Nicotine-induced phosphorylation of Akt through epidermal growth factor receptor and Src in PC12h cells

Journal of Neurochemistry

Volumn 83, Issue 6, 2002, Pages 1372-1379

  Nakayama, Hitoshi ^a   Numakawa, Tadahiro ^b   Ikeuchi, Toshihiko ^c  

^a NARA MEDICAL UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c KANSAI UNIVERSITY   (Japan)

Author keywords

Acetylcholine receptor; Akt; EGFR; Nicotine; Nicotinic; PC12 cells

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALMODULIN INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINE; NICOTINIC RECEPTOR BLOCKING AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR; PROTEIN KINASE P60;

ANIMAL CELL; ARTICLE; CELL STRAIN; CELL SURVIVAL; DOSE RESPONSE; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM CHANNEL BLOCKERS; CALMODULIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; MITOGEN-ACTIVATED PROTEIN KINASES; NICOTINE; NICOTINIC ANTAGONISTS; PC12 CELLS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

ANIMALIA;

EID: 0036906212     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2002.01248.x     Document Type: Article

References (52)

1. Akaike A., Tamura Y., Yokota T., Shimohama S. and Kimura J. (1994) Nicotine-induced protection of cultured cortical neurons against N-methyl-D-aspartate receptor-mediated glutamate cytotoxicity. Brain Res. 644, 181-187.
2. Andreev J., Galisteo M. L., Kranenburg O., Logan S. K., Chiu E. S., Okigaki M., Cary L. A., Moolenaar W. H. and Schlessinger J. (2001) Src and Pyk2 mediate G protein-coupled receptor activation of epidermal growth factor receptor (EGFR) but are not required for coupling to the mitogen-activated protein (MAP) kinase signaling cascade. J. Biol. Chem. 276, 20130-20135.
3. 1101 is associated with modulation of receptor function. J. Biol. Chem. 274, 8335-8343.
4. Bogdan S. and Klämbt C. (2001) Epidermal growth factor receptor signaling. Curr. Biol. 10, 292-295.
5. Bridges A. J., Zhou H., Cody D. R., Rewcastle G. W., McMichael A., Showalter H. D., Fry D. W., Kraker A. J. and Denny W. A. (1996) Tyrosine kinase inhibitors. 8. An unusually steep structure-activity relationship for analogues of 4-(3-bromoanilino)-6,7-dimethoxyquinazoline (PD 153035), a potent inhibitor of the epidermal growth factor receptor. J. Med. Chem. 39, 267-276.
6. Carpenter G. (1999) Employment of the epidermal growth factor receptor in growth factor-independent signaling pathways. J. Cell Biol. 146, 697-702.
7. Conroy W. G. and Berg D. K. (1995) Neuron can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Biol. Chem. 270, 4424-4431.
8. Couturier S., Bertrand D., Matter J.-M., Hernandez M.-C., Bertrand S., Millar N., Valera S., Barkas T. and Ballivet M. (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-Btx. Neuron 5, 2654-2661.
9. Crowder R. J. and Freeman R. S. (1999) The survival of sympathetic neurons promoted by potassium depolarization, but not by cyclic AMP, requires phosphotidylinositol-3 kinase and Akt. J. Neurochem. 73, 466-473.
10. Daaka Y., Luttrell L. M. and Lefkowitz R. J. (1997) Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature 390, 88-91.
11. Daub S., Wallasch C., Lankenau A., Herrlich A. and Ullrich A. (1997) Signal characteristics of G protein-transactivated EGF receptor. EMBO J. 16, 7032-7044.
12. Dikic I., Tokiwa G., Lev S., Courtneidge S. A. and Schlessinger J. (1996) A role for Pyk2 and Src in linking G protein-coupled receptors with MAP kinase activation. Nature 383, 547-550.
13. Egea J., Espinet C. and Comella J. X. (1999) Calcium influx activates extracellular-regulated kinase/mitogen-activated protein kinase pathway through a calmodulin-sensitive mechanism in PC12 cells. J. Biol. Chem. 274, 75-85.
14. Eguchi S., Numaguchi K., Iwasaki H., Matsumoto T., Yamakawa T., Utsunomiya H., Motley E. D., Kawakatsu H., Owada K. M., Hirata Y., Marumo F. and Inagami T. (1998) Calcium-dependent epidermal growth factor receptor transactivation mediates the angiotensin ?-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. J. Biol. Chem. 273, 8890-8896.
15. Fruman D. A., Meyer R. E. and Cantley L. W. (1998) Phosphoinositide kinases. Annu. Rev. Biochem. 67, 481-507.
16. Fry D. W., Kraker A. J., McMichael A., Ambroso L. A., Nelson J. M., Leopold W. R., Connors R. W. and Bridges A. J. (1994) A specific inhibitor of the epidermal growth factor receptor tyrosine kinase. Science 265, 1093-1095.
17. Garrido R., Malecki A., Hennig B. and Toborek M. (2000) Nicotine attenuates arachidonic acid-induced neurotoxicity in cultured spinal cord neurons. Brain Res. 861, 59-68.
18. 2+/calmodulin-dependent protein kinase activity. Science 57, 9-20.
19. Hansen M. R., Zha X.-M., Bok Jinwoong B. and Green S. H. (2001) Multiple distinct signalal pathways, including an autocrine neurotrophic mechanism, contribute to the survival-promoting effect of depolarization on spinal ganglion neurons in vitro. J. Neurosci. 21, 2256-2267.
20. Henderson L. P., Gdovin M. J., Liu C., Gardner P. D. and Maue R. A. (1994) Nerve growth factor increases nicotinic ACh receptor gene expression and current density in wild-type and protein kinase A-deficient PC12 cells. J. Neurosci. 14, 1153-1163.
21. Huang E. J. and Reichardt L. F. (2001) Neurotrophins: Roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
22. Ikegami K. and Koike T. (2000) Membrane depolarization-mediated survival of sympathetic neurons occurs through both phosphatidylinositol 3-kinase- and CaM kinase II-dependent pathways. Brain Res. 866, 218-226.
23. Kaneko S., Maeda T., Kume T., Kochiyama H., Akaike A., Shimohama S. and Kimura J. (1997) Nicotine protects cultured cortical urons against glutamate-induced cytotoxicity via α7-neuronal receptors and neuronal CNS receptors. Brain Res. 765, 135-140.
24. Kassenbrock C. K., Hunter S., Garl P., Johnson G. L. and Anderson S. M. (2002) Inhibition of Src family kinases blocks epidermal growth factor (EGF)-induced activation of Akt, phosphorylation of c-Cb1, and ubiquitination of the EGF receptor. J. Biol. Chem. 277, 24967-24975.
25. Kihara T., Shimohama S., Sawada H., Kimura J., Kume T., Kochiyama H., Maeda M. S. and Akaike A. (1997) Nicotinic receptor stimulation protects neurons against β-amyloid toxicity. Ann. Neurol. 42, 159-163.
26. Kihara T., Shimohama S., Sawada H., Honda K., Nakamizo T., Shibasaki H., Kume T. and Akaike A. (2001) Alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block Aβ-amyloid-induced neurotoxicity. J. Biol. Chem. 276, 13541-13546.
27. Kitagawa D., Tanemura S., Ohata S., Shimizu N., Seo J., Nishitai G., Watanabe T., Nakagawa K., Kishimoto H., Wada T., Tezuka T., Yamamoto T., Nishina H. and Katada T. (2002) Activation of extracellular signal-regulated kinase by ultraviolet is mediated through Src-dependent epidermal growth factor receptor phosphorylation. Its implication in an antiapoptotic function. J. Biol. Chem. 277, 366-371.
28. Lee F. S. and Chao M. V. (2001) Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl. Acad. Sci. USA 98, 3555-3560.
29. 2+-induced regulation of ion channel and MAP kinase function. Nature 376, 737-745.
30. Levitzki A. and Gazit A. (1995) Tyrosine kinase inhibition: An approach to drug development. Science 267, 1782-1788.
31. Luttrell L. M., Ferguson S. S., Daaka Y., Miller W. E., Maudsley S., Della R. G. J., Lin F., Kawakatsu H., Owada K., Luttrell D. K., Caron M. G. and Lefkowitz R. J. (1999) B-arrestin-dependent formation of β2 adrenergic receptor-src protein kinase complexes. Science 283, 655-661.
32. Messi M. L., Renganathan M., Erigorenko E. and Delbono O. (1997) Activation of α7 nicotinic acetylcholine receptor promotes survival of spinal cord motoneurons. FEBS Lett. 411, 32-38.
33. Miller T. M., Tansey M. G., Johnson E. M. Jr and Creedom D. J. (1997) Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization- and insulin-like growth factor I-mediated survival of cerebellar granule cells. J. Biol. Chem. 272, 9847-9853.
34. Miñana M.-D., Montoliu C., Llansola M., Grisolia S. and Felipo V. (1998) Nicotine prevents glutamate-induced proteolysis of the microtubule-associated protein MAP-2 and glutamate neurotoxicity in primary cultures of cerebellar neurons. Neuropharmacology 37, 847-857.
35. Mittaud P., Marangi P. A., Erb-Vogtli S. and Fuhrer C. (2001) Agrin-induced activation of acetylcholine receptor-bound Src family kinases requires Rapsyn and correlates with acetylcholine receptor clustering. J. Biol. Chem 276, 14505-14513.
36. Mohamed A., Rivas-Plata K. A., Kraas J. R., Saleh S. M. and Swope S. L. (2001) Src-class kinases act within the agrin/MuSK pathway to regulate acetylcholine receptor phosphorylation, cytoskeletal anchoring, and clustering. J. Neurosci. 21, 3806-3818.
37. Nakayama H., Numakawa T., Ikeuchi T. and Hatanaka H. (2001) Nicotine-induced phosphorylation of extracellular signal-regulated protein kinase and CREB in PC12h cells. J. Neurochem. 79, 489-498.
38. Pleiman C., Hertz W. M. and Cambier J. C. (1994) Activation of phosphatidylinositol-3′ kinase by Src-family kinase SH3 binding to the p85 subunit. Science 263, 1609-1612.
39. Prenzel N., Fischer O. M., Streit S., Hart S. and Ullrich A. (2001) The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr. Rela. Cancer 8, 11-31.
40. Rocic P., Govindarajan G., Abdelkarim S. and Lucchesi P. (2001) A role for PYK2 in regulation of ERK1/2 MAP kinases and PI3-kinase by ANG II in vascular smooth muscle. Am. J. Physiol. Cell Physiol. 280, C90-C99.
41. Rogers S. W., Mandelzys A., Deneris E. S., Cooper E. and Heinemann S. (1992) The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J. Neurosci. 12, 4611-4623.
42. Rosen L. B. and Greenberg M. E. (1996) Stimulation of growth factor receptor signal transduction by activation of voltage-sensitive calcium channels. Proc. Natl. Acad. Sci. USA 93, 1113-1118.
43. Séguéla P., Wadiche J., Dineley-Miller K., Dani J. A. and Patrick J. W. (1993) Molecular cloning, functional expression and distribution of rat brain α7: A nicotinic cation channel highly permeable to calcium. J. Neurosci. 13, 596-604.
44. Soler R. M., Egea J., Mintenig G. M., Sanz-Rodriguez C., Iglesias M. and Comella J. X. (1998) Calmodulin is involved in membrane depolarization-mediated survival of motoneurons by phosphotidylinositol-3 kinase- and MAPK-independent pathways. J. Neurosci. 18, 1230-1239.
45. Stein R. C. and Waterfield M. D. (2000) PI3-kinase inhibition: A target for drug development? Mol. Med. Today 6, 347-357.
46. Vaillant A. R., Mazzoni I., Tudan C., Boudreau M., Kaplan D. R. and Miller F. D. (1999) Depolarization and neurotrophins converge on the phosphotidylinositol-3 kinase-Akt pathway to synergistically regulate neuronal survival. J. Cell Biol. 146, 955-966.
47. Vernallis A. B., Conroy W. G. and Berg D. W. (1993) Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaing subunit segregation among receptor subtypes. Neuron 10, 451-464.
48. West A. E., Chen W. G., Dalva M. B., Dolmetsch R. E., Kornhauser J. M., Shaywitz A. J., Takasu M. A., Tao X. and Greenberg M. E. (2001) Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA 98, 11024-11031.
49. Yamashita H. and Nakamura S. (1996) Nicotine rescures PC12 cells from death induced by nerve growth factor deprivation. Neurosci. Lett. 213, 145-147.
50. Yano S., Tokumitsu H. and Soderling T. M. (1998) Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature 396, 584-588.
51. Zwick E., Daub H., Aoki N., Yamaguchi-Aoki Y., Tinhofer I., Maly K. and Ullrich A. (1997) Critical role of calcium-dependent epidermal growth factor receptor transactivation in PC12 cell membrane depolarization and bradykinin signaling. J. Biol. Chem. 272, 24767-24770.
52. Zwick E., Wallasch C., Daub H. and Ullrich A. (1999) Distinct calcium-dependent pathways of epidermal growth factor receptor transactivation and PYK2 tyrosine phosphorylation in PC12 cells. J. Biol. Chem. 274, 20989-20996.