Cell lineage and regional identity of cultured spinal cord neural stem cells and comparison to brain-derived neural stem cells

PLoS ONE

Volumn 4, Issue 1, 2009, Pages

  Kelly, Theresa K ^a,b   Karsten, Stanislav L ^c   Geschwind, Daniel H ^a,b   Kornblum, Harley I ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UCLA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CELL NUCLEUS RECEPTOR; HOX PROTEIN; HOXD10 PROTEIN; MITOGENIC AGENT; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTION FACTOR IRX3; TRANSCRIPTION FACTOR LEX; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR PACE4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CELL LINEAGE; CELL RENEWAL; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL CULTURE; NONHUMAN; SPINAL CORD NERVE CELL; ANIMAL; ANIMAL EMBRYO; BRAIN; COMPARATIVE STUDY; CYTOLOGY; NERVE CELL; SPINAL CORD; STEM CELL;

ANIMALS; BRAIN; CELL LINEAGE; EMBRYO, MAMMALIAN; MICE; NEURONS; SPINAL CORD; STEM CELLS;

EID: 62649083772     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004213     Document Type: Article

References (61)

1. Pluchino S, Zanotti L, Deleidi M, Martino G (2005) Neural stem cells and their use as therapeutic tool in neurological disorders. Brain Res Brain Res Rev 48: 211-219.
2. Kornblum HI, Geschwind DH (2001) Molecular markers in CNS stem cell research: hitting a moving target. Nat Rev Neurosci 2: 843-846.
3. Hitoshi S, Tropepe V, Ekker M, van der Kooy D (2002) Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain. Development 129: 233-244.
4. Ostenfeld T, Joly E, Tai YT, Peters A, Caldwell M, et al. (2002) Regional specification of rodent and human neurospheres. Brain Res Dev Brain Res 134: 43-55.
5. Watanabe K, Nakamura M, Iwanami A, Fujita Y, Kanemura Y, et al. (2004) Comparison between fetal spinal-cord- and forebrain-derived neural stem/ progenitor cells as a source of transplantation for spinal cord injury. Dev Neurosci 26: 275-287.
6. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, et al. (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16: 7599-7609.
7. Zappone MV, Galli R, Catena R, Meani N, De Biasi S, et al. (2000) Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 127: 2367-2382.
8. Kim HT, Kim IS, Lee IS, Lee JP, Snyder EY, et al. (2006) Human neurospheres derived from the fetal central nervous system are regionally and temporally specified but are not committed. Exp Neurol 199: 222-235.
9. He W, Ingraham C, Rising L, Goderie S, Temple S (2001) Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis. J Neurosci 21: 8854-8862.
10. Shihabuddin LS, Ray J, Gage FH (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 148: 577-586.
11. Gabay L, Lowell S, Rubin LL, Anderson DJ (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40: 485-499.
12. Brock SC, Bonsall J, Luskin MB (1998) The neuronal progenitor cells of the forebrain subventricular zone: intrinsic properties in vitro and following transplantation. Methods 16: 268-281.
13. Yang H, Mujtaba T, Venkatraman G, Wu YY, Rao MS, et al. (2000) Region-specific differentiation of neural tube-derived neuronal restricted progenitor cells after heterotopic transplantation. Proc Natl Acad Sci U S A 97: 13366-13371.
14. Santa-Olalla J, Baizabal JM, Fregoso M, del Carmen Cardenas M, Covarrubias L (2003) The in vivo positional identity gene expression code is not preserved in neural stem cells grown in culture. Eur J Neurosci 18: 1073-1084.
15. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Gotz M (2004) Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol Cell Neurosci 25: 664-678.
16. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765.
17. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, et al. (2003) Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425: 962-967.
18. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
19. Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, et al. (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176: 230-242.
20. Geschwind DH, Ou J, Easterday MC, Dougherty JD, Jackson RL, et al. (2001) A genetic analysis of neural progenitor differentiation. Neuron 29: 325-339.
21. Tsai RY, McKay RD (2002) A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev 16: 2991-3003.
22. Simeone A, Gulisano M, Acampora D, Stornaiuolo A, Rambaldi M, et al. (1992) Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. Embo J 11: 2541-2550.
23. Kimura J, Suda Y, Kurokawa D, Hossain ZM, Nakamura M, et al. (2005) Emx2 and Pax6 function in cooperation with Otx2 and Otx1 to develop caudal forebrain primordium that includes future archipallium. J Neurosci 25: 5097-5108.
24. Herault Y, Beckers J, Kondo T, Fraudeau N, Duboule D (1998) Genetic analysis of a Hoxd-12 regulatory element reveals global versus local modes of controls in the HoxD complex. Development 125: 1669-1677.
25. Kukekov VG, Laywell ED, Thomas LB, Steindler DA (1997) A nestin-negative precursor cell from the adult mouse brain gives rise to neurons and glia. Glia 21: 399-407.
26. Nakano I, Paucar AA, Bajpai R, Dougherty JD, Zewail A, et al. (2005) Maternal embryonic leucine zipper kinase (MELK) regulates multipotent neural progenitor proliferation. J Cell Biol 170: 413-427.
27. Dennis C (2003) Draft guidelines ease restrictions on use of genome sequence data. Nature 421: 877-878.
28. Carpenter EM (2002) Hox genes and spinal cord development. Dev Neurosci 24: 24-34.
29. Roy K, Kuznicki K, Wu Q, Sun Z, Bock D, et al. (2004) The Tlx gene regulates the timing of neurogenesis in the cortex. J Neurosci 24: 8333-8345.
30. Shi Y, Chichung Lie D, Taupin P, Nakashima K, Ray J, et al. (2004) Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427: 78-83.
31. Bishop KM, Goudreau G, O'Leary DD (2000) Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288: 344-349.
32. Tao W, Lai E (1992) Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron 8: 957-966.
33. Nornes HO, Das GD (1974) Temporal pattern of neurogenesis in spinal cord of rat. I. An autoradiographic study-time and sites of origin and migration and settling patterns of neuroblasts. Brain Res 73: 121-138.
34. Nornes HO, Das GD (1972) Temporal pattern of neurogenesis in spinal cord: cytoarchitecture and directed growth of axons. Proc Natl Acad Sci U S A 69: 1962-1966.
35. Capela A, Temple S (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35: 865-875.
36. Capela A, Temple S (2006) LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev Biol 291: 300-313.
37. Bartsch D, Mai JK (1991) Distribution of the 3-fucosyl-N-acetyl-lactosamine (FAL) epitope in the adult mouse brain. Cell Tissue Res 263: 353-366.
38. Ashwell KW, Mai JK (1997) Developmental expression of the CD15-epitope in the brainstem and spinal cord of the mouse. Anat Embryol (Berl) 196: 13-25.
39. Kim M, Morshead CM (2003) Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J Neurosci 23: 10703-10709.
40. Imura T, Nakano I, Kornblum HI, Sofroniew MV (2006) Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 53: 277-293.
41. Kalyani AJ, Mujtaba T, Rao MS (1999) Expression of EGF receptor and FGF receptor isoforms during neuroepithelial stem cell differentiation. J Neurobiol 38: 207-224.
42. Kalyani A, Hobson K, Rao MS (1997) Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev Biol 186: 202-223.
43. Ciccolini F, Svendsen CN (1998) Fibroblast growth factor 2 (FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: identification of neural precursors responding to both EGF and FGF-2. J Neurosci 18: 7869-7880.
44. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, et al. (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208: 166-188.
45. Irvin DK, Dhaka A, Hicks C, Weinmaster G, Kornblum HI (2003) Extrinsic and intrinsic factors governing cell fate in cortical progenitor cultures. Dev Neurosci 25: 162-172.
46. Yamamoto S, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M (2001) Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp Neurol 172: 115-127.
47. Tanabe Y, Jessell TM (1996) Diversity and pattern in the developing spinal cord. Science 274: 1115-1123.
48. Qian X, Goderie SK, Shen Q, Stern JH, Temple S (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125: 3143-3152.
49. Parmar M, Skogh C, Bjorklund A, Campbell K (2002) Regional specification of neurosphere cultures derived from subregions of the embryonic telencephalon. Mol Cell Neurosci 21: 645-656.
50. Machon O, Backman M, Krauss S, Kozmik Z (2005) The cellular fate of cortical progenitors is not maintained in neurosphere cultures. Mol Cell Neurosci 30: 388-397.
51. Na E, McCarthy M, Neyt C, Lai E, Fishell G (1998) Telencephalic progenitors maintain anteroposterior identities cell autonomously. Curr Biol 8: 987-990.
52. Horiguchi S, Takahashi J, Kishi Y, Morizane A, Okamoto Y, et al. (2004) Neural precursor cells derived from human embryonic brain retain regional specificity. J Neurosci Res 75: 817-824.
53. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, et al. (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100: 15178-15183.
54. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
55. Taylor MD, Poppleton H, Fuller C, Su X, Liu Y, et al. (2005) Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8: 323-335.
56. Wachs FP, Couillard-Despres S, Engelhardt M, Wilhelm D, Ploetz S, et al. (2003) High efficacy of clonal growth and expansion of adult neural stem cells. Lab Invest 83: 949-962.
57. Kornblum HI, Hussain R, Wiesen J, Miettinen P, Zurcher SD, et al. (1998) Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor. J Neurosci Res 53: 697-717.
58. Verdugo RA, Medrano JF (2006) Comparison of gene coverage of mouse oligonucleotide microarray platforms. BMC Genomics 7: 58.
59. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
60. Lobo MK, Karsten SL, Gray M, Geschwind DH, Yang XW (2006) FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat Neurosci 9: 443-452.
61. Karsten SL, Kudo LC, Jackson R, Sabatti C, Kornblum HI, et al. (2003) Global analysis of gene expression in neural progenitors reveals specific cell-cycle, signaling, and metabolic networks. Dev Biol 261: 165-182.