GTPase-deficient Gα16 and Gαq induce PC12 cell differentiation and persistent activation of cJun NH2-terminal kinases

Molecular and Cellular Biology

Volumn 16, Issue 2, 1996, Pages 648-656

  Heasley, Lynn E ^a   Storey, Brooke ^a   Fanger, Gary R ^b   Butterfield, Laura ^a   Zamarripa, Jeffrey ^a   Blumberg, Deborah ^a   Maue, Robert A ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRIXIS; UNIDENTIFIED RETROVIRUS; ANIMALIA;

BRADYKININ; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; INOSITOL PHOSPHATE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; NERVE FIBER GROWTH; NONHUMAN; ONCOGENE C JUN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; RAT; RETROVIRUS;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL DIFFERENTIATION; ENZYME ACTIVATION; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NEURITES; NEURONS; PC12 CELLS; PHOSPHOLIPASE C; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RECOMBINANT PROTEINS; RETROVIRIDAE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SODIUM CHANNELS;

EID: 0029671217     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.2.648     Document Type: Article

References (61)

1. Abdel-Hafiz, H. A.-M., L. E. Heasley, J. M. Kyriakis, J. Avruch, D. J. Kroll, G. L. Johnson, and J. P. Hoeffler. 1992. Activating transcription factor-2 DNA-binding activity is stimulated by phosphorylation catalyzed by p42 and p54 microtubule-associated protien kinases. Mol Endocrinol. 6:2079-2089.
2. 16, a G protein α subunit specifically expressed in hematopoietic cells. Proc Natl. Acad. Sci. USA 88:5587-5591
3. ras, Raf-1, and MAP kinase kinase. J. Biol. Chem. 269:31836-31844.
4. Blumer, K. J., and G. L. Johnson. 1994. Diversity in function and regulation of MAP kinase pathways. Trends Biochem. Sci 19:236-240.
5. Cano, E., and L. C. Mahadevan. 1995. Parallel signal processing among mammalian MAPKs Trends Biochem Sci. 20:117-122.
6. 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.
7. Cooperman, S. S., S. A. Grubman, R. L. Barchi, R. H. Goodman, and G. Mandel. 1987. Modulation of sodium channel mRNA levels in rat skeletal muscle Proc. Natl Acad Sci USA 84:8721-8725
8. Coso, O. A., M. Chiariello, G. Kalinec, J. M. Kyriakis, J. Woodgett, and J. S. Gutkind. 1995 Transforming G protein-coupled receptors potently activate JNK (SAPK). J. Biol Chem. 270:5620-5624.
9. 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.
10. D'Arcangelo, G., and S. Halegoua. 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.
11. D'Arcangelo, G., K. Paradiso, D. Shepard, P. Brehin, S. Haleguoa, and G. Mandel. 1993. Neuronal growth factor regulation of two different sodium channel types through distinct signal transduction pathways. J. Cell Biol 122:915-921
12. Derijard, B., M. Hibi, I.-H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994 JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain Cell 76:1025-1037
13. Dhanasekaran, N., L. E. Heasley, and G. L. Johnson. 1995. G protein-coupled receptor systems involved in cell growth and oncogenesis. Endocrine Rev 16:259-270
14. Dichter, M. A., A. S. Tischler, and L. A. Greene. 1977. Nerve growth factor-induced increase in electrical excitability and acetylcholine sensitivity of a rat pheochromocytoma cell line. Nature (London) 268:501-504.
15. Dikie, I., J. Schlessinger, and I. Lax. 1994. PC12 cells overexpressing the insulin receptor undergo insulin-dependent neuronal differentiation. Curr. Biol. 4:702-708.
16. 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.
17. 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
18. Greene, L. A., and A. S. Tischler. 1982. PC12 pheochromocytoma cells in neurobiology research. Adv. Cell. Neurobiol. 3:373-414
19. Gupta, S. K., E. Diez, L. E. Heasley, S. Osawa, and G. L. Johnson. 1990. A G protein mutant that inhibits thrombin and purinergic receptor activation of phospholipase A2. Science 249:662-666
20. Gupta, S. K., C. Gallego, G. L. Johnson, and L. E. Heasley. 1992. MAP kinase is constitutively activated in grp2 and src transformed Ratla fibroblasts. J. Biol Chem. 267:7987-7990.
21. 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, New York
22. Halegoua, S., R. C. Armstrong, and N. E. Kremer. 1991. Dissecting the mode of action of a neuronal growth factor Curr Top Microbiol Immunol. 165:95-118
23. Heasley, L. E. Unpublished data.
24. Heasley, L. E., and G. L. Johnson. 1992. The β-PDGF receptor induces neuronal differentiation of PC12 cells. Mol. Biol Cell 3:545-553.
25. Heasley, L. E., S. I. Senkfor, S. Winitz, A. Strasheim, I. Teitelbaum, and T. Berl. 1994. Hormonal regulation of MAP kinase in cultured rat inner medullary collecting tubule cells. Am J. Physiol. 267(Renal Fluid Electrolyte Physiol. 36):F366-F373.
26. Heasley, L. E., J. Zamarripa, B. Storey, B. Helfrich, F. M. Mitchell, P. A. Bunn, Jr., and G. L. Johnson. Discordant signal transduction and growth inhibition of small cell lung carcinomas induced by expression of GTPase-deficient Gα16. J Biol. Chem , in press.
27. 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
28. Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993 Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain Genes Dev. 7:2135-2148.
29. Ito, E., J. L. Sonnenberg, and R. Narayanan. 1989. Nerve growth factor-induced differentiation in PC12 cells is blocked by fos oncogene. Oncogene 4:1193-1199
30. Jiang, H., D. Wu, and M. I. Simon. 1994. Activation of phospholipase C β4 by heterotrimeric GTP-binding proteins. J. Biol Chem. 269:7593-7596.
31. Kalinec, G., A. J. Nazarali, S. Hermouet, N. Zu, and J. S. Gutkind. 1992 Mutated α subunit of the Gq protein induces malignant transformation in NIH 3T3 cells. Mol. Cell. Biol. 12:4687-4693.
32. Kalman, D. B. Wong, A. E. Horvai, M. J. Cline, and P. H. O'Lague. 1990. Nerve growth factor acts through cAMP-dependent protein kinase to increase the number of sodium channels in PC12 cells. Neuron 2:355-366.
33. Kaplan, D. R., and R. M. Stephens. 1994. Neurotrophin signal transduction by the trk receptor J Neurobiol. 25:1404-1417
34. Kirschmeier, P. T., G. M. Housey, M. D. Johnson, A. S. Perkins, and I. B. Weinstein. 1988. Construction and characterization of a retroviral vector demonstrating efficient expression of cloned cDNA sequences DNA 7:219-225.
35. 16α from Sf9 cells. activation of purified phospholipase C isozymes by G-protein α subunits. Proc. Natl. Acad. Sci. USA 90:9176-9180.
36. 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 requries a sequence of src and ras actions. J. Cell Biol 115:809-819.
37. Kyriakis, J. M., P. Banerjee, E. Nikolakaki, T. Dai, E. A. Rubie, M. F. Ahmad, J. Avruch, and J. R. Woodgett. 1994 The stress-activated protein kinase subfamily of c-Jun kinases Nature (London) 369:156-160.
38. + channels by nerve growth factor Proc. Natl Acad Sci. USA 85:924-928.
39. Markowitz, D., S. Goff, and A. Bank. 1988 A safe packaging line for gene transfer separating viral genes on two different plasmids. J. Virol 62:1120-1124.
40. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
41. Maruyama, K., S. C. Schiavi, W. Huse, G. L. Johnson, and H. E. Ruley. 1987 Myc and E1A oncogenes alter the responses of PC12 cells to nerve growth factor and block differentiation. Oncogene 4:361-367.
42. Miller, A. D., and C. Buttimore. 1986. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production Mol. Cell. Biol. 6:2895-2902
43. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-990.
44. Minden, A., A. Lin, M. McMahon, C. Lange-Carter, B. Derijard, R. J. Davis, G. L. Johnson, and M. Karin. 1994. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719-1723.
45. ras in rat pheochromocytoma PC12 cells. Oncogene 7:277-281.
46. Nemenoff, R. A. Personal communication.
47. Noda, M., M. Ko, A. Ogura, D. G. Liu, T. Amano, T. Takano, and Y. Ikawa. 1985. Sarcoma viruses carrying ras oncogenes induce differentiation-associated properties in a neuronal cell line. Nature (London) 318:73-75.
48. Obermeier, A., R. A. Bradshaw, K. Seedorf, A. Choidas, J. Schlessinger, and A. Ulrich. 1994. Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLCγ. EMBO J. 13:1585-1590
49. 12 induces neoplastic transformation of Rat-1 cells. Proc. Natl. Acad. Sci. USA 88:7031-7035.
50. Pollock, J. D., M. Krempin, and B. Rudy. 1990. Differential effects of NGF, FGF, EGF, cAMP, and dexamethasone on neurite outgrowth and sodium channel expression in PC12 cells. J. Neurosci. 10:2626-2637.
51. 16 inhibits Swiss 3T3 cell growth J. Biol. Chem. 269: 17417-17423.
52. 1 muscarinic acetylcholine receptor. Proc Natl. Acad. Sci. USA 90:4077-4081
53. Rudy, S., B. Kirschenbaum, and L. A. Greene. 1982. Nerve growth factor-induced increase in saxitoxin binding to rat PC12 pheochromocytoma cells J Neurosci. 2:1405-1411.
54. Sills, M. N., Y. C. Xu, E. Barachini, R. H. Goodman, S. S. Cooperman, G. Mandel, and K. R. Chien. 1989. Expression of diverse Na channel messenger RNAs in rat myocardium. J. Clin. Invest. 84:331-336.
55. Stephens, R. M., D. M. Loeb, T. D. Copeland, T. Pawson, L. A. Greene, and D. R. Kaplan. 1994. Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ1 to mediate NGF responses. Neuron 12: 691-705.
56. o promote an increased number of neurites per cell. J Neurosci. 14:2327-2338.
57. Traverse, S., N. Gomez, H. Paterson, C. Marshall, and P. Cohen. 1992. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Biochem. J. 288:351-355.
58. Traverse, S., K. Seedorf, H. Paterson, C. J. Marshall, P. Cohen, and A. Ullrich. 1994. EGF triggers neuronal differentiation of PC12 cells that overexpress the EGF receptor. Curr. Biol. 4:694-701.
59. Vaillancourt, R. R., L. E. Heasley, J. Zamarripa, 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.
60. 13. J. Biol. Chem. 270:18655-18659.
61. Wood, K. W., H. Qi, G. D'Arcangelo, R. C. Armstrong, T. M. Roberts, and S. Halegoua. 1993. The cytoplasmic raf oncogene induces a neuronal phenotype in PC12 cells; a potential role for cellular raf kinases in neuronal growth factor signal transduction. Proc. Natl. Acad. Sci USA 90:5016-5020