G protein βγ subunits regulate cardiomyocyte hypertrophy through a perinuclear Golgi phosphatidylinositol 4-phosphate hydrolysis pathway

Molecular Biology of the Cell

Volumn 26, Issue 6, 2015, Pages 1188-1198

  Malik, S ^a   De Rubio, R G ^a   Trembley, M ^a   Irannejad, R ^b   Wedegaertner, P B ^c   Smrcka, A V ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHOLIPASE C; PROTEIN KINASE D; G-PROTEIN BETA GAMMA; PHOSPHATIDYLINOSITOL 4-PHOSPHATE; POLYPHOSPHOINOSITIDE;

ARTICLE; CELL SURFACE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GOLGI COMPLEX; HEART FAILURE; HEART MUSCLE CELL; HUMAN; HYDROLYSIS; HYPERTROPHY; INTRACELLULAR MEMBRANE; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; SIGNAL TRANSDUCTION; ANIMAL; CARDIOMEGALY; CELL CULTURE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SECOND MESSENGER; SPRAGUE DAWLEY RAT;

ANIMALS; CARDIOMEGALY; CELLS, CULTURED; GOLGI APPARATUS; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; HYDROLYSIS; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN TRANSPORT; RATS, SPRAGUE-DAWLEY; SECOND MESSENGER SYSTEMS;

EID: 84924940163     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-10-1476     Document Type: Article

References (47)

1. Balla T, Szentpetery Z, Kim YJ (2009). Phosphoinositide signaling: new tools and insights. Physiology 24, 231-244.
2. Balla A, Tuymetova G, Tsiomenko A, Várnai P, Balla T (2005). A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-iii α: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol Biol Cell 16, 1282-1295.
3. Balla T, Varnai P (2002). Visualizing cellular phosphoinositide pools with GFP-fused protein-modules. Sci STKE 2002, pl3.
4. Bkaily G, Avedanian L, Al-Khoury J, Provost C, Nader M, D'Orléans-Juste P, Jacques D (2011). Nuclear membrane receptors for ET-1 in cardiovascular function. Am J Physiol Regul Integr Comp Physiol 300, R251-R263.
5. Blumer JB, Smrcka AV, Lanier SM (2007). Mechanistic pathways and biological roles for receptor-independent activators of G-protein signaling. Pharmacol Ther 113, 488-506.
6. Bonacci TM, Mathews JL, Yuan C, Lehmann DM, Malik S, Wu D, Font JL, Bidlack JM, Smrcka AV (2006). Differential targeting of G βγ-subunit signaling with small molecules. Science 312, 443-446.
7. Bos JL (2003). Epac: a new cAMP target and new avenues in cAMP research. Nat Rev Mol Cell Biol 4, 733-738.
8. Campelo F, Malhotra V (2012). Membrane fission: the biogenesis of transport carriers. Annu Rev Biochem 81, 407-427.
9. Casey LM, Pistner AR, Belmonte SL, Migdalovich D, Stolpnik O, Nwakanma FE, Vorobiof G, Dunaevsky O, Matavel A, Lopes CM, et al. (2010). Smal molecule disruption of G βγ signaling inhibits the progression of heart failure. Circ Res 107, 532-539.
10. Chisari M, Saini DK, Kalyanaraman V, Gautam N (2007). Shuttling of G protein subunits between the plasma membrane and intracellular membranes. J Biol Chem 282, 24092-24098.
11. q overexpression induces cardiac contractile failure in mice. Proc Natl Acad Sci USA 94, 8121-8126.
12. Diaz Anel AM (2007). Phospholipase C β3 is a key component in the G βγ/PKCη/PKD-mediated regulation of trans-Golgi network to plasma membrane transport. Biochem J 406, 157-165.
13. 2- and PKD-mediated transport to the cell surface and the organization of the Golgi apparatus. J Cell Biol 169, 83-91.
14. Fielitz J, Kim M-S, Shelton JM, Qi X, Hill JA, Richardson JA, Bassel-Duby R, Olson EN (2008). Requirement of protein kinase D1 for pathologica cardiac remodeling. Proc Natl Acad Sci USA 105, 3059-3063.
15. Filtz TM, Grubb DR, McLeod-Dryden TJ, Luo J, Woodcock EA (2009). Gq-initiated cardiomyocyte hypertrophy is mediated by phospholipase Cβ1b. FASEB J 23, 3564-3570.
16. Irannejad R, Wedegaertner PB (2010). Regulation of constitutive cargo transport from the trans-Golgi network to plasma membrane by Golgilocalized G protein βγ subunits. J Biol Chem 285, 32393-32404.
17. Jamora C, Yamanouye N, Van Lint J, Laudenslager J, Vandenheede JR, Faulkner DJ, Malhotra V (1999). G βγ-mediated regulation of Golgi organization is through the direct activation of protein kinase D. Cell 98, 59-68.
18. Knowlton KU, Michel MC, Itani M, Shubeita HE, Ishihara K, Brown JH, Chien KR (1993). The α 1A-adrenergic receptor subtype mediates biochemical, molecular, and morphologic features of cultured myocardial cel hypertrophy. J Biol Chem 268, 15374-15380.
19. Koch WJ, Rockman HA, Samama P, Hamilton RA, Bond RA, Milano CA, Lefkowitz RJ (1995). Cardiac function in mice overexpressing the b-adrenergic receptor kinase or a β ARK inhibitor. Science 268, 1350-1353.
20. Kunkel MT, Toker A, Tsien RY, Newton AC (2007). Calcium-dependent regulation of protein kinase D revealed by a genetically encoded kinase activity reporter. J Biol Chem 282, 6733-6742.
21. Lorenz K, Schmitt JP, Schmitteckert EM, Lohse MJ (2009). A new type of ERK1/2 autophosphorylation causes cardiac hypertrophy. Nat Med 15, 75-83.
22. Naga Prasad SV, Esposito G, Mao L, Koch WJ, Rockman HA (2000). G βγ-dependent phosphoinositide 3-kinase activation in hearts with in vivo pressure overload hypertrophy. J Biol Chem 275, 4693-4698.
23. Nienaber JJ, Tachibana H, Naga Prasad SV, Esposito G, Wu D, Mao L, Rockman HA (2003). Inhibition of receptor-localized PI3K preserves cardiac β-adrenergic receptor function and ameliorates pressure overload heart failure. J Clin Invest 112, 1067-1079.
24. 2+ release in the heart by activation of protein kinase Cε and calcium-calmodulin kinase II. J Biol Chem 284, 1514-1522.
25. 2+ mobilization in cardiac myocytes. J Biol Chem 282, 5488-5495.
26. O'Neill PR, Karunarathne W K A, Kalyanaraman V, Silvius JR, Gautam N (2012). G-protein signaling leverages subunit-dependent membrane affinity to differentially control βγ translocation to intracellular membranes. Proc Natl Acad Sci USA 109, E3568-E3577.
27. Oner SS, Vural A, Lanier SM (2013). Translocation of activator of G-protein signaling 3 to the Golgi apparatus in response to receptor activation and its effect on the trans-Golgi network. J Biol Chem 288, 24091-24103.
28. Perrino C, Rockman HA, Chiariello M (2006). Targeted inhibition of phosphoinositide 3-kinase activity as a novel strategy to normalize β-adrenergic receptor function in heart failure. Vasc Pharmacol 45, 77-85.
29. Prasad S V N., Perrino C, Rockman HA (2003). Role of phosphoinositide 3-kinase in cardiac function and heart failure. Trends Cardiovasc Med 13, 206-212.
30. Rengo G, Lymperopoulos A, Leosco D, Koch WJ (2011). GRK2 as a novel gene therapy target in heart failure. J Mol Cell Cardiol 50, 785-792.
31. Rockman HA, Chien KR, Choi DJ, Iaccarino G, Hunter JJ, Ross J Jr, Lefkowitz RJ, Koch WJ (1998). Expression of a β-adrenergic receptor kinase 1 inhibitor prevents the development of myocardial failure in genetargeted mice. Proc Natl Acad Sci USA 95, 7000-7005.
32. Ruppert C, Deiss K, Herrmann S, Vidal M, Oezkur M, Gorski A, Weidemann F, Lohse MJ, Lorenz K (2013). Interference with ERKThr188 phosphorylation impairs pathological but not physiological cardiac hypertrophy. Proc Natl Acad Sci USA 110, 7440-7445.
33. Saini DK, Kalyanaraman V, Chisari M, Gautam N (2007). A family of G protein βγ subunits translocate reversibly from the plasma membrane to endomembranes on receptor activation. J Biol Chem 282, 24099-24108.
34. Saini DK, Karunarathne WK, Angaswamy N, Saini D, Cho JH, Kalyanaraman V, Gautam N (2010). Regulation of Golgi structure and secretion by receptor-induced G protein βγ complex translocation. Proc Natl Acad Sci USA 107, 11417-11422.
35. Santagata S, Boggon TJ, Baird CL, Gomez CA, Zhao J, Shan WS, Myszka DG, Shapiro L (2001). G-protein signaling through tubby proteins. Science 292, 2041-2050.
36. Smrcka AV, Brown JH, Holz GG (2012). Role of phospholipase Cε in physiological phosphoinositide signaling networks. Cell Signal 29, 1333-1343.
37. Smrcka AV, Hepler JR, Brown KO, Sternweis PC (1991). Regulation of polyphosphoinositide-specific phospholipase C activity by purified Gq. Science 251, 804-807.
38. Taylor SJ, Chae HZ, Rhee SG, Exton JH (1991). Activation of the β1 isozyme of phospholipase C by α subunits of the G q class of G proteins. Nature 350, 516-518.
39. Teruel MN, Blanpied TA, Shen K, Augustine GJ, Meyer T (1999). A versatile microporation technique for the transfection of cultured CNS neurons. J Neurosci Methods 93, 37-48.
40. Thal DM, Homan KT, Chen J, Wu EK, Hinkle PM, Huang ZM, Chuprun JK, Song J, Gao E, Cheung JY, et al. (2012). Paroxetine is a direct inhibitor of g protein-coupled receptor kinase 2 and increases myocardial contractility. ACS Chem Biol 7, 1830-1839.
41. Thal DM, Yeow RY, Schoenau C, Huber J, Tesmer JJ (2011). Molecular mechanism of selectivity among G protein-coupled receptor kinase 2 inhibitors. Mol Pharmacol 80, 294-303.
42. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN, McKinsey TA (2004). Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 24, 8374-8385.
43. Wang H, Oestreich EA, Maekawa N, Bullard TA, Vikstrom KL, Dirksen RT, Kelley GG, Blaxall BC, Smrcka AV (2005). Phospholipase Cε modulates β-adrenergic receptor-dependent cardiac contraction and inhibits cardiac hypertrophy. Circ Res 97, 1305-1313.
44. Wing MR, Houston D, Kelley GG, der CJ, Siderovski DP, Harden TK (2001). Activation of phospholipase C-ε by heterotrimeric G protein βγ-subunits. J Biol Chem 276, 48257-48261.
45. 2+ signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 116, 675-682.
46. Zhang L, Malik S, Kelley GG, Kapiloff MS, Smrcka AV (2011). Phospholipase Cε scaffolds to muscle-specific A kinase anchoring protein (mAKAP (3) and integrates multiple hypertrophic stimuli in cardiac myocytes. J Biol Chem 286, 23012-23021.
47. Zhang L, Malik S, Pang J, Wang H, Park K, Yule D, Blaxall B, Smrcka A (2013). Phospholipase Cε hydrolyzes perinuclear phosphatidylinositol 4-phosphate to regulate cardiac hypertrophy. Cell 153, 216-227.