Engrafted neural progenitor cells express a tissue-restricted reporter gene associated with differentiated retinal photoreceptor cells

Cell Transplantation

Volumn 15, Issue 2, 2006, Pages 147-160

  Sam, Thien N ^a   Xiao, Jing ^a   Roehrich, Heidi ^a   Low, Walter C ^a   Gregerson, Dale S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cell differentiation; Immunofluorescence; Immunohistochemistry; Mice, transgenic; Neural proteins; Neurons; Photoreceptor cells; Progenitor cell transplantation; Retina; Stem cell transplantation

Indexed keywords

BETA GALACTOSIDASE; DNA; RETINA S ANTIGEN;

ANIMAL CELL; ANTERIOR EYE CHAMBER; ARTICLE; BRAIN TISSUE; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONCENTRATION RESPONSE; EMBRYO; GENE EXPRESSION REGULATION; HISTOCHEMISTRY; ISOGRAFT; MOUSE; NEUROPROTECTION; NONHUMAN; PERITONEAL CAVITY; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; STAINING; STEM CELL TRANSPLANTATION; SURVIVAL; TISSUE REACTION;

ANIMALS; ARRESTIN; BETA-GALACTOSIDASE; BRAIN; BRAIN CHEMISTRY; CELL DIFFERENTIATION; CELL MOVEMENT; DNA; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HISTOCYTOCHEMISTRY; MICE; MICE, TRANSGENIC; NEURONS; PERITONEAL CAVITY; PHOTORECEPTORS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); RETINA; RETINAL DISEASES; SPLEEN; STEM CELL TRANSPLANTATION; STEM CELLS;

MURINAE; MUS MUSCULUS;

EID: 33646569924     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/000000006783982098     Document Type: Article

References (64)

1. Akashi, K.; Reya, T.; Dalma-Weiszhausz, D.; Weissman, I. L. Lymphoid precursors. Curr. Opin. Immunol. 12:144-150; 2000.
2. Akashi, K.; Traver, D.; Miyamoto, T.; Weissman, I. L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404:193-197; 2000.
3. Akita, J.; Takahashi, M.; Hojo, M.; Nishida, A.; Haruta, M.; Honda, Y. Neuronal differentiation of adult rat hippocampus-derived neural stem cells transplanted into embryonic rat explanted retinas with retinoic acid pretreatment. Brain Res. 954:286-293; 2002.
4. Alison, M.; Sarraf, C. Hepatic stem cells. J. Hepatol. 29:676-682; 1998.
5. Altshuler, D.; Lo Turco, J. J.; Rush, J.; Cepko, C. Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119:1317-1328; 1993.
6. Avichezer, D.; Liou, G. I.; Chan, C. C.; Lewis, G. M.; Wiggert, B.; Donoso, L. A.; Nickerson, J. M.; Crawford, M. A.; Caspi, R. R. Interphotoreceptor retinoid-binding protein (IRBP)-deficient C57BL/6 mice have enhanced immunological and immunopathogenic responses to IRBP and an altered recognition of IRBP epitopes. J. Autoimmun. 21:185-194; 2003.
7. Berson, E. L. Nutrition and retinal degenerations. Int. Ophthalmol. Clin. 40:93-111; 2000.
8. Bjornson, C. R.; Rietze, R. L.; Reynolds, B. A.; Magli, M. C.; Vescovi, A. L. Turning brain into blood: A hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534-537; 1999.
9. 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. 43:937-946; 2003.
10. Clarke, D. L.; Johansson, C. B.; Wilbertz, J.; Veress, B.; Nilsson, E.; Karlstrom, H.; Lendahl, U.; Frisen, J. Generalized potential of adult neural stem cells. Science 288:1660-1663; 2000.
11. Constable, I. J. Age-related macular degeneration and its possible prevention. Despite well publicised claims of the therapeutic value of dietary supplements and other new treatments, the evidence for their effectiveness is modest. Med. J. Aust. 181:471-472; 2004.
12. Delyfer, M. N.; Leveillard, T.; Mohand-Said, F; Hicks, D.; Picaud, S.; Sahel, J. A. Inherited retinal degenerations: Therapeutic prospects. Biol. Cell 96:261-269; 2004.
13. Dong, X.; Pulido, J. S.; Qu, T.; Sugaya, K. Differentiation of human neural stem cells into retinal cells. Neuroreport 14:143-146; 2003.
14. Ferrari, G.; Cusella-De Angelis, G.; Coletta, M.; Paolucci, E.; Stornaiuolo, A.; Cossu, G.; Mavilio, F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528-1530; 1998.
15. Fuchs, E.; Segre, J. A. Stem cells: A new lease on life. Cell 100:143-155; 2000.
16. Gage, F. H. Mammalian neural stem cells. Science 287:1433-1438; 2000.
17. Galli, R.; Borello, U.; Gritti, A.; Minasi, M. G.; Bjornson, C.; Coletta, M.; Mora, M.; De Angelis, M. G.; Fiocco, R.; Cossu, G.; Vescovi, A. L. Skeletal myogenic potential of human and mouse neural stem cells. Nat. Neurosci. 3:986-991; 2000.
18. Gregerson, D. S.; Dou, C. Spontaneous induction of immunoregulation by an endogenous retinal protein. Invest. Ophthalmol. Vis. Sci. 43:2984-2991; 2002.
19. Gregerson, D. S.; Torseth, J. W.; McPherson, S. W.; Roberts, J. P.; Shinohara, T.; Zack, D. J. Retinal expression of a neo-self antigen, beta-galactosidase, is not tolerogenic, and creates a target for autoimmune uveoretinitis. J. Immunol. 163:1073-1080; 1999.
20. Gregerson, D. S.; Xiao, J. Failure of memory (CD44 high) CD4 T cells to recognize their target antigen in retina. J. Neuroimmunol. 120:34-41; 2001.
21. Gronthos, S.; Zannettino, A. C.; Graves, S. E.; Ohta, S.; Hay, S. J.; Simmons, P. J. Differential cell surface expression of the STRO-1 and alkaline phosphatase antigens on discrete developmental stages in primary cultures of human bone cells. J. Bone Miner. Res. 14:47-56; 1999.
22. Hara, A.; Niwa, M.; Kunisada, T.; Yoshimura, N.; Katayama, M.; Kozawa, O.; Mori, H. Embryonic stem cells are capable of generating a neuronal network in the adult mouse retina. Brain Res. 999:216-221; 2004.
23. Haynesworth, S. E.; Goshima, J.; Goldberg, V. M.; Caplan, A. I. Characterization of cells with osteogenic potential from human marrow. Bone 13:81-88; 1992.
24. Jackson, K. A.; Mi, T.; Goodell, M. A. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc. Natl. Acad. Sci. USA 96:14482-14486; 1999.
25. Jiang, Y.; Henderson, D.; Blackstad, M.; Chen, A.; Miller, R. F.; Verfaillie, C. M. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc. Natl. Acad. Sci. USA 100:11854-11860; 2003.
26. Jiang, Y.; Jahagirdar, B. N.; Reinhardt, R. L.; Schwartz, R. E.; Keene, C. D.; Ortiz-Gonzalez, X. R.; Reyes, M.; Lenvik, T.; Lund, T.; Blackstad, M.; Du, J.; Aldrich, S.; Lisberg, A.; Low, W. C.; Largaespada, D. A.; Verfaillie, C. M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49; 2002.
27. Kick, A.; Shen, W. Y.; Wilson, A. S.; Constable, I. J.; Robertson, T.; Rakoczy, P. E. Differentiation of marrow stromal cells into photoreceptors in the rat eye. J. Neurosci. 23:7742-7749; 2003.
28. Klassen, H. J.; Ng, T. F.; Kurimoto, Y.; Kirov, I.; Shatos, M.; Coffey, P.; Young, M. J. Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest. Ophthalmol. Vis. Sci. 45:4167-4173; 2004.
29. Liu, M.; Regillo, C. D. A review of treatments for macular degeneration: A synopsis of currently approved treatments and ongoing clinical trials. Curr. Opin. Ophthalmol. 15:221-226; 2004.
30. Magrassi, L.; Castello, S.; Ciardelli, L.; Podesta, M.; Gasparoni, A.; Conti, L.; Pezzotta, S.; Frassoni, F.; Cattaneo, E. Freshly dissociated fetal neural stem/progenitor cells do not turn into blood. Mol. Cell. Neurosci. 22:179-187; 2003.
31. McPherson, S. W.; Yang, J.; Chan, C. C.; Dou, C.; Gregerson, D. S. Resting CD8 T cells recognize beta-galactosidase expressed in the immune privileged retina, and mediate autoimmune disease when activated. Immunology 110:386-396; 2003.
32. Meyer, J. S.; Katz, M. L.; Maruniak, J. A.; Kirk, M. D. Neural differentiation of mouse embryonic stem cells in vitro and after transplantation into eyes of mutant mice with rapid retinal degeneration. Brain Res. 1014:131-144; 2004.
33. Mezey, E.; Chandross, K. J.; Harta, G.; Maki, R. A.; McKercher, S. R. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290:1779-1782; 2000.
34. Moles, J. P.; Watt, F. M. The epidermal stem cell compartment: Variation in expression levels of E-cadherin and catenins within the basal layer of human epidermis. J. Histochem. Cytochem. 45:867-874; 1997.
35. Morshead, C. M.; Benveniste, P.; Iscove, N. N.; van der Kooy, D. Hematopoietic competence is a rare property of neural stem cells that may depend on genetic and epigenetic alterations. Nat. Med. 8:268-273; 2002.
36. Namba, K.; Ogasawara, K.; Kitaichi, N.; Matsuki, N.; Takahashi, A.; Sasamoto, Y.; Kotake, S.; Matsuda, H.; Iwabuchi, K.; Ohno, S.; Onoe, K. Identification of a peptide inducing experimental autoimmune uveoretinitis (EAU) in H-2Ak-carrying mice. Clin. Exp. Immunol. 111:442-449; 1998.
37. Neophytou, C.; Vernallis, A. B.; Smith, A.; Raff, M. C. Muller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development. Development 124:2345-2354; 1997.
38. 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. 41:4268-4274; 2000.
39. Orkin, S. H. Embryonic stem cells and transgenic mice in the study of hematopoiesis. Int. J. Dev. Biol. 42:927-934; 1998.
40. Petersen, B. E.; Bowen, W. C.; Patrene, K. D.; Mars, W. M.; Sullivan, A. K.; Murase, N.; Boggs, S. S.; Greenberger, J. S.; Goff, J. P. Bone marrow as a potential source of hepatic oval cells. Science 284:1168-1170; 1999.
41. Phelan, J. K.; Bok, D. A brief review of retinitis pigmentosa and the identified retinitis pigmentosa genes. Mol. Vis. 6:116-124; 2000.
42. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147; 1999.
43. Potten, C. S.; Booth, C.; Pritchard, D. M. The intestinal epithelial stem cell: the mucosal governor. Int. J. Exp. Pathol. 78:219-243; 1997.
44. Qiu, G.; Seiler, M. J.; Mui, C.; Arai, S.; Aramant, R. B.; de Juan, Jr., E.; Sadda, S. Photoreceptor differentiation and integration of retinal progenitor cells transplanted into transgenic rats. Exp. Eye Res. 80:515-525; 2005.
45. Reh, T. A.; Levine, E. M. Multipotential stem cells and progenitors in the vertebrate retina. J. Neurobiol. 36:206-220; 1998.
46. Reynolds, B. A.; Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710; 1992.
47. Richards, L. J.; Kilpatrick, T. J.; Bartlett, P. F. De novo generation of neuronal cells from the adult mouse brain. Proc. Natl. Acad. Sci. USA 89:8591-8595; 1992.
48. Sakakibara, S.; Imai, T.; Hamaguchi, K.; Okabe, M.; Aruga, J.; Nakajima, K.; Yasutomi, D.; Nagata, T.; Kurihara, Y.; Uesugi, S.; Miyata, T.; Ogawa, M.; Mikoshiba, K.; Okano, H. Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176:230-242; 1996.
49. Shamblott, M. J.; Axelman, J.; Wang, S.; Bugg, E. M.; Littlefield, J. W.; Donovan, P. J.; Blumenthal, P. D.; Huggins, G. R.; Gearhart, J. D. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc. Natl. Acad. Sci. USA 95:13726-13731; 1998.
50. Song, H.; Stevens, C. F.; Gage, F. H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44; 2002.
51. Sternberg, Jr., P.; Lewis, H. Photodynamic therapy for age-related macular degeneration: A candid appraisal. Am. J. Ophthalmol. 137:483-485; 2004.
52. Sunayashiki-Kusuzaki, K.; Kikuchi, T.; Wawrousek, E. F.; Shinohara, T. Arrestin and phosducin are expressed in a small number of brain cells. Mol. Brain Res. 52:112-120; 1997.
53. Takahashi, M.; Palmer, T. D.; Takahashi, J.; Gage, F. H. Widespread integration and survival of adult-derived neural progenitor cells in the developing optic retina. Mol. Cell. Neurosci. 12:340-348; 1998.
54. Takahashi, T.; Kalka, C.; Masuda, H.; Chen, D.; Silver, M.; Kearney, M.; Magner, M.; Isner, J. M.; Asahara, T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat. Med. 5:434-438; 1999.
55. Terskikh, A. V.; Easterday, M. C.; Li, L.; Hood, L.; Kornblum, H. I.; Geschwind, D. H.; Weissman, I. L. From hematopoiesis to neuropoiesis: Evidence of overlapping genetic programs. Proc. Natl. Acad. Sci. USA 98:7934-7939; 2001.
56. Theise, N. D.; Badve, S.; Saxena, R.; Henegariu, O.; Sell, S.; Crawford, J. M.; Krause, D. S. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31:235-240; 2000.
57. Thomson, J. A.; Kalishman, J.; Golos, T. G.; Durning, M.; Harris, C. P.; Becker, R. A.; Hearn, J. P. Isolation of a primate embryonic stem cell line. Proc. Natl. Acad. Sci. USA 92:7844-7848; 1995.
58. Thomson, J. A.; Marshall, V. S. Primate embryonic stem cells. Curr. Top. Dev. Biol. 38:133-165; 1998.
59. 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 287:2032-2036; 2000.
60. Voo, I.; Small, K. W. Update on the genetics of macular dystrophies. Retina 24:591-601; 2004.
61. Weimann, J. M.; Johansson, C. B.; Trejo, A.; Blau, H. M. Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant. Nat. Cell Biol. 5:959-966; 2003.
62. Weleber, R. G.; Kurz, D. E.; Trzupek, K. M. Treatment of retinal and choroidal degenerations and dystrophies: Current status and prospects for gene-based therapy. Ophthalmol. Clin. North Am. 16:583-593; 2003.
63. Young, M. J.; Ray, J.; Whiteley, S. J.; Klassen, H.; Gage, F. H. Neuronal differentiation and morphological integration of hippocampal progenitor cells transplanted to the retina of immature and mature dystrophic rats. Mol. Cell. Neurosci. 16:197-205; 2000.
64. Yusta-Boyo, M. J.; Gonzalez, M. A.; Pavon, N.; Martin, A. B.; De La Fuente, R.; Garcia-Castro, J.; De Pablo, F.; Moratalla, R.; Bernad, A.; Vicario-Abejon, C. Absence of hematopoiesis from transplanted olfactory bulb neural stem cells. Eur. J. Neurosci. 19:505-512; 2004.