Astrocytes as stem cells: Nomenclature, phenotype, and translation

GLIA

Volumn 43, Issue 1, 2003, Pages 62-69

  Steindler, Dennis A ^a   Laywell, Eric D ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Astrocyte; Gliomagenesis; Neural repair; Phenotypy; Stem cell

Indexed keywords

ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CARCINOGENESIS; CELL CLONE; CELL FUNCTION; CELL GROWTH; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; GLIA CELL; HUMAN; NERVE CELL DIFFERENTIATION; NEUROLOGIC DISEASE; NOMENCLATURE; NONHUMAN; PHENOTYPE; STEM CELL;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; HUMANS; NEUROGLIA; NEURONS; PHENOTYPE; STEM CELLS;

EID: 0038643444     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.10242     Document Type: Article

References (77)

1. Aboody KS, et al. 2000. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial tumors. Proc Natl Acad Sci USA 97:12846-12851.
2. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. 2001. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2:287-293.
3. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970.
4. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. 1998. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats: similarities to astrocyte grafts. Proc Natl Acad Sci USA 95:3908-3913.
5. Brazelton TR, Rossi FM, Keshet GI, Blau HM. 2000. From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775-1779.
6. Brodkey JA, Laywell ED, O'Brien TF, Faissner A, Stefansson K, Dorries U, Schachner M, Steindler DA. 1995. Focal brain injury and the upregulation of a developmentally-regulated extracellular matrix protein. J Neurosurg 82:106-112.
7. Cai J, Wu Y, Mirua T, Pierce JL, Lucero MT, Albertin KH, Spangrude GJ, Rao JS. 2002. Properties of a fetal multipotent neural stem cell (NEP cell). Dev Biol 251:221-240.
8. Cameron RS, Rakic P. 1991. Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4:124-137.
9. Cooper NGF, Steindler DA. 1986. Monoclonal antibody to glial fibrillary acidic protein reveals a parcellation of individual barrels in the early postnatal mouse somatosensory cortex. Brain Res 380:341-348.
10. Corbo JC, Deuel TA, Long JM, LaPorte P, Tsai E, Wynshaw-Boris A, Walsh CA. 2002. Doublecortin is required in mice for lamination of the hippocampus but not neocortex. J Neursci 22:7548-7557.
11. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL. 1990. Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J Neurosci 10:684-692.
12. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
13. Eliasson C., Sahlgren C, Berthold CH, Stakeberg J, Celis JE, Betscholtz C, Eriksson JE, Pekny M. 1999. Intermediate filament protein partnership in astrocytes. J Biol Chem 274:23996-234006.
14. Gaiano N, Fishell G. 2002. The role of notch in promoting glial and neural stem cell fates. Ann Rev Neurosci 25:471-490.
15. Galli R, Borelo U, Gritti A, Minasi MG, Bjornson C, Coletta M, Mora M, De Angelis MG, Fiocco R, Cossu G, Vescovi AL. 2000. Skeletal myogenic potential of human and mouse neural stem cells. Nat Neurosci 3:986-991.
16. Gates MA, Thomas LB, Howard E, Laywell ED, Sajin B, Faissner A, Silver J, Steindler DA. 1995. A cell and molecular analysis of the developing and adult mouse subependymal zone of the cerebral hemispheres. J Comp Neurol 361:249-266.
17. Gensert JM, Goldman JE. 2001. Heterogeneity of cycling glial progenitors in the adult mammalian cortex and white matter. J Neurobiol 48:75-86.
18. Geschwind DH, Ou J, Easterday MC, Dougherty JD, Jackson RL, Chen Z, Antoine H, Terskikh A, Weissman IL, Nelson SF, Kornblum HI. 2001. A genetic analysis of neural progenitor differentiation. Neuron 29:325-339.
19. Grant MB, May WS, Caballero S, Brown GA, Guthrie SM, Mames RN, Byrne BJ, Vaught T, Spoerri PE, Peck AB, Scott EW. 2002. Adult hematopoietic stem cells provide functional hemanglioblast activity during retinal neovascularization. Nat Med 8:607-612.
20. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, Barde YA, Götz M. 2002. Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 5:308-315.
21. Herrup K, Busser JC. 1995. The induction of multiple cell cycle events precedes target-related neuronal death. Development 121:2385-2395.
22. Ignatova T, Kukekov VG, Laywell ED, Suslov ON, Vrionis F, Steindler DA. 2002. Human cortical glial tumors contain stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39:193-206.
23. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. 2002. A stem cell molecular signature. Science 298:601-604.
24. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
25. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34.
26. Kabos P, Ehtesham M, Kabosova A, Black KL, Yu JS. 2002. Generation of neural progenitor cells from whole adult bone marrow. Exp Neurol 178:288-293.
27. Kernie SG, Erwin TM, Parada LF. 2001. Brain remodelling due to neuronal and astrocytic proliferation after controlled cortical injury in mice. J Neurosci Res 66:317-326.
28. Kondo T, Raff M. 2000. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754-1756.
29. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. 2001. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105:369-377.
30. Kukekov VG, Laywell ED, Thomas LB, Scheffler B, Davies K, O'Brien TF, Kusakabe M, Steindler DA. 1999. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 156:333-344.
31. Kusakabe M, Mangiarini L, Laywell ED, Bates GP, Steindler DA. 2001. Loss of cortical and thalamic neuronal tenascin-C expression in a transgenic mouse expressing exon 1 of the human Huntington disease gene. J Comp Neurol 430:485-500.
32. Laywell ED, Bartsch U, Dorries U, Bartsch S, Faissner A, Schachner M, Steindler DA. 1992. Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc Natl Acad Sci USA 89:2634-2638.
33. Laywell ED, Rakic P, Kukekov VG, Holland E, Steindler DA. 2000. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 97:13883-13888.
34. Laywell ED, Steindler DA. 2002. Glial stem-like cells: implications for ontogeny, phylogeny, and CNS regeneration. Prog Brain Res 138:437-452.
35. Leavitt BR, Hernit-Grant CS, Macklis JD. 1999. Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp Neurol 157:43-57.
36. Lendahl U, Zimmerman LB, McKay RDG. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
37. Lie DC, Dziewczapolski G, Willhoite AR, Kaspar BK, Shults CW, Gage FH. 2002. The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 22:6639-6649.
38. Magavi SS, Macklis JD. 2002. Manipulation of neural precursors in situ. In: Zigova T, Snyder EY, Sanberg PR, editors. Neural stem cells for brain and spinal cord repair. Totowa, NJ: Humana Press. p 229-267.
39. Marmur R, Mabie PC, Gokhan S, Song Q, Kessler JA, Mehler MF. 1998. Isolation and developmental characterization of cerebral cortical multipotent progenitors. Dev Biol 204:577-591.
40. McKay R. 1997. Stem cells in the central nervous system. Science 276:66-71.
41. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714-720.
42. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR. 2002. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22:3161-3173.
43. Nowakowski RS, Hayes, NL. 2000. New neurons: extraordinary evidence or extraordinary conclusion. Science 286:548-552.
44. Palmer TD, Willhoite AR, Gage FR. 2000. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494.
45. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61-84.
46. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. 2002. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298:597-600.
47. Redmond L, Hockfield S, Morabito M. 1996. The divergent homeobox gene PBX1 is expressed in the postnatal subventricular zone and interneurons of the olfactory bulb. J Neurosci 16:2972-2982.
48. Reh TA. 2002. Neural stem cells: form and function. Nat Neurosci 5:392-394.
49. Reya T, Morrison SJ, Clarke JF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105-111.
50. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
51. Richards LJ, Kilpatrick TJ, Bartlett PF. 1992. De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci USA 89:8591-8595.
52. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. 2001. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412:690-691.
53. Sanchez-Ramos JS, Song F, Cardozo-Pelaez C, Hazzi T, Stedeford A, Willing TB, Freeman TB, Saporta S, Janssen W, Patel N, Cooper DR, Sanberg PR. 2000. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164:247-256.
54. Scheffler B, Horn M, Bluemcke I, Laywell ED, Coomes D, Kukekov VG, Steindler DA. 1999. Marrow-mindedness: a perspective on neuropoiesis. Trends Neurosci 22:348-357.
55. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153.
56. Snyder EY, Yoon C, Flax J, Macklis JD. 1997. Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc Natl Acad Sci USA 94:11663-11668.
57. Soriano E, Alvarado-Mallart RM, Dumesnil N, Del Rio JA, Sotelo C. 1997. Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18:563-577.
58. Staugaitis SM, Zerlin M, Hawkes R, Levine JM, Goldman JE. 2001. Aldolase c/zebrin II expression in the neonatal rat forebrain reveals cellular heterogeneity within the subventricular zone and early astrocytic differentiation. J Neurosci 21:6195-6205.
59. Steindler DA, Cooper NGF, Faissner A, Schachner M. 1989. Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. Dev Biol 131:243-260.
60. Steindler DA, O'Brien TF, Laywell, E, Harrington K, Faissner A, Schachner M. 1990. Boundaries during normal and abnormal brain development: in vivo and in vitro studies of glia and glycoconjugates. Exp Neurol 109:35-56.
61. Steindler DA. 1993. Glial boundaries in the developing nervous system. Ann Rev Neurosci 16:445-470.
62. Steindler DA, Kadrie T, Fillmore H, Thomas, L. 1996. The subependymal zone: "brain marrow." Prog Brain Res 108:349-363.
63. Steindler DA. 2002. Neural stem cells, scaffolds, and chaperones. Nat Biotech 20:1091-1093.
64. Steindler DA, Pincus D. 2002. Stem cells and neuropoiesis in the adult human brain. Lancet 359:1047-1054.
65. Steindler DA, Scheffler B, Zheng T, Laywell ED, Suslov ON, Kukekov VG. 2002. Neural stem/progenitor cell clones or "neurospheres": a model for understanding neuromorphogenesis. In: Zigova T, Snyder EY, Sanberg PR, editors. Neural stem cells for brain repair. Totowa, NJ: Humana Press. p 183-201.
66. Stoykova A, Gruss P. 1994. Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J Neurosci 14:1395-1412.
67. Suslov O, Kukekov VG, Ignatova T, Steindler DA. 2002. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres in vitro. Proc Natl Acad Sci USA 99:1456-14511.
68. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Petersen BE, Scott EW. 2002. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416:542-545.
69. Thomas LB, Gates MA, Steindler DA. 1996. Young neurons from the adult mouse subependymal zone migrate and proliferate along an astrocyte, extracellular matrix-rich pathway. Glia 17:1-14.
70. Tsai RYL, McKay RDG. 2000. Cell contact regulates fate choice by cortical stem cells. J Neurosci 20:3725-3735.
71. Tsai RYL, McKay DG. 2002. A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev 16:2991-3003.
72. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. 2002. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297:2256-2259.
73. Woodbury D, Schwarz EJ, Prockop DJ, Black I. 2000. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61:364-370.
74. Yang X, Zhong R, Heintz N. 1996. Granule cell specification in the developing mouse brain as defined by expression of the zinc finger transcription factor RU49. Development 122:555-566.
75. Ying QL, Nichols J, Evans EP, Smith AG. 2002. Changing potency by spontaneous fusion. Nature 416:485-487.
76. Zheng T, Steindler DA, Laywell ED. 2002. Transplantation of an indigenous neural stem cell population leading to hyperplasia and atypical integration. Cloning Stem Cells 4:3-8.
77. Zigova T, Betarbet R, Soteres BJ, Brock BJ, Bakay RA, Luskin MB. 1996. A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotypically transplanted telencephalic ventricular zone cells. Dev Biol 173:459-474.