Analysis of mutant platelet-derived growth factor receptors expressed in PC12 cells identifies signals governing sodium channel induction during neuronal differentiation

Molecular and Cellular Biology

Volumn 17, Issue 1, 1997, Pages 89-99

  Fanger, Gary R ^a   Vaillancourt, Richard R ^b   Heasley, Lynn E ^c   Montmayeur, Jean Pierre R ^b   Johnson, Gary L ^b,c   Maue, Robert A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR RECEPTOR; RIBONUCLEASE; SODIUM CHANNEL; SODIUM ION; STROMELYSIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; MUTANT; NERVE CELL DIFFERENTIATION; NONHUMAN; ONCOGENE C FOS; PATCH CLAMP; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0031034397     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.1.89     Document Type: Article

References (86)

1. Akopian, A. N., L. Sivilotti, and J. N. Wood. 1996. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 257-262.
2. Arvidsson, A.-K., E. Rupp, E. Nanberg, J. Downward, L. Ronnstrand, S. Wennstrom, J. Schlessinger, C.-H. Heldin, and L. Claesson-Welsh. 1994. Tyr-716 in the platelet-derived growth factor β-receptor kinase insert is involved in GRB2 binding and ras activation. Mol. Cell. Biol. 14:6715-6726.
3. Auger, K. R., L. A. Serunian, S. P. Soltoff, P. Libby, and L. C. Cantley. 1989. PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell 57:167-175.
4. Barker, P. (McGill University). 1995. Personal communication.
5. Catterall, W. A. 1992. Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 72:515-541.
6. Chao, M. V. 1992. Growth factor signaling: where is the specificity? Cell 68:995-997.
7. Chirgwin, J. M., A. E. Przybyla, R. J. MacDonald, and W. J. Rutter. 1979. Isolation of biologically active ribonucleic acids from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
8. Claesson-Welsh, L. 1994. Platelet-derived growth factor receptor signals. J. Biol. Chem. 269:32023-32026.
9. Coughlin, S. R., J. A. Escobedo, and L. T. Williams. 1989. Role of phosphatidylinositol kinase in PDGF receptor signal transduction. Science 243:1191-1194.
10. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
11. D'Arcangelo, G., and S. Haleguoa. 1993. A branched signaling pathway for nerve growth factor is revealed by Src-, Ras-, and Raf-mediated gene inductions. Mol. Cell. Biol. 13:3146-3155.
12. D'Arcangelo, G., K. Paradiso, D. Shepherd, P. Brehm, S. Halegoua, and G. Mandel. 1993. Neuronal growth factor regulation of two different sodium channel types through distinct signal transduction pathways. J. Cell Biol. 4:915-921.
13. Dikic, I., J. Schlessinger, and I. Lax. 1994. PC12 cells overexpressing the insulin receptor undergo insulin-dependent neuronal differentiation. Curr. Biol. 4:702-708.
14. Eccleston, P. A., K. Funa, and C. H. Heldin. 1993. Expression of plateletderived growth factor (PDGF) and PDGF α-and β-receptors in the peripheral nervous system: an analysis of sciatic nerve and dorsal root ganglia. Dev. Biol. 155:459-470.
15. Fanger, G. R. 1995. Ph.D. thesis. Dartmouth College, Hanover, N.H.
16. Fanger, G. R., C. Brennan, L. P. Henderson, P. D. Gardner, and R. A. Maue. 1995. Differential expression of sodium channels and nicotinic acetylcholine receptors channels in nnr variants of the PC12 pheochromocytoma cell line. J. Membr. Biol. 144:71-80.
17. Fanger, G. R., P. Erhardt, G. M. Cooper, and R. A. Maue. 1993. Ras-independent induction of rat brain type II sodium channel expression in nerve growth factor-treated PC12 cells. J. Neurochem. 61:1977-1980.
18. Fanger, G. R., J. R. Jones, and R. A. Maue. 1995. Differential regulation of neuronal sodium channel expression by endogenous and exogenous tyrosine kinase receptors expressed in rat pheochromocytoma cells. J. Neurosci. 15: 202-213.
19. Fanger, G. R., and R. A. Maue. Unpublished observations.
20. Fantl, W. J., J. A. Escobedo, and L. T. Williams. 1989. Mutations of the platelet-derived growth factor receptor that cause a loss of ligand-induced conformational change, subtle changes in kinase activity, and impaired ability to stimulate DNA synthesis. Mol. Cell. Biol. 9:4473-4478.
21. Gautron, S., G. Dos-Santos, D. Pinto-Henrique, A. Koulakoff, F. Gros, and Y. Y. Berwald-Netter. 1992. The glial voltage-gated sodium channel: cell-and tissue-specific mRNA expression. Proc. Natl. Acad. Sci. USA 89:7272-7276.
22. Ghosh, A., and M. E. Greenberg. 1995. Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103.
23. Ginty, D. D., G. R. Fanger, J. A. Wagner, and R. A. Maue. 1992 The activity of cAMP-dependent protein kinase is required at a posttranslational level for the induction of voltage-dependent sodium channels by peptide growth factors in PC12 cells. J. Cell. Biol. 116:1465-1473.
24. Grant, S. G. N., T. J. O'Dell, K. A. Karl, P. L. Stein, P. Soriano, and E. R. Kandel. 1992. Impaired long term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910.
25. Greene, L. A., and A. S. Tischler. 1982. PC12 pheochromocytoma cells in neurobiology research. Adv. Cell Neurobiol. 3:373-414.
26. Guroff, G. 1985. PC12 cells as a model of neuronal differentiation, p. 245-272. In J. E. Bottenstein and G. Sato (ed.), Cell culture in the neurosciences. Plenum Press, New York, N.Y.
27. Hart, C. E., R. A. Seifert, and D. F. Bowen-Pope. 1987. Synthesis, phosphorylation, and degradation of multiple forms of the platelet-derived growth factor receptor studied using a monoclonal antibody. J. Biol. Chem. 262: 10780-10785.
28. Heasley, L. E., and G. L. Johnson. 1992. The β-PDGF receptor induces neuronal differentiation of PC12 cells. Mol. Biol. Cell 3:545-553.
29. Hefti, F., J. Hartikka, and B. Knusel. 1989. Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol. Aging 10:515-533.
30. Heidecker, G., M. Huleihel, J. L. Cleveland, W. Kolch, T. W. Beck, P. Lloyd, T. Pawson, and U. R. Rapp. 1990. Mutational activation of c-raf-1 and definition of the minimal transforming sequence. Mol. Cell. Biol. 10:2503-2512.
31. Heldin, C. H. 1995. Dimerization of cell surface receptors in signal transduction. Cell 80:213-223.
32. Hempstead, B. L., S. J. Rabin, L. Kaplan, S. Reid, L. F. Parada, and D.R. Kaplan. 1992. Overexpression of the trk tyrosine kinase rapidly accelerates nerve growth factor-induced differentiation. Neuron 9:883-896.
33. Hod, Y. 1992. A simplified ribonuclease protection assay. BioTechniques 13:852-854.
34. Ignelzi, M. A., D. R. Miller, P. Soriano, and P. F. Maness. 1994. Impaired neurite outgrowth of src-cerebellar neurons on the cell adhesion molecule L1. Neuron 12:873-884.
35. Kaplan, D. R., D. K. Morris, G. Wong, F. McCormick, and L. T. Williams. 1990. PDGF β-receptor stimulates tyrosine phosphorylation of GAP and association of GAP with a signaling complex. Cell 61:125-133.
36. Kaplan, D. R., and R. M. Stephens. 1994. Neurotrophin signal transduction by the trk receptor. J. Neurobiol. 25:1404-1417.
37. γ1. Mol. Biol. Cell 4:49-57.
38. Kashishian, A., A. Kazlauskas, and J. A. Cooper. 1992. Phosphorylalion sites in the PDGF receptor with different specificities for binding GAP and PI3-kinase in vivo. EMBO J. 11:1373-1382.
39. Kazlauskas, A., and J. A. Cooper. 1989. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58:1121-1133.
40. Kazlauskas, A., D. L. Durden, and J. A. Cooper. 1991. Functions of the major tyrosine phosphorylation site of the PDGF receptor β subunit. Cell. Regul. 2:413-425.
41. Kazlauskas, A., T. Ellis, T. Pawson, and J. A. Cooper. 1990. Binding of GAP to activated PDGF receptors. Science 247:1578-1581.
42. Korsching, S. 1993. The neurotrophic factor concept: a reexamination. J. Neurosci. 13:2739-2748.
43. Kremer, N. E., G. D'Arcangelo, S. M. Thomas, M. DeMarco, J. S. Brugge, and S. Halegoua. 1991. Signal transduction by nerve growth factor and fibroblast growth factor in PC12 cells requires a sequence of src and ras actions. J. Cell Biol. 115:809-819.
44. Kypta, R. M., Y. Goldberg, E. T. Ulug, and S. A. Courtneidge. 1990. Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 62:481-492.
45. Levi-Montalcini, R. 1987. The nerve growth factor: thirty-five years later. EMBO J. 6:1145-1154.
46. Li, W. R., A. Nishimura, A. Kashishian, A. G. Batzer, W. J. Kim, J. A. Cooper, and J. Schlessinger. 1994. A new function for a phosphotyrosine phosphatase: linking Grb2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14:509-517.
47. γ1 abolishes NGF-promoted peripherin induction but not neurite outgrowth. J. Biol. Chem. 269:8901-8910.
48. Machida, C. M., K. D. Rodland, L. Matrisian, B. E. Magun, and G. Ciment. 1989. NGF induction of the gene encoding the protease transin accompanies neuronal differentiation. Neuron 2:1587-1596.
49. Mandel, G., S. S. Cooperman, R. A. Maue, R. H. Goodman, and P. Brehm. 1988. Selective induction of brain type II Na channels by nerve growth factor. Proc. Natl. Acad. Sci. USA 85:924-928.
50. Maness, P. F. 1992. Nonreceptor protein tyrosine kinases associated with neuronal development. Dev. Neurosci. 14:257-270.
51. Marshall, C. J. 1995. Specificity of tyrosine receptor signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-186.
52. Mendell, L. M. 1994. Neurotrophic factors and the specification of neural function. Neuroscientist Preview issue:21-29.
53. Molloy, C. J., D. P. Bottaro, T. P. Fleming, M. S. Marshall, J. B. Gibbs, and S. A. Aaronson. 1989. PDGF induction of tyrosine phosphorylation of GT-Pase activating protein. Nature 342:711-714.
54. Mori, S., L. Ronnstrand, K. Yokote, A. Engstrom, S. A. Courtneidge, L. Claesson-Welsh, and C.-H. Heldin. 1993. Identification of two juxtamembrane autophosphorylation sites in the PDGF β-receptor: involvement in the interaction with Src family tyrosine kinases. EMBO J. 12:2257-2264.
55. Nikkhah, G., P. Odin, A. Smits, A. Tingstrom, A. Othberg, P. Brundin, K. Funa, and O. Lindvall. 1993. Platelet-derived growth factor promotes survival of rat and human mesencephalic dopaminergic neurons in culture. Exp. Brain Res. 92:516-523.
56. Noda, M., T. Ikeda, H. Suzuki, H. Takeshima, T. Takahashi, M. Kuno, and S. Numa. 1986. Existence of distinct sodium channel messenger RNAs in rat brain. Nature 320:188-192.
57. γ. EMBO J. 13: 1585-1590.
58. Panayotou, G., and M. D. Waterfield. 1993. The assembly of signaling complexes by receptor tyrosine kinases. Bioessays 15:171-177.
59. Pawson, T., and G. D. Gish. 1992. SH2 and SH3 domains: from structure to function. Cell 71:359-362.
60. Peng, X., L. A. Greene, D. R. Kaplan, and R. M. Stephens. 1995. Deletion of conserved juxtamembrane sequence in trk abolishes NGF-promoted neuritogenesis. Neuron 15:395-406.
61. Rabin, S. J., V. Cleghon, and D. R. Kaplan. 1993. SNT, a differentiation-specific target of neurotrophic factor-induced tyrosine kinase activity in neurons and PC12 cells. Mol. Cell. Biol. 13:2203-2213.
62. Rausch, D. M., G. Dickens, S. Doll, K. Fujita, S. Koizumi, B. B. Rudkin, M. Tocco, L. E. Eiden, and G. Guroff. 1989. Differentiation of PC12 cells with v-src: comparison with nerve growth factor. J. Neurosci. Res. 24:49-58.
63. γ. EMBO J. 11:3911-3919.
64. Sasahara, M., J. W. U. Fries, E. W. Raines, A. M. Gown, L. E. Westrum, M. P. Frosch, D. T. Bonthron, R. Ross, and T. Collins. 1991. PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model. Cell 64:217-227.
65. Schaller, K. L., D. M. Krzemien, P. J. Yarowsky, B. K. Krueger, and J. H. Caldwell. 1995. A novel, abundant sodium channel expressed in neurons and glia. J. Neurosci. 15:3231-3242.
66. Scheinman, R. I., V. J. Auld, A. L. Goldin, N. Davidson, R. J. Dunn, and W. A. Catterall. 1989. Developmental regulation of sodium channel expression in the rat forebrain. J. Biol. Chem. 264:10660-10666.
67. Smith, R. D., and A. L. Goldin. 1992. Protein kinase A phosphorylation enhances sodium channel currents in Xenopus oocytes. Am. J. Physiol. 263:660-666.
68. Smits, A., M. Kato, B. Westermark, M. Nister, C. H. Heldin, and K. Funa. 1991. Neurotrophic activity of platelet-derived growth factor (PDGF): rat neuronal cells possess functional PDGF β-type receptors and respond to PDGF. Proc. Natl. Acad. Sci. USA 88:8159-8163.
69. Smits, A., A. E. Ballagi, and K. Funa. 1993. PDGF-BB exerts trophic activity on cultured GABA interneurons from the newborn rat cerebellum. Eur. J. Neurosci. 5:986-994.
70. Snider, W. D. 1994. Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77:627-638.
71. γ1 to mediate NGF responses. Neuron 12: 691-705.
72. Suzuki, H. S., S. Beckh, H. Kubo, N. Yahagi, H. Ishida, T. Kayano, M. Noda, and S. Numa. 1988. Functional expression of cloned cDNA encoding sodium channel HI. FEBS Lett. 228:195-200.
73. Szeberenyi, J., H. Cai, and G. M. Cooper. 1990. Effect of a dominant inhibitory Ha-ras mutation on neuronal differentiation of PC12 cells. Mol. Cell. Biol. 10:5324-5332.
74. Temple, S., and X. Qian. 1995. bFGF, Neurotrophins, and the control of cortical neurogenesis. Neuron 15:249-252.
75. Toledo-Aral, J. J., P. Brehm, S. Halegoua, and G. Mandel. 1995. A single pulse of nerve growth factor triggers long-term neuronal excitability through sodium channel gene induction. Neuron 14:607-611.
76. Traverse, S., N. Gomez, H. Paterson, C. J. Marshall, and P. Cohen. 1992. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for the differentiation of PC12 cells: comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288:351-355.
77. Traverse, S., K. Seedorf, H. Paterson, C. J. Marshall, P. Cohen, and A. Ullrich. 1994. EGF triggers neuronal differentiation of PC12 cells that over-express the EGF receptor. Curr. Biol. 4:694-701.
78. Ullrich, A., and J. Schlessinger. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61:203-212.
79. Vaillancourt, R. R., L. E. Heasley, J. Zamparripa, B. Storey, M. Valius, A. Kazlauskas, and G. L. Johnson. 1995. Mitogen-activated protein kinase activation is insufficient for growth factor receptor-mediated PC12 cell differentiation. Mol. Cell. Biol. 15:3644-3653.
80. γ1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 73:321-334.
81. γ1. Mol. Cell. Biol. 15:3058-3071.
82. Vicaro-Abejon, C., K. K. Johe, T. G. Hazel, D. Collazo, and R. D. G. McKay. 1995. Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15:105-114.
83. Waechter, C. J., J. W. Schmidt, and W. A. Catterall. 1983. Glycosylation is required for maintenance of functional sodium channels in neuroblastoma cells. J. Biol. Chem. 258:5117-5123.
84. Walicke, P., and A. Baird. 1988. Neurotrophic effects of basic and acidic fibroblast growth factors are not mediated through glial cells. Brain Res. 468:71-79.
85. Wollner, D. A., R. Scheinman, and W. A. Catterall. 1988. Sodium channel expression and assembly during development of retinal ganglion cells. Neuron 1:727-737.
86. Yarden, Y., and A. Ullrich. 1988. Growth factor receptor tyrosine kinases. Annu. Rev. Biochem. 57:443-478.