Heparin, but not other proteoglycans potentiates the mitogenic effects of FGF-2 on mesencephalic precursor cells

Experimental Neurology

Volumn 152, Issue 1, 1998, Pages 1-10

  Caldwell, Maeve A ^a   Svendsen, Clive N ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

EGF; FGF 2; Heparin; Neural stem cell; Precursor; Proteoglycan

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE; FIBROBLAST GROWTH FACTOR 2; HEPARIN; HYALURONIC ACID; KERATIN; PROTEOGLYCAN; SODIUM CHLORATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; IMMUNOCYTOCHEMISTRY; MESENCEPHALON; MITOGENESIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; STEM CELL;

EID: 0031843933     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1998.6815     Document Type: Article

References (63)

1. Anderson, K. J., D. Dam, S. Lee, and C. W. Cotman. 1988. Basic fibroblast growth factor prevents death of lesioned cholinergic neurons in vivo. Nature 332: 360-361.
2. Aviezer, D., E. Levy, M. Safran, C. Svahn, E. Buddecke, A. Schmidt, G. David, I. Vlodavsky, and A. Yayon. 1994. Differential structural requirements of heparin and heparan sulfate proteoglycans that promote binding of basic fibroblast growth factor to its receptor. J. Biol. Chem. 269: 114-121.
3. Baeuerle, P. A., and W. B. Huttner. 1986. Chlorate-a potent inhibitor of protein sulfation in intact-cells. Biochem. Biophys. Res. Commun. 141: 870-877.
4. Baird, A. 1994. Fibroblast growth factors: Activities and significance of non-neurotropin neurotropic growth factors. Curr. Opin. Neurobiol. 4: 78-86.
5. Basilico, C., and D. Moscatelli. 1992. The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59: 115-165.
6. Bernard, O., M. Li, and H. H. Reid. 1991. Expression of two different forms of fibroblast growth factor receptor 1 in different mouse tissue and cell lines. Proc. Natl. Acad. Sci. USA 88: 7625-7629.
7. Bouvier, M. M., and C. Mytilineou. 1995. Basic fibroblast growth factor increases division and delays differentiation of dopamine precursors in vitro. J. Neurosci. 15: 7141-7149.
8. Butler, H., and B. H. J. Juurlink. 1987. Mouse and Rat. In An Atlas for Staging Mammalian and Chick Embryos (H. Butler and B. H. J. Juurlink, Eds.), pp. 89-102. CRC Press, FL.
9. Casper, D., C. Mytilineou, and M. Blum. 1991. EGF enhances the survival of dopamine neurons in rat embryonic mesencephalon primary cell culture. J. Neurosci. Res. 30: 372-381.
10. Casper, D., G. J. Roboz, and M. Blum. 1994. Epidermal growth factor and basic fibroblast growth factor have independent actions on mesencephalic dopamine neurons in culture. J. Neurochem. 62: 2166-2177.
11. Damon, D. H., P. A. D'Amore, and J. A. Wagner. 1988. Sulfated glycosaminoglycans modify growth factor-induced neurite out-growth in PC12 cells. J. Cell Physiol. 135: 293-300.
12. Dunnett, S. B., and A. Bjorklund. 1992. Staging and dissection of rat embryos. In Neural Transplantation: A Practical Approach (S. B. Dunnett and A. Bjorklund, Eds.), pp. 1-18. Oxford Univ. Press, New York.
13. Faham, S., R. E. Hileman, J. R. Fromm, R. J. Linhardt, and D. C. Rees. 1996. Heparin structure and interactions with basic fibroblast growth factor. Science 271: 1116-1120.
14. Gage, F. H., J. Ray, and L. J. Fisher. 1995. Isolation, Characterization and use of stem cells from the CNS. Annu. Rev. Neurosci. 18: 159-192.
15. Gensburger, C., G. Labourdette, and M. Sensenbrenner. 1987. Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett. 217: 1-5.
16. Gomez-Pinilla, F., S. Miller, J. Choi, and C. W. Cotman. 1997. Heparin sulfate potentiates the autocrine action of basic fibroblast growth factor in astrocytes: An in vivo and in vitro study. Neuroscience 76: 137-145.
17. Gomez-Pinilla, F., L. Vu, and C. W. Cotman. 1995. Regulation of astrocyte proliferation by FGF-2 and heparin sulfate in vivo. J. Neurosci. 15: 2021-2029.
18. Gospadorowicz, D., J. Cheng, G. Lui, A. Baird, and P. Bohlen. 1984. Isolation of brain fibroblast growth factor by heparin-sepharose affinity-chromatography : Identity with pituitary fibroblast growth factor. Proc. Natl. Acad. Sci. USA 81: 6963-6967.
19. Gospodarowicz, D., and J. Chen. 1986. Heparin protects acidic and basic FGF from inactivation. J. Cell Physiol. 128: 475-484.
20. Gritti, A., E. A. Parati, L. Cova, P. Frolichsthal, R. Galli, E. Wanke, L. Faravelli, D. J. Morassutti, F. Roisen, D. D. Nickel, and A. L. Vescovi. 1996. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16: 1091-1100.
21. Hansen, M. B., S. E. Nielsen, and K. Berg. 1989. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 119: 203-210.
22. Hynes, M., K. Poulsen, M. Tessier-Lavigne, and A. Rosenthal. 1995. Control of neuronal diversity by the floor plate: Contact-mediated induction of midbrain dopaminergic neurons. Cell 80: 95-111.
23. Johe, K. K., T. G. Hazel, T. Muller, M. Dugich-Djordjevic, and R. D. G. McKay. 1996. Single factors direct the differentiation of stem cells from the fetal and adult Central nervous system. Genes Dev. 10: 3129-3140.
24. Kan, M., D. Disorbo, J. Z. Hou, H. Hoshi, P. E. Mansson, and W. L. McKeehan. 1988. High and low affinity binding of heparin-binding growth-factor to a 130-KDa receptor correlates with stimulation and inhibition of growth. J. Biol. Chem. 263: 11306-11313.
25. Kan, M., F. Wang, Y. Xu, J. W. Crabb, J. Hou, and W. L. McKeehan. 1993. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 259: 1918-1921.
26. Keller, K. M., P. R. Brauer, and J. M. Keller. 1989. Modulation of cell surface heparin sulfate structure by growth of cells in the presence of chlorate. Biochemistry 28: 8100-8107.
27. Kilpatrick, T. J., and P. F. Bartlett. 1993. Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 10: 255-265.
28. Kilpatrick, T. J., and P. F. Bartlett. 1995. 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: 3653-3661.
29. Klagsbrun, M., and A. Baird. 1991. A Dual receptor system is required for fibroblast growth factor activity. Cell 67: 229-231.
30. Knusel, B., P. P. Michel, J. S. Schwaber, and F. Hefti. 1990. Selective and nonselective stimulation of central cholinergic and dopaminergic development in vitro by nerve growth factor, basic fibroblast growth factor, epidermal growth factor, insulin and insulin-like growth factors I and II. J. Neurosci. 10: 558-570.
31. Lander, A. D. 1993. Proteoglycans in the nervous system. Curr. Opin. Neurobiol. 3: 716-723.
32. Lazar, L. M., and M. Blum. 1992. Regional distribution and developmental expression of epidermal growth factor and transforming growth factor-a mRNA in mouse brain by quantitative nuclease protection assay. J. Neurosci. 12: 1688-1697.
33. Letourneau, P. C., M. L. Condic, and D. M. Snow. 1994. Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14: 915-928.
34. Lillien, L., and C. Cepko. 1992. Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF-alpha. Development 115: 253-266.
35. Lindahl, U., and M. Hook. 1978. Glycosaminoglycans and their binding to Biological Macromolecules. Annu. Rev. Biochem. 47: 385-417.
36. Lindvall, O. 1997. Neural Transplantation: A hope for patients with Parkinson's disease. NeuroReport 8: iii-x.
37. Lobb, R. R., and J. W. Fett. 1984. Purification of two distinct growth factors from bovine neural tissue by heparin affinity chromatography. Biochemistry 24: 6295-6299.
38. Maccarana, M., B. Casu, and U. Lindahl. 1993. Minimal sequence in heparin heparan sulfate required for binding of basic fibroblast growth factor. J. Biol. Chem. 268: 23898-23905.
39. Mario, H., I. Tatsuno, A. Hirai, Y. Tamura, and Y. Saito. 1996. Pituitary adenyl cyclase-activating polypeptide protects rat-cultured cortical neurons from glutamate induced cytotoxicity. Brain Res. 741: 82-88.
40. McKay, R. 1997. Stem cells in the central nervous system. Science 276: 66-71.
41. Mueller, S. N., K. A. Thomas, J. DiSalvo, and E. M. Levine. 1989. Stabilization by heparin of acidic fibroblast growth factor mitogenicity for human endothelial cells in vitro. J. Cell Physiol. 140: 439-448.
42. Mytilineou, C., T. H. Park, and J. Shen. 1992. Epidermal growth factor-induced survival and proliferation of neuronal precursor cells from embryonic rat mesencephalon. Neurosci. Lett. 135: 62-66.
43. Perraud, F., F. Besnard, B. Pettmann, M. Sensenbrenner, and M. Labourdette. 1988. Effects of acidic and basic fibroblast growth factors (aFGF and bFGF) on the proliferation and glutamine synthetase expression of rat astroblast in culture. Glia 1: 124-131.
44. Ptak, L. R., K. R. Hart, D. Lin, and P. M. Carvey. 1995. Isolation and manipulation of rostral mesencephalic tegmental progenitor cells from rat. Cell Transplant. 4: 335-342.
45. Qian, X., A. A. Davis, S. K. Goderie, and S. Temple. 1997. FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18: 81-93.
46. Ray, J., and F. H. Gage. 1994. Spinal cord neuroblasts proliferate in response to basic fibroblast growth factor. J. Neurosci. 14: 3548-3564.
47. Ray, J., D. A. Peterson, M. Schinstine, and F. H. Gage. 1993. Proliferation, differentiation and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. USA 90: 3602-3606.
48. Reynolds, B. A., W. Tetzlaff, and S. Weiss. 1992. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12: 4565-4574.
49. Reynolds, B. A., and S. Weiss. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
50. Rosser, A. E., P. Tyers, M. terBorg, S. B. Dunnett, and C. N. Svendsen. 1997. Co-expression of MAP-2 and GFAP in cells developing from rat EGF responsive precursor cells. Dev. Brain Res. 98: 291-295.
51. Sabate, O., P. Horellou, E. Vigne, P. Colin, M. Perricaudet, M.-H. Buc-Caron, and J. Mallet. 1995. Transplantation to the rat brain of human neural progenitors that were genetically modified using adenoviruses. Nature Genet. 9: 256-260.
52. Saksela, O., D. Moscatelli, A. Sommer, and D. B. Rifkin. 1988. Endothelial cell-derived heparin sulfate binds basic fibroblast growth factor and protects it from Proteolytic degradation. J. Cell Biol. 107: 743-751.
53. Santa-Olalla, J., and L. Covarrubias. 1995. Epidermal growth factor (EGF), transforming growth factor-a (TGF-a), and basic fibroblast growth factor (bFGF) differentially influence neural precursor cells of mouse embryonic mesencephalon. J. Neurosci. Res. 42: 172-183.
54. Svendsen, C. N. 1997. Neural Stem Cells for brain repair. Alzheimers Res. 3: 131-135.
55. Svendsen, C. N., D. J. Clarke, A. E. Rosser, and S. B. Dunnett. 1996. Survival and differentiation of rat and human epidermal growth factor-responsive precursor cells following grafting into the lesioned adult central nervous system. Exp. Neurol. 137: 376-388.
56. Svendsen, C. N., J. W. Fawcett, C. Bentlage, and S. B. Dunnett. 1995. Increased survival of rat EGF-generated CNS precursor cells using B27 supplemented medium. Exp. Brain Res. 102: 407-414.
57. Svendsen, C. N., and A. E. Rosser. 1995. Neurons from stem cells. Trends Neurosci. 18: 465-467.
58. Svendsen, C. N., M. terBorg, P. Tyers, M. A. Caldwell, and A. E. Rosser. 1997. EGF responsive precursor cells cannot be isolated from primary E14 striatum. Soc. Neurosci. 2: 1418. [Abstract]
59. Sweetnam, P. M., H. R. Sanon, L. A. White, B. J. Brass, M. Jaye, and S. R. Whittemore. 1991. Differential effects of acidic and basic fibroblast growth factors on spinal cord cholinergic, GAB-Aergic, and Glutamatergic neurons. J. Neurochem. 57: 237-249.
60. Vicario-Abejon, C., K. K. Johe, T. G. Hazel, D. Collazo, and R. D. G. McKay. 1995. Functions of basic fibroblast growth factor and neurotropins in the Differentiation of hippocampal neurons. Neuron 15: 105-114.
61. Wagner, J. A. 1991. The fibroblast growth factors: An emerging family of neural growth factors. Curr. Topics Microbiol. Immunol. 165: 95-118.
62. Walicke, P. A. 1988. Basic and acidic growth factors have tropic effects on neurons from multiple CNS regions. J. Neurosci. 8: 2618-2627.
63. Weiss, S., C. Dunne, J. Hewson, C. Wohl, M. Wheatley, A. C. Peterson, and B. A. Reynolds. 1996. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16: 7599-7609.