The neurogenic competence of progenitors from the postnatal rat retina in vitro

Experimental Eye Research

Volumn 78, Issue 5, 2004, Pages 1025-1036

  Engelhardt, Maren ^a   Wachs, Frank Peter ^a   Couillard Despres, Sebastien ^a   Aigner, Ludwig ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Ciliary body; Differentiation; Neural stem cells; Neuronal precursors; Subventricular zone

Indexed keywords

BETA TUBULIN; BIOCHEMICAL MARKER; BROXURIDINE; DOUBLECORTIN; GALACTOSYLCERAMIDASE; GLIAL FIBRILLARY ACIDIC PROTEIN; HOMEOBOX PROTEIN CHX10; HOMEODOMAIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; NEURON SPECIFIC ENOLASE; PROTEOGLYCAN; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CILIARY BODY; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; MALE; NEWBORN; NONHUMAN; OLIGODENDROGLIA; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA DEVELOPMENT; RETINA NERVE CELL; STEM CELL;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; FEMALE; MALE; MICROSCOPY, FLUORESCENCE; NEUROGLIA; NEURONS; OLIGODENDROGLIA; RATS; RATS, LONG-EVANS; RETINA; STEM CELLS;

EID: 1642462114     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2003.12.002     Document Type: Article

References (43)

1. Ahmad I., Dooley C.M., Thoreson W.B., Rogers J.A., Afiat S. In vitro analysis of a mammalian retinal progenitor that gives rise to neurons and glia. Brain Res. 831:1999;1-10.
2. Ahmad I., Tang L., Pham H. Identification of neural progenitors in the adult mammalian eye. Biochem. Biophys. Res. Commun. 270:2000;517-521.
3. Akagi T., Haruta M., Akita J., Nishida A., Honda Y., Takahashi M. Different characteristics of rat retinal progenitor cells from different culture periods. Neurosci. Lett. 341:2003;213-216.
4. 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. 954:2002;286-293.
5. Alexiades M.R., Cepko C.L. Subsets of retinal progenitors display temporally regulated and distinct biases in the fates of their progeny. Development. 124:1997;1119-1131.
6. Anchan R.M., Reh T.A. Transforming growth factor-beta-3 is mitogenic for rat retinal progenitor cells in vitro. J. Neurobiol. 28:1995;133-145.
7. Anchan R.M., Reh T.A., Angello J., Balliet A., Walker M. EGF and TGF-alpha stimulate retinal neuroepithelial cell proliferation in vitro. Neuron. 6:1991;923-936.
8. Arsenijevic Y. Mammalian neural stem-cell renewal: nature versus nurture. Mol. Neurobiol. 27:2003;73-98.
9. Bhattacharya S., Jackson J.D., Das A.V., Thoreson W.B., Kuszynski C., James J., Joshi S., Ahmad I. Direct identification and enrichment of retinal stem cells/progenitors by Hoechst dye efflux assay. Invest. Ophthalmol. Vis. Sci. 44:2003;2764-2773.
10. 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. Vision Res. 43:2003;937-946.
11. Chacko D.M., Rogers J.A., Turner J.E., Ahmad I. Survival and differentiation of cultured retinal progenitors transplanted in the subretinal space of the rat. Biochem. Biophys. Res. Commun. 268:2000;842-846.
12. Couillard-Despres S., Winkler J., Uyanik G., Aigner L. Molecular mechanisms of neuronal migration disorders. Curr. Mol. Med. 1:2001;677-688.
13. Fischer A.J., Reh T.A. Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat. Neurosci. 4:2001;247-252.
14. Gage F.H. Mammalian neural stem cells. Science. 287:2000;1433-1438.
15. Gage F.H., Ray J., Fisher L.J. Isolation, characterization, and use of stem cells from the CNS. Ann. Rev. Neurosci. 18:1995;159-192.
16. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell. 92:1998;63-72.
17. Hartfuss E., Galli R., Heins N., Gotz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229:2001;15-30.
18. Hitchcock P.F., Macdonald R.E., VanDeRyt J.T., Wilson S.W. Antibodies against Pax6 immunostain amacrine and ganglion cells and neuronal progenitors, but not rod precursors, in the normal and regenerating retina of the goldfish. J. Neurobiol. 29:1996;399-413.
19. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Nat. Acad. Sci. USA. 99:2002;11946-11950.
20. Kilpatrick T.J., Bartlett P.F. Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J. Neurosci. 15:1995;3653-3661.
21. Kurimoto Y., Shibuki H., Kaneko Y., Ichikawa M., Kurokawa T., Takahashi M., Yoshimura N. Transplantation of adult rat hippocampus-derived neural stem cells into retina injured by transient ischemia. Neurosci. Lett. 306:2001;57-60.
22. Lendahl U., Zimmerman L.B., McKay R.D., stem C.N.S. cells express a new class of intermediate filament protein. Cell. 60:1990;585-595.
23. Levine J.M., Nishiyama A. The NG2 chondroitin sulfate proteoglycan: a multifunctional proteoglycan associated with immature cells. Perspect Dev. Neurobiol. 3:1996;245-259.
24. Liu I.S., Chen J.D., Ploder L., Vidgen D., van der Kooy D., Kalnins V.I., McInnes R.R. Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron. 13:1994;377-393.
25. McGinnis J.F., Stepanik P.L., Chen W., Elias R., Cao W., Lerious V. Unique retina cell phenotypes revealed by immunological analysis of recoverin expression in rat retina cells. J. Neurosci. Res. 55:1999;252-260.
26. McKay R. Stem cells in the central nervous system. Science. 276:1997;66-71.
27. 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. 41:2000;4268-4274.
28. Palmer T.D., Markakis E.A., Willhoite A.R., Safar F., Gage F.H. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 19:1999;8487-8497.
29. Rao M.S., Noble M., Mayer-Proschel M. A tripotential glial precursor cell is present in the developing spinal cord. Proc. Nat. Acad. Sci. USA. 95:1998;3996-4001.
30. Reynolds B.A., Tetzlaff W., Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12:1992;4565-4574.
31. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255:1992;1707-1710.
32. Sharon D., Blackshaw S., Cepko C.L., Dryja T.P. Profile of the genes expressed in the human peripheral retina, macula, and retinal pigment epithelium determined through serial analysis of gene expression (SAGE). Proc. Nat. Acad. Sci. USA. 99:2002;315-320.
33. Svendsen C.N., ter Borg M.G., Armstrong R.J., Rosser A.E., Chandran S., Ostenfeld T., Caldwell M.A. A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods. 85:1998;141-152.
34. 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. 12:1998;340-348.
35. 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. 287:2000;2032-2036.
36. Vinores S.A., Derevjanik N.L., Mahlow J., Hackett S.F., Haller J.A., deJuan E., Frankfurter A., Campochiaro P.A. Class III beta-tubulin in human retinal pigment epithelial cells in culture and in epiretinal membranes. Exp. Eye Res. 60:1995;385-400.
37. Vroemen M., Aigner L., Winkler J., Weidner N. Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur. J. Neurosci. 18:2003;743-751.
38. Wachs F.P., Couillard-Despres S., Engelhardt M., Wilhelm D., Ploetz S., Vroemen M., Kaesbauer J., Uyanik G., Klucken J., Karl C., Tebbing J., Svendsen C., Weidner N., Kuhn H.G., Winkler J., Aigner L. High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest. 83:2003;949-962.
39. Warfvinge K., Kamme C., Englund U., Wictorin K. Retinal integration of grafts of brain-derived precursor cell lines implanted subretinally into adult, normal rats. Exp. Neurol. 169:2001;1-12.
40. Yamaguchi T.P., Dumont D.J., Conlon R.A., Breitman M.L., Rossant J. flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development. 118:1993;489-498.
41. Yang K., Cepko C.L. Flk-1, a receptor for vascular endothelial growth factor (VEGF), is expressed by retinal progenitor cells. J. Neurosci. 16:1996;6089-6099.
42. 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. 16:2000;197-205.
43. Young R.W. Cell proliferation during postnatal development of the retina in the mouse. Brain Res. 353:1985;229-239.