Regulation of mTOR and S6K1 activation by the nPKC isoforms, PKCε and PKCδ, in adult cardiac muscle cells

Journal of Molecular and Cellular Cardiology

Volumn 43, Issue 6, 2007, Pages 754-766

  Moschella, Phillip C ^a   Rao, Vijay U ^a   McDermott, Paul J ^a,b   Kuppuswamy, Dhandapani ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

Cardiomyocytes; Endothelin 1; Hypertrophy; mTOR; Phenylephrine; PKC; S6K1

Indexed keywords

ANGIOTENSIN II; ENDOTHELIN 1; INSULIN; ISOPROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHENYLEPHRINE; PROTEIN KINASE C; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; ROTTLERIN; S6 KINASE; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAT; CELL CULTURE; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IN VITRO STUDY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ANDROSTADIENES; ANIMALS; CATS; CELLS, CULTURED; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, DOMINANT; ISOENZYMES; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-RAF; RIBOSOMAL PROTEIN S6 KINASES;

FELIDAE;

EID: 36448942182     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2007.09.015     Document Type: Article

References (50)

1. Chua B.H., Russo L.A., Gordon E.E., Kleinhans B.J., and Morgan H.E. Faster ribosome synthesis induced by elevated aortic pressure in rat heart. Am J Physiol 252 (1987) C323-C327
2. Cooper G.T. Basic determinants of myocardial hypertrophy: a review of molecular mechanisms. Annu Rev Med 48 (1997) 13-23
3. Shioi T., McMullen J.R., Tarnavski O., Converso K., Sherwood M.C., Manning W.J., et al. Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circulation 107 (2003) 1664-1670
4. Ha T., Li Y., Gao X., McMullen J.R., Shioi T., Izumo S., et al. Attenuation of cardiac hypertrophy by inhibiting both mTOR and NFkappaB activation in vivo. Free Radic Biol Med 39 (2005) 1570-1580
5. McMullen J.R., Sherwood M.C., Tarnavski O., Zhang L., Dorfman A.L., Shioi T., et al. Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 109 (2004) 3050-3055
6. Montagne J., Stewart M.J., Stocker H., Hafen E., Kozma S.C., and Thomas G. Drosophila S6 kinase: a regulator of cell size. Science 285 (1999) 2126-2129
7. Shima H., Pende M., Chen Y., Fumagalli S., Thomas G., and Kozma S.C. Disruption of the p70(s6k)/p85(s6k) gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J 17 (1998) 6649-6659
8. Jefferies H.B., Reinhard C., Kozma S.C., and Thomas G. Rapamycin selectively represses translation of the "polypyrimidine tract" mRNA family. Proc Natl Acad Sci U S A 91 (1994) 4441-4445
9. de Groot R.P., Ballou L.M., and Sassone-Corsi P. Positive regulation of the cAMP-responsive activator CREM by the p70 S6 kinase: an alternative route to mitogen-induced gene expression. Cell 79 (1994) 81-91
10. Wang X., Li W., Williams M., Terada N., Alessi D.R., and Proud C.G. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J 20 (2001) 4370-4379
11. Raught B., Peiretti F., Gingras A.C., Livingstone M., Shahbazian D., Mayeur G.L., et al. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J 23 (2004) 1761-1769
12. Richardson C.J., Broenstrup M., Fingar D.C., Julich K., Ballif B.A., Gygi S., et al. SKAR is a specific target of S6 kinase 1 in cell growth control. Curr Biol 14 (2004) 1540-1549
13. Kim D.H., Sarbassov D.D., Ali S.M., King J.E., Latek R.R., Erdjument-Bromage H., et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110 (2002) 163-175
14. Hara K., Maruki Y., Long X., Yoshino K., Oshiro N., Hidayat S., et al. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110 (2002) 177-189
15. Loewith R., Jacinto E., Wullschleger S., Lorberg A., Crespo J.L., Bonenfant D., et al. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10 (2002) 457-468
16. Bolster D.R., Kubica N., Crozier S.J., Williamson D.L., Farrell P.A., Kimball S.R., et al. Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle. J Physiol 553 (2003) 213-220
17. Kenessey A., and Ojamaa K. Thyroid hormone stimulates protein synthesis in the cardiomyocyte by activating the Akt-mTOR and p70S6K pathways. J Biol Chem 281 (2006) 20666-20672
18. Chiang G.G., and Abraham R.T. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J Biol Chem 280 (2005) 25485-25490
19. Varma S., and Khandelwal R.L. Effects of rapamycin on cell proliferation and phosphorylation of mTOR and p70(S6K) in HepG2 and HepG2 cells overexpressing constitutively active Akt/PKB. Biochim Biophys Acta 1770 (2007) 71-78
20. Pullen N., Dennis P.B., Andjelkovic M., Dufner A., Kozma S.C., Hemmings B.A., et al. Phosphorylation and activation of p70s6k by PDK1. Science 279 (1998) 707-710
21. Dufner A., and Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res 253 (1999) 100-109
22. Han J.W., Pearson R.B., Dennis P.B., and Thomas G. Rapamycin, wortmannin, and the methylxanthine SQ20006 inactivate p70s6k by inducing dephosphorylation of the same subset of sites. J Biol Chem 270 (1995) 21396-21403
23. Mahalingam M., and Templeton D.J. Constitutive activation of S6 kinase by deletion of amino-terminal autoinhibitory and rapamycin sensitivity domains. Mol Cell Biol 16 (1996) 405-413
24. Erikson R.L. Structure, expression, and regulation of protein kinases involved in the phosphorylation of ribosomal protein S6. J Biol Chem 266 (1991) 6007-6010
25. Chou M.M., and Blenis J. The 70 kDa S6 kinase: regulation of a kinase with multiple roles in mitogenic signalling. Curr Opin Cell Biol 7 (1995) 806-814
26. Chung J., Grammer T.C., Lemon K.P., Kazlauskas A., and Blenis J. PDGF- and insulin-dependent pp70S6k activation mediated by phosphatidylinositol-3-OH kinase. Nature 370 (1994) 71-75
27. Monfar M., Lemon K.P., Grammer T.C., Cheatham L., Chung J., Vlahos C.J., et al. Activation of pp70/85 S6 kinases in interleukin-2-responsive lymphoid cells is mediated by phosphatidylinositol 3-kinase and inhibited by cyclic AMP. Mol Cell Biol 15 (1995) 326-337
28. Cass L.A., Summers S.A., Prendergast G.V., Backer J.M., Birnbaum M.J., and Meinkoth J.L. Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol Cell Biol 19 (1999) 5882-5891
29. Laser M., Kasi V.S., Hamawaki M., Cooper G.T., Kerr C.M., and Kuppuswamy D. Differential activation of p70 and p85 S6 kinase isoforms during cardiac hypertrophy in the adult mammal. J Biol Chem 273 (1998) 24610-24619
30. Iijima Y., Laser M., Shiraishi H., Willey C.D., Sundaravadivel B., Xu L., et al. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem 277 (2002) 23065-23075
31. Puceat M., Hilal-Dandan R., Strulovici B., Brunton L.L., and Brown J.H. Differential regulation of protein kinase C isoforms in isolated neonatal and adult rat cardiomyocytes. J Biol Chem 269 (1994) 16938-16944
32. Steinberg S.F., Goldberg M., and Rybin V.O. Protein kinase C isoform diversity in the heart. J Mol Cell Cardiol 27 (1995) 141-153
33. Rao V.U., Shiraishi H., and McDermott P.J. PKC-epsilon regulation of extracellular signal-regulated kinase: a potential role in phenylephrine-induced cardiocyte growth. Am J Physiol Heart Circ Physiol 286 (2004) H2195-H2203
34. Li C., Chen X., and Williams J.A. Regulation of CCK-induced amylase release by PKC-delta in rat pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 287 (2004) G764-G771
35. Wenzel S., Abdallah Y., Helmig S., Schafer C., Piper H.M., and Schluter K.D. Contribution of PI 3-kinase isoforms to angiotensin II- and alpha-adrenoceptor-mediated signalling pathways in cardiomyocytes. Cardiovasc Res 71 (2006) 352-362
36. Schluter K.D., Simm A., Schafer M., Taimor G., and Piper H.M. Early response kinase and PI 3-kinase activation in adult cardiomyocytes and their role in hypertrophy. Am J Physiol 276 (1999) H1655-H1663
37. Zhao X.S., Pan W., Bekeredjian R., and Shohet R.V. Endogenous endothelin-1 is required for cardiomyocyte survival in vivo. Circulation 114 (2006) 830-837
38. Shah O.J., Ghosh S., and Hunter T. Mitotic regulation of ribosomal S6 kinase 1 involves Ser/Thr, Pro phosphorylation of consensus and non-consensus sites by Cdc2. J Biol Chem 278 (2003) 16433-16442
39. Wang T.L., Yang Y.H., Chang H., and Hung C.R. Angiotensin II signals mechanical stretch-induced cardiac matrix metalloproteinase expression via JAK-STAT pathway. J Mol Cell Cardiol 37 (2004) 785-794
40. Mackay K., and Mochly-Rosen D. Localization, anchoring, and functions of protein kinase C isozymes in the heart. J Mol Cell Cardiol 33 (2001) 1301-1307
41. Wang L., Rolfe M., and Proud C.G. Ca(2+)-independent protein kinase C activity is required for alpha1-adrenergic-receptor-mediated regulation of ribosomal protein S6 kinases in adult cardiomyocytes. Biochem J 373 (2003) 603-611
42. Gschwendt M., Muller H.J., Kielbassa K., Zang R., Kittstein W., Rincke G., et al. Rottlerin, a novel protein kinase inhibitor. Biochem Biophys Res Commun 199 (1994) 93-98
43. Gschwendt M., Kittstein W., and Marks F. Elongation factor-2 kinase: effective inhibition by the novel protein kinase inhibitor rottlerin and relative insensitivity towards staurosporine. FEBS Lett 338 (1994) 85-88
44. Woo S.H., and Lee C.O. Effects of endothelin-1 on Ca2+ signaling in guinea-pig ventricular myocytes: role of protein kinase C. J Mol Cell Cardiol 31 (1999) 631-643
45. Northcott C.A., Hayflick J., and Watts S.W. Upregulated function of phosphatidylinositol-3-kinase in genetically hypertensive rats: a moderator of arterial hypercontractility. Clin Exp Pharmacol Physiol 32 (2005) 851-858
46. Doenst T., Wijeysundera D., Karkouti K., Zechner C., Maganti M., Rao V., et al. Hyperglycemia during cardiopulmonary bypass is an independent risk factor for mortality in patients undergoing cardiac surgery. J Thorac Cardiovasc Surg 130 (2005) 1144
47. Sawhney R.S., Cookson M.M., Sharma B., Hauser J., and Brattain M.G. Autocrine transforming growth factor alpha regulates cell adhesion by multiple signaling via specific phosphorylation sites of p70S6 kinase in colon cancer cells. J Biol Chem 279 (2004) 47379-47390
48. Williamson D.L., Kubica N., Kimball S.R., and Jefferson L.S. Exercise-induced alterations in extracellular signal-regulated kinase 1/2 and mammalian target of rapamycin (mTOR) signalling to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 573 (2006) 497-510
49. Kumar V., Pandey P., Sabatini D., Kumar M., Majumder P.K., Bharti A., et al. Functional interaction between RAFT1/FRAP/mTOR and protein kinase cdelta in the regulation of cap-dependent initiation of translation. EMBO J 19 (2000) 1087-1097
50. Parekh D., Ziegler W., Yonezawa K., Hara K., and Parker P.J. Mammalian TOR controls one of two kinase pathways acting upon nPKCdelta and nPKCepsilon. J Biol Chem 274 (1999) 34758-34764