Differential regulation of mTOR-dependent S6 phosphorylation by muscarinic acetylcholine receptor subtypes

Journal of Cellular Biochemistry

Volumn 104, Issue 5, 2008, Pages 1818-1831

  Slack, Barbara E ^a   Blusztajn, Jan K ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mammalian target of rapamycin; Mitogen activated protein kinase; Ribosomal S6 protein

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; BISINDOLYLMALEIMIDE; CARBACHOL; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC RECEPTOR; MUSCARINIC RECEPTOR BLOCKING AGENT; PHORBOL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P90; RAPAMYCIN; S6 KINASE;

ARTICLE; CELL LINE; EMBRYO; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; RECEPTOR AFFINITY; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CARBACHOL; CELL LINE, TUMOR; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASES; RECEPTOR, MUSCARINIC M2; RECEPTOR, MUSCARINIC M3; RECEPTORS, MUSCARINIC; RIBOSOMAL PROTEIN S6; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; TETRADECANOYLPHORBOL ACETATE; TRANSFECTION;

MAMMALIA;

EID: 50249152320     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21745     Document Type: Article

References (43)

1. Alessi DR. 1997. The protein kinase C inhibitors Ro 318220 and GF 109203X are equally potent inhibitors of MAPKAP kinase-1beta (Rsk-2) and p70 S6 kinase. FEBS Lett 402:121-123.
2. Arunlakshana O, Schild HO. 1959. Some quantitative uses of drug antagonists. Br J Pharmacol Chemother 14: 48-58.
3. Arvisais EW, Romanelli A, Hou X, Davis JS. 2006. AKT-independent phosphorylation of TSC2, and activation of mTOR and ribosomal protein S6 kinase signaling by prostaglandin F2α. J Biol Chem 281:26904-26913.
4. Ballif BA, Roux PP, Gerber SA, MacKeigan JP, Blenis J, Gygi SP. 2005. Quantitative phosphorylation profiling of the ERK/p90 ribosomal S6 kinase-signaling cassette and its targets, the tuberous sclerosis tumor suppressors. Proc Natl Acad Sci USA 102:667-672.
5. Baumgartner MK, Wei J, Aronstam RS. 1993. Retinoic acid-induced differentiation of a human neuroblastoma cell line alters muscarinic receptor expression. Dev Brain Res 72:305-308.
6. S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc Natl Acad Sci USA 100:14368-14373.
7. Caulfield MP, Birdsall NJM. 1998. International union of pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50:279-290.
8. Crespo P, Xu N, Simonds WF, Gutkind JS. 1994. Ras-dependent activation of MAP kinase pathway mediated by G-protein βSgamma subunits. Nature 369:418-420.
9. Dufner A, Thomas G. 1999. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res 253:100-109.
10. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM. 1998. Identification of a novel inhibitor of mitogenactivated protein kinase kinase. J Biol Chem 273: 18623-18632.
11. Felder CC. 1995. Muscarinic acetylcholine receptors: Signal transduction through multiple effectors. FASEB J 9:619-625.
12. Fingar DC, Blenis J. 2004. Target of rapamycin (TOR): An integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23:3151-3171.
13. Fisher SK, Heacock AM. 1988. A putative M3 muscarinic cholinergic receptor of high molecular weight couples to phosphoinositide hydrolysis in human SK-N-SH neuroblastoma cells. J Neurochem 50:984-987.
14. Gautam D, Duttaroy A, Cui Y, Han SJ, Deng C, Seeger T, Alzheimer C, Wess J. 2006. M1-M3 muscarinic acetylcholine receptor-deficient mice: Novel phenotypes. J Mol Neurosci 30:157-160.
15. Gong R, Park CS, Abbassi NR, Tang S-J. 2006. Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J Biol Chem 281:18802-18815.
16. Guizzetti M, Costa LG. 2002. Effect of ethanol on protein kinase Czeta and p70S6 kinase activation by carbachol: A possible mechanism for ethanol-induced inhibition of glial cell proliferation. J Neurochem 82:38-46.
17. Hay N, Sonenberg N. 2004. Upstream and downstream of mTOR. Genes Dev 18:1926-1945.
18. Inoki K, Li Y, Zhu T, Wu J, Guan K-L. 2002. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4:648-657.
19. Inoki K, Zhu T, Guan K-L. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590.
20. Kelleher RJ III, Govindarajan A, Jung HY, Kang H, Tonegawa S. 2004a. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479.
21. Kelleher RJ III, Govindarajan A, Tonegawa S. 2004b. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 59:59-73.
22. King TD, Song L, Jope RS. 2006. AMP-activated protein kinase (AMPK) activating agents cause dephosphorylation of Akt and glycogen synthase kinase-3. Biochem Pharmacol 71:1637-1647.
23. ras. Proc Natl Acad Sci USA 91:12706-12710.
24. Ma L, Chan Z, Erdjument-Bromage H, Tempst P, Pandolfi PP. 2005. Phosphorylation and functional inactivation of TSC2 by Erk: Implications for tuberous sclerosis and cancer pathogenesis. Cell 121:179-193.
25. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marmé D, Schächtele C. 1993. Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J Biol Chem 268:9194-9197.
26. Origlia N, Kuczewski N, Aztiria E, Gautam D, Wess J, Domenici L. 2006. Muscarinic acetylcholine receptor knockout mice show distinct synaptic plasticity impairments in the visual cortex. J Physiol 577:829-840.
27. Peralta EG, Ashkenazi A, Winslow JW, Ramachandran J, Capon DJ. 1988. Differential regulation of PI hydrolysis and adenylyl cyclase by muscarinic receptor subtypes. Nature 334:434-437.
28. RSK activity in vitro and in adult ventricular myocytes. Br J Pharmacol 145:477-489.
29. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J. 2004. Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 101:13489-13494.
30. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N, Blenis J. 2007. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 282:14056-14064.
31. Sandmann J, Peralta EG, Wurtman RJ. 1991. Coupling of transfected muscarinic acetylcholine receptor subtypes to phospholipase D. J Biol Chem 266:6031-6034.
32. Slack BE. 2000. The m3 muscarinic acetylcholine receptor is coupled to mitogen-activated protein kinase via protein kinase C and epidermal growth factor receptor kinase. Biochem J 348:381-387.
33. Tang SJ, Reis G, Gingras A-C, Sonenberg N, Schuman EM. 2002. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci USA 99:467-472.
34. Tang XW, Wang LJ, Proud CG, Downes CP. 2003. Muscarinic receptor-mediated activation of p70 S6 kinase 1 (S6K1) in 1321N1 astrocytoma cells: Permissive role of phosphoinositide 3-kinase. Biochem J 374:137-143.
35. Tee AR, Blenis J. 2005. mTOR, translational control and human disease. Semin Cell Dev Biol 16:29-37.
36. Tee AR, Anjum R, Blenis J. 2003. Inactivation of the tuberous sclerosis complex-1 and-2 gene products occurs by phosphoinositide 3-kinase/Akt-dependent and -independent phosphorylation of tuberin. J Biol Chem 278: 37288-37296.
37. Van Koppen CJ, Kaiser B. 2003. Regulation of muscarinic acetylcholine receptor signaling. Pharmacol Ther 98: 197-220.
38. Wall SJ, Yasuda RP, Li M, Wolfe BB. 1991. Development of an antiserum against m3 muscarinic receptors: Distribution of m3 receptors in rat tissues and clonal cell lines. Mol Pharmacol 40:783-789.
39. Wang LJ, Proud CG. 2002. Ras/Erk signaling is essential for activation of protein synthesis by Gq protein receptor agonists in adult cardiomyocytes. Circ Res 91:821-829.
40. Wang L, Gout I, Proud CG. 2001. Cross-talk between the ERK and p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J Biol Chem 276:32670-32677.
41. Wess J. 2004. Muscarinic acetylcholine receptor knockout mice: Novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 44:423-450.
42. Winitz S, Russell M, Qian N-X, Gardner A, Dwyer L, Johnson GL. 1993. Involvement of Ras and Raf in the Gr coupled acetylcholine muscarinic m2 receptor activation of mitogen-activated protein (MAP) kinase kinase and MAP kinase. J Biol Chem 268:19196-19199.
43. Wullschleger S, Loewith R, Hall MN. 2006. TOR signaling in growth and metabolism. Cell 124:471-484.