Spinal cord neuroblasts proliferate in response to basic fibroblast growth factor

Journal of Neuroscience

Volumn 14, Issue 6, 1994, Pages 3548-3564

  Ray, Jasodhara ^a   Gage, Fred H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

basic fibroblast growth factor; perpetual neuronal cultures; proliferation of neuroblasts; spinal cord neuroblasts; stable gene transfer

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BETA GALACTOSIDASE; EPIDERMAL GROWTH FACTOR; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; EMBRYO DEVELOPMENT; GENE TRANSFER; GENETIC TRANSDUCTION; GROWTH REGULATION; MITOGENESIS; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR AFFINITY; SPINAL CORD;

EID: 0028238394     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.14-06-03548.1994     Document Type: Article

References (74)

1. Alderson RF, Alterman AL, Barde Y-A, Lindsay RM (1990) Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5:297-306.
2. Altman J, Bayer SA (1984) The development of rat spinal cord. In: Advances in anatomy, embryology and cell biology, Vol 85 (Beck F, Hild W, van Limborgh J, Ortmann R, Pauly JE, Schiebler TH, eds), pp 1-166. Berlin: Springer.
3. Arakawa Y, Sendtner M, Thoenen H (1990) Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J Neurosci 10:3507-3515.
4. Assouline JG, Pantazis NJ (1989) Detection of a nerve growth factor receptor on fetal human schwann cells in culture: absence of the receptor on fetal human astrocytes. Dev Brain Res 45:1-14.
5. Bottenstein JE, Sato G (1980) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 76: 514-517.
6. Cattaneo E, McKay RDG (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347: 762-765.
7. Cepko CL (1988) Immortalization of neuronal cells via oncogene transduction. Trends Neurosci 11:6-8.
8. Cepko CL (1989) Immortalization of neural cells via retrovirus-mediated oncogene transduction. Annu Rev Neurosci 12:47-65.
9. Chiu AY, Chen EW, Loera S (1993) A motor neuron-specific epitope and the low-affinity nerve growth factor receptor display reciprocal patterns of expression during development, axotomy, and regeneration. J Comp Neurol 328:351-363.
10. Cordon-Cardo C, Tapley P, Jing S, Nanduri V, O'Rourke E, Lamballe F, Kovary K, Klein R, Jones KR, Reichardt LF, Barbacid M (1991) The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 66:173-183.
11. Deloulme JC, Baudier J, Sensenbrenner M (1991) Establishment of pure neuronal cultures from fetal rat spinal cord and proliferation of the neuronal precursor cells in the presence of fibroblast growth factor. J Neurosci Res 29:499-509.
12. Digby J, Harrison R, Jehanli A, Lunt GG, Clifford-Rose F (1985) Cultured rat spinal cord neurons: interaction with motor neuron disease immunoglobulins. Muscle Nerve 8:595-605.
13. Dionne CA, Crumley G, Bellot F, Kaplow JM, Searfoss G, Ruta M, Burgess WH, Jaye M, Schlessinger J (1990) Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J 9:2685-2692.
14. Drago J, Murphy M, Carroll SM, Harvey RP, Bartlett PF (1991) Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc Natl Acad Sci USA 88:2199-2203.
15. Erkman L, Touzeau G, Bertrand D, Bader CR, Kato AC (1989) Characterization of dissociated monolayer cultures of human spinal cord. Brain Res Bull 22:57-65.
16. Gensburger C, Labourdette G, Sensenbrenner M (1987) Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett 217:1-5.
17. Gonzales A-M, Buscaglia M, Ong M, Baird A (1990) Distribution of basic fibroblast growth factor in the 18-day rat fetus: localization in the basement membranes of diverse tissues. J Cell Biol 110:753-765.
18. Hatikka J, Hefti F (1988) Comparison of nerve growth factor's effects on development of septum, striatum, and nucleus basalis cholinergic neurons in vitro. J Neurosci Res 21:352-364.
19. Hatten ME, Lynch M, Rydel RE, Sanchez J, Joseph-Silverstein J, Moscatelli D, Rifkin DB (1988) In vitro neunte extension by granule neurons is dependent upon astroglia-derived growth factor. Dev Biol 125:280-289.
20. Hughes RA, Sendtner M, Goldfarb M, Lindholm D, Thoenen H (1993) Evidence that fibroblast growth factor 5 is a major muscle-derived survival factor for cultured spinal motoneurons. Neuron 10:369-377.
21. Hughes SM, Lillien LE, Raff MC, Rohrer H, Sendtner M (1988) Ciliary neurotrophic factor induced type-2 astrocyte differentiation in culture Nature 335:70-73.
22. NGFR TrkA, and TrkB mRNA in rat C6 glioma and type I astrocyte cultures. J Neurosci Res 32:375-383.
23. Ip NY, Li Y, Yancopoulos GD, Lindsay RM (1993) Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J Neurosci 13:3394-3405.
24. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991) The trk proto-oncogene product: a signal transducing receptor for the nerve growth factor. Science 252:554-558.
25. Kato H, Wanaka A, Tohyama M (1992) Co-localization of basic fibroblast growth factor-like immunoreactivity and its receptor mRNA in the rat spinal cord and the dorsal root ganglion. Brain Res 576: 351-354.
26. Keegan K, Johnson DE, Williams LT, Hyman MJ (1991) Isolation of an additional member of the fibroblast growth factor receptor family, FGFR-3. Proc Natl Acad Sci USA 88:1095-1099.
27. Kilpatrick TJ, Bartlet PF (1993) Cloning and growth of multipotential neuronal precursors: requirements for proliferation and differentiation. Neuron 10:255-265.
28. Klagsbrun M, Baird A (1991) A dual receptor system is required for basic fibroblast growth factor activity. Cell 67:229-231.
29. Klein R, Jing S, Nanduri V, O'Rourke E, Barbacid M (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 66: 967-979.
30. Kornblum HI, Raymon HK, Morrison RS, Cavanaugh KP, Bradshaw RA, Leslie FM (1990) Epidermal growth factor and basic fibroblast growth factor: effects on an overlapping population of neocortical neurons in vitro. Brain Res 535:255-263.
31. Kornbluth S, Paulson KE, Hanafusa H (1988) Novel tyrosine kinase identified by phosphotyrosine antibody screening of cDNA libraries. Mol Cell Biol 8:5541-5544.
32. Landon RM, Robbins RJ (1986) Somatostatin release from dissociated cerebral cortical cell cultures. Methods Enzymol 124:412-424.
33. Leber SM, Breedlove SM, Sanes JR (1990) Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J Neurosci 10:2451-2462.
34. Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT (1989) Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245:57-60.
35. Lendhal U, McKay RDG (1990) The use of cell lines in neurobiology. Trends Neurosci 13:132-137.
36. Liu L, Nicoll CS (1988) Evidence for a role of basic fibroblast growth factor in rat embryonic growth and differentiation. Endocrinology 123:2027-2031.
37. Luskin MB, Pearlman AL, Sanes JR (1988) Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1:635-647.
38. Luskin MB, Parnavelas JG, Barfield JA (1993) Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J Neurosci 13:1730-1750.
39. Magal E, Burnham P, Varon S (1991) Effects of ciliary neuronotrophic factor on rat spinal cord neurons in vitro: survival and expression of choline acetyltransferase and low-affinity nerve growth factor receptors. Dev Brain Res 63:141-150.
40. McManaman JL, Smith RJ, Appel SH (1985) Low molecular weight peptide stimulates cholinergic development in ventral spinal cord cultures. Dev Biol 112:248-252.
41. Morrison RS, Sharma A, de Vellis J, Bradshaw RA (1986) Basic fibroblast growth factor supports the survival of cerebral cortical neurons in primary culture. Proc Natl Acad Sci USA 83:7537-7541.
42. Morrison RS, Kornblum HI, Leslie FM, Bradshaw RA (1987) Trophic stimulation of cultured neurons from neonatal rat brain by epidermal growth factor. Science 238:72-75.
43. Morrison RS, Keating RF, Moskal JR (1988) Basic fibroblast growth factor and epidermal growth factor exert differential trophic effects on CNS neurons. J Neurosci Res 21:71-79.
44. Murphy M, Drago J, Bartlett PF (1990) Fibroblast growth factor stimulates the proliferation and differentiation of neuronal precursor cells in vitro. J Neurosci Res 25:463-475.
45. Noble M, Murry K (1984) Purified astrocytes promote the in vitro division of a bipotential glial progenitor cell. EMBO J 3:2243-2247.
46. Noble M, Murry K, Stroobant P, Waterfield MD, Riddle P (1988) Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 333:560-562.
47. Nornes HO, Das GD (1972) Temporal pattern of neurogenesis in spinal cord: cytoarchitecture and directed growth of axons. Proc Natl Acad Sci USA 69:1962-1966.
48. 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.
49. Ohashi T, Boggs S, Robbins P, Bahnson A, Patrene K, Wei F-S, Wei J-F, Li J, Lucht L, Fei Y, Clark S, Kimak M, He H, Mowery-Rushton P, Barranger JA (1992) Efficient transfer and sustained high expression of the human glucocerebrosidase gene in mice and their functional macrophages following transplantation of bone marrow transduced by a retroviral vector. Proc Natl Acad Sci USA 89:11332-11336.
50. Oppenheim RW (1986) The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. J Comp Neurol 246:281-286.
51. Partanen J, Makela TP, Eerola E, Korhonen J, Hirvonen H, Claesson-Welsh L, Alitalo K (1991) FGFR-4, a novel acidic fibroblast growth factor receptor with a distinct expression pattern. EMBO J 10:1347-1354.
52. Perraud F, Besnard F, Pettmenn B, Sensenbrenner M, Labourdette G (1988) Effects of acidic and basic fibroblast growth factors (aFGF and bFGF) on the proliferation and the glutamine synthetase expression of rat astroblasts in culture. Glia 1:124-131.
53. Phelps PE, Barber RP, Vaughn JE (1988) Generation patterns of four groups of cholinergic neurons in rat cervical spinal cord: a combined tritiated thymidine autoradiographic and choline acetyltransferase immunocytochemical study. J Comp Neurol 273:459-472.
54. Price J, Thurlow L (1988) Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104:473-482.
55. Price J, Turner D, Cepko C (1987) Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc Natl Acad Sci USA 84:156-160.
56. Raff MC (1989) Glial cell diversification in the rat optic nerve. Science 243:1450-1455.
57. Ray J, Peterson DA, Schinstine M, Gage FH (1993) Proliferation, differentiation and long-term culture of primary hippocampal neurons. Proc Natl Acad Sci USA 90:3602-3606.
58. Renfranz PJ, Cunningham MG, McKay RDG (1991) Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell 66:713-729.
59. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
60. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574.
61. Ryder EF, Snyder EY, Cepko CL (1989) Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J Neurobiol 21:356-375.
62. Sanes JR, Rubenstein JLR, Nicols J-F (1986) Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J 5:3133-3142.
63. Sendtner M, Arakawa Y, Stockli KA, Kreutzberg GW, Thoenen H (1991) Effect of ciliary neurotrophic factor (CNTF) on motoneuron survival. J Cell Sci [Suppl] 15:103-109.
64. Smith RG, Appel SH (1983) Extracts of skeletal muscle increase neurite outgrowth and cholinergic activity of fetal rat spinal motor neurons. Science 219:1079-1081.
65. Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartweig EA, Cepko CL (1992) Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 68:33-51.
66. Stemple DL, Anderson DJ (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:973-985.
67. Walicke PA (1988) Basic and acidic fibroblast growth factors have trophic effects on neurons from multiple CNS regions. J Neurosci 8:2618-2627.
68. Walicke PA, Baird A (1988) Neurotrophic effects of basic and acidic fibroblast growth factors are not mediated through glia cells. Dev Brain Res 40:71-79.
69. Walicke P, Cowan WM, Ueno N, Baird A, Guillemin R (1986) Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neunte extension. Proc Natl Acad Sci USA 83:3012-3016.
70. Walicke PA, Feige J-J, Baird A (1989) Characterization of the neuronal receptor for basic fibroblast growth factor and comparison to receptors on mesenchymal cells. J Biol Chem 264:4120-4126.
71. Wanaka A, Johnson EM, Milbrandt J (1990) Localization of FGF receptor mRNA in the adult rat central nervous system by in situ hybridization. Neuron 5:288-292.
72. Wanaka A, Milbrandt J, Johnson EM (1991) Expression of FGF receptor gene in rat development. Development 111:455-468.
73. Williams BP, Read J, Price J (1991) The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7:685-693.
74. Yan Q, Johnson EM (1988) An immunohistochemical study of the nerve growth factor (NGF) receptor in developing rats. J Neurosci 8:3481-3498.