Disguising adult neural stem cells

Current Opinion in Neurobiology

Volumn 14, Issue 1, 2004, Pages 125-131

  Morshead, Cindi M ^a   Van Der Kooy, Derek ^b  

^a Department of Surgery   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Dentate gyrus; DG; EGF; Epidermal growth factor; Ganciclovir; GCV; GFAP; Glial fibrillary acidic protein; SE; Side population; SP; Subependyma; Thymidine kinase; Tk

Indexed keywords

BIOLOGICAL MARKER;

BRAIN NERVE CELL; CELL MATURATION; FOREBRAIN; IN VIVO STUDY; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 1342306690     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2004.01.008     Document Type: Review

References (47)

1. Seaberg R.M., van der Kooy D. Stem and progenitor cells: the premature disertion of rigorous definitions. Trends Neurosci. 26:2003;125-131.
2. Bjornson C.R., Rietze R.L., Reynolds B.A., Magli M.C., Vescovi A.L. Turning brain into blood: a hematopoetic fate adopted by adult neural stem cells in vivo. Science. 283:1999;534-537.
3. 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. 3:2000;986-991.
4. Mezey E., Chandross K.J., Harta G., Marki R.A., McKercher S.R. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science. 290:2000;1779-1782.
5. 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. 288:2000;1660-1663.
6. Krause D.S. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 105:2001;369-377.
7. Morrison S.J. Stem cell potential: can anything make anything? Curr Biol. 11:2001;R7-9.
8. Ying Q.L., Nichols J., Evans E.P., Smith A.G. Changing potency by spontaneous fusion. Nature. 416:2002;545-548.
9. Alvarez-Dolado M, Parda IR, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois C, Morrison SJ, Alvarez-Buylla A: Fusion of bone-marrow-derived cells with purkinje neurons, cardiomyocytes and hepatocytes. Nature.
10. Morshead C.M., Benveniste P., Iscove N.N., van der Kooy D. Hematopoietic competence is a rare property of neural stem cells and may depend on genetic and epigenetic alterations. Nat Med. 8:2002;268-273 This was the first report that directly refuted the claims of neural stem cell plasticity and proposed that cellular transformation could account for the original report by Bjornson et al. [2]. It was the first report in a chain of many to provide alternative explanations for the claims of robust stem cell plasticity.
11. Potten C.S., Loeffler M. Stem cell: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development. 110:1990;1001-1020.
12. Fuchs E., Segre J.A. Stem cells: a new lease on life. Cell. 100:2000;143-155.
13. 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.
14. Reynolds B.A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol. 175:1996;1-13.
15. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., Weiss S., van der Kooy D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron. 13:1994;1071-1082.
16. Johansson C.B., Momma S., Clarke D.L., Risling M., Lendahl U., Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 96:1999;25-34.
17. Chiasson B.J., Tropepe V., Morshead C.M., van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci. 19:1999;4462-4471.
18. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neuronal stem cells in the adult mammalian brain. Cell. 97:1999;703-716.
19. Laywell E.D., Raki P., Kukekov V.G., Holland E.C., Steindler D.A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci U S A. 97:2000;13883-13888.
20. Morshead C.M., van der Kooy D. A new 'spin' on neural stem cells? Curr Opin Neurobiol. 11:2001;59-65.
21. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 11:1993;173-189.
22. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 264:1994;1145-1148.
23. Cameron H.A., Woolley C.S., McEwan B.S., Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience. 56:1993;337-344.
24. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 16:1996;2027-2033.
25. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 425:2000;479-494.
26. Seri B., Garcia-Verdugo J.M., McEwan B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 21:2001;7153-7160.
27. Seaberg R.M., van der Kooy D. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci. 22:2002;1784-1793 The paper highlights the fact that not all neurospheres are derived from neural stem cells. Indeed, the hippocampus contains neural and glial progenitors and not neural stem cells.
28. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 17:1997;5046-5061.
29. Morshead C.M., Craig C.G., van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development. 125:1998;2251-2261.
30. Morshead C.M., Garcia A.D., Sofroniew M.V., van der Kooy D. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur J Neurosci. 18:2003;76-84 This is the first loss of function report of the effect of selective depletion of GFAP expressing cells from the adult subependyma. Importantly, the selective ablation is done both in vivo and in vitro, and in either case the loss of neural stem cells (assayed by examining neurosphere formation) is observed.
31. Frank K.B., Chiou J.-F., Cheng Y.-C. Interaction of herpes simplex virus-induced DNA polymerase with 9-(1,3-dihydroxy-2-propoxymethyl) gyanin triphosphate. J Biol Chem. 259:1989;1566-1569.
32. Borelli E., Heyman R.A., Aria C., Sawchenko P.E., Evans R.M. Transgenic mice with inducible dwarfism. Nature. 339:1994;538-541.
33. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron. 36:2002;1021-1034 This report challenges the idea that neurosphere formation is a good indicator of neural stem cells and indeed, purports that neurospheres are derived from neural stem cell progeny, the Dlx2 positive transit amplifying cells in vitro. The loss of function experiments are only performed in vitro and hence the conclusions drawn are premature but provocative.
34. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A. 96:1999;11619-11624.
35. Weissman I.L. Stem cells: units of development, units of regeneration, and units of evolution. Cell. 100:2000;157-168.
36. Gritti A., Frolichsthal-Schoeller P., Galli R., Parati E.A., Cova L., Pagano S.F., Bjornson C.R., Vescovi A.L. Epidermal and fibroblast growth factor behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci. 19:1999;3287-3297.
37. Tropepe V., Sibilia M., Ciruna B.G., Rossant J., Wagner E.F., van der Kooy D. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol. 208:1999;166-188.
38. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature. 417:2002;39-44.
39. ••].
40. Kim M, Morshead CM: Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J Neurosci 2003, in press.
41. Goodell M.A., Brose K., Paradis B., Conner A.S., Mulligan R.D. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 183:1996;1797-1806.
42. Gritti A., Parati E.A., Cova L., Frolichsthal P., Galli R., Wanke E., Faravelli L., Morassutti D.J., Roisen F., Nickel D.D., Vescovi A.L. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci. 16:1996;1091-1100.
43. Kawaguchi A., Miyata T., Sawamoto K., Takashita N., Murayama A., Akamatsu W., Ogawa M., Okabe M., Tano Y., Goldman S.A., Okano H. Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci. 17:2001;259-273.
44. Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as non-ependymal. Neuron. 35:2002;865-875 The authors present a nice study to identify markers that are expressed on neural stem cells. The very low frequency of neural stem cells makes this work difficult. Importantly, they show a correlation between in vivo and in vitro expression of LeX/ssea1 in the adult brain.
45. Reitze R.L., Valcanis H., Brooker G.F., Tomas T., Voss A.K., Bartlett P.F. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature. 412:2001;736-739.
46. Murayama A., Matsuzaki Y., Kawaguchi A., Shimazaki T., Okano H. Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. J Neurosci Res. 69:2002;837-847.
47. ••].