer E., Snyder E.Y., McIntosh T.K. Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery 2002, 51:1043-1052. (Discussion 1052-1044).
123. Sakai K., Yamamoto A., Matsubara K., Nakamura S., Naruse M., Yamagata M., Sakamoto K., Tauchi R., Wakao N., Imagama S., Hibi H., Kadomatsu K., Ishiguro N., Ueda M. Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J. Clin. Investig. 2012, 122:80-90.
124. Salero E., Blenkinsop T.A., Corneo B., Harris A., Rabin D., Stern J.H., Temple S. Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives. Cell Stem Cell 2012, 10:88-95.
125. Sandvig A., Berry M., Barrett L.B., Butt A., Logan A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 2004, 46:225-251.
126. Schwartz S.D., Hubschman J.P., Heilwell G., Franco-Cardenas V., Pan C.K., Ostrick R.M., Mickunas E., Gay R., Klimanskaya I., Lanza R. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012, 379:713-720.
127. Schwartz S.D., Regillo C.D., Lam B.L., Eliott D., Rosenfeld P.J., Gregori N.Z., Hubschman J.P., Davis J.L., Heilwell G., Spirn M., Maguire J., Gay R., Bateman J., Ostrick R.M., Morris D., Vincent M., Anglade E., Del Priore L.V., Lanza R. Human embryonic stem cell-derived retinal pigment epithelium in patients with age-related macular degeneration and Stargardt's macular dystrophy: follow-up of two open-label phase 1/2 studies. Lancet 2014, 10.1016/S0140-6736(08)61345-8.
128. Sieving P.A., Caruso R.C., Tao W., Coleman H.R., Thompson D.J., Fullmer K.R., Bush R.A. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3896-3901.
129. Singer N.G., Caplan A.I. Mesenchymal stem cells: mechanisms of inflammation. Annu. Rev. Pathol. 2011, 6:457-478.
130. Singh T., Prabhakar S., Gupta A., Anand A. Recruitment of stem cells into the injured retina after laser injury. Stem Cells Dev. 2012, 21:448-454.
131. Siqueira R.C., Messias A., Voltarelli J.C., Scott I.U., Jorge R. Intravitreal injection of autologous bone marrow-derived mononuclear cells for hereditary retinaldystrophy: a phase I trial. Retina 2011, 31:1207-1214.
132. Sofroniew M.V., Howe C.L., Mobley W.C. Nerve growth factor signaling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 2001, 24:1217-1281.
133. Sommerfeld M.T., Schweigreiter R., Barde Y.A., Hoppe E. Down-regulation of the neurotrophin receptor TrkB following ligand binding. Evidence for an involvement of the proteasome and differential regulation of TrkA and TrkB. J. Biol. Chem. 2000, 275:8982-8990.
134. Strauss O. The retinal pigment epithelium in visual function. Physiol. Rev. 2005, 85:845-881.
135. Sugitani S., Tsuruma K., Ohno Y., Kuse Y., Yamauchi M., Egashira Y., Yoshimura S., Shimazawa M., Iwama T., Hara H. The potential neuroprotective effect of human adipose stem cells conditioned medium against light-induced retinal damage. Exp. Eye Res. 2013, 116:254-264.
136. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., Zhang K., Yeung C., Feng G., Yankner B.A., He Z. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480:372-375.
137. Tamaki Y., Nakahara T., Ishikawa H., Sato S. In vitro analysis of mesenchymal stem cells derived from human teeth and bone marrow. Odontology 2012, 101(2):121-132.
138. Tropepe V., Coles B.L., Chiasson B.J., Horsford D.J., Elia A.J., McInnes R.R., van der Kooy D. Retinal stem cells in the adult mammalian eye. Science 2000, 287:2032-2036.
139. Tsuruma K., Yamauchi M., Sugitani S., Otsuka T., Ohno Y., Nagahara Y., Ikegame Y., Shimazawa M., Yoshimura S., Iwama T., Hara H. Progranulin, a major secreted protein of mouse adipose-derived stem cells, inhibits light-induced retinal degeneration. Stem Cells Transl. Med. 2014, 3:42-53.
140. Tucker B.A., Park I.H., Qi S.D., Klassen H.J., Jiang C., Yao J., Redenti S., Daley G.Q., Young M.J. Transplantation of adult mouse iPS cell-derived photoreceptor precursors restores retinal structure and function in degenerative mice. Plos One 2011, 6:e18992.
141. Tzameret A., Sher I., Belkin M., Treves A.J., Meir A., Nagler A., Levkovitch-Verbin H., Barshack I., Rosner M., Rotenstreich Y. Transplantation of human bone marrow mesenchymal stem cells as a thin subretinal layer ameliorates retinal degeneration in a rat model of retinal dystrophy. Exp. Eye Res. 2014, 118:135-144.
142. Vallières L., Sawchenko P.E. Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity. J. Neurosci. 2003, 23:5197-5207.
143. Vugler A., Carr A.J., Lawrence J., Chen L.L., 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.
144. Wang H.C., Brown J., Alayon H., Stuck B.E. Transplantation of quantum dot-labelled bone marrow-derived stem cells into the vitreous of mice with laser-induced retinal injury: survival, integration and differentiation. Vis. Res. 2010, 50:665-673.
145. West E.L., Pearson R.A., Tschernutter M., Sowden J.C., MacLaren R.E., Ali R.R. Pharmacological disruption of the outer limiting membrane leads to increased retinal integration of transplanted photoreceptor precursors. Exp. Eye Res. 2008, 86:601-611.
146. Wilkins A., Kemp K., Ginty M., Hares K., Mallam E., Scolding N. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. 2009, 3:63-70.
147. Wilson S.W., Houart C. Early steps in the development of the forebrain. Dev. Cell 2004, 6:167-181.
148. Wright L.S., Phillips M.J., Pinilla I., Hei D., Gamm D.M. Induced pluripotent stem cells as custom therapeutics for retinal repair: progress and rationale. Exp. Eye Res. 2014, 123:161-172.
149. Xu H., Sta Iglesia D.D., Kielczewski J.L., Valenta D.F., Pease M.E., Zack D.J., Quigley H.A. Characteristics of progenitor cells derived from adult ciliary body in mouse, rat, and human eyes. Invest. Ophthalmol. Vis. Sci. 2007, 48:1674-1682.
150. Yañez R., Lamana M.L., García-Castro J., Colmenero I., Ramírez M., Bueren J.A. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 2006, 24:2582-2591.
151. Ye C.Q., Yuan X.D., Liu H., Cai Y.A., Ou Y. Ultrastructure of neuronal-like cells differentiated from adult adipose-derived stromal cells. Neural. Regen. Res. 2010, 5:1456-1463.
152. 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.
153. Yu H., Vu T.H., Cho K.S., Guo C., Chen D.F. Mobilizing endogenous stem cells for retinal repair. Transl. Res. 2014, 163:387-398.
154. Zhang Y., Wang W. Effects of bone marrow mesenchymal stem cell transplantation on light-damaged retina. Invest. Ophthalmol. Vis. Sci. 2010, 51:3742-3748.
155. Zhang R., Zhang H., Xu L., Ma K., Wallrapp C., Jonas J.B. Neuroprotective effect of intravitreal cell-based glucagon-like peptide-1 production in the optic nerve crush model. Acta Ophthalmol. 2011, 89:e320-e326.
156. Zhou Z., Chen Y., Zhang H., Min S., Yu B., He B., Jin A. Comparison of mesenchymal stem cells from human bone marrow and adipose tissue for the treatment of spinal cord injury. Cytotherapy 2013, 15(4):434-448.
157. Zwart I., Hill A.J., Al-Allaf F., Shah M., Girdlestone J., Sanusi A.B., Mehmet H., Navarrete R., Navarrete C., Jen L.S. Umbilical cord blood mesenchymal stromal cells are neuroprotective and promote regeneration in a rat optic tract model. Exp. Neurol. 2009, 216:439-448.