Increases in intracellular sodium activate transcription and gene expression via the salt-inducible kinase 1 network in an atrial myocyte cell line

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 1, 2012, Pages

  Popov, Sergej ^a   Venetsanou, Kyriaki ^a   Jorge Chedrese, P ^a   Pinto, Vanda ^b   Takemori, Hiroshi ^c   Franco Cereceda, Anders ^d   Eriksson, Per ^a   Mochizuki, Naoki ^e   Soares da Silva, Patricio ^b   Bertorello, Alejandro M ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b Inst of Pharmacol and Therapeutics   (Portugal)

^c NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^d KAROLINSKA INSTITUTE   (Sweden)

^e NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

Cardiac hypertrophy; Hypertension; Ion gradients; K+ ATPase; Na+

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; HISTONE DEACETYLASE 5; MYOCYTE ENHANCER FACTOR 2; MYOSIN HEAVY CHAIN; NATRIURETIC PEPTIDE RECEPTOR A; PROTEIN KINASE; SALT INDUCIBLE KINASE 1; SODIUM CALCIUM EXCHANGE PROTEIN; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ARTERIAL PRESSURE; ARTICLE; CELL CULTURE; ENZYME ACTIVITY; GENE EXPRESSION; HEART DEVELOPMENT; HEART VENTRICLE HYPERTROPHY; MECHANICAL STRESS; MUSCLE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SALT INTAKE; SODIUM CELL LEVEL;

BIOPSY; CARDIOMEGALY; CELL LINE; GENE EXPRESSION; HEART ATRIA; HISTONE DEACETYLASES; HUMANS; HYDROGEN-ION CONCENTRATION; MADS DOMAIN PROTEINS; MONENSIN; MYOCYTES, CARDIAC; MYOGENIC REGULATORY FACTORS; NFATC TRANSCRIPTION FACTORS; PHOSPHORYLATION; PLASMIDS; PROTEIN-SERINE-THREONINE KINASES; RNA; SODIUM; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84863636917     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00512.2011     Document Type: Article

References (57)

1. Adrogué HJ, Madias NE. Sodium and potassium in the pathogenesis of hypertension. N Engl J Med 356: 1966-1978, 2007.
2. Berdeaux R, Goebel N, Banaszynski L, Takemori H, Wandless T, Shelton GD, Montminy M. SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes. Nat Med 13: 597-603, 2007.
3. Berk BC, Vekshtein V, Gordon HM, Tsuda T. Angiotensin II-stimulated protein synthesis in cultured vascular smooth muscle cells. Hypertension 13: 305-314, 1989.
4. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529, 2003.
5. Black BL, Olson EN. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14: 167-196, 1998.
6. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95: 2979-2984, 1998.
7. Dai YS, Xu J, Molkentin JD. The DnaJ-related factor Mrj interacts with nuclear factor of activated T cells c3 and mediates transcriptional repression through class II histone deacetylase recruitment. Mol Cell Biol 25: 9936-9948, 2005.
8. + -ATPase activity is modulated by intracellular sodium concentration. J Biol Chem 277: 11489-11496, 2002.
9. Frey N, Olson EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol 65: 45-79, 2003.
10. Frohlich ED, Chien Y, Sesoko S, Pegram BL. Relationship between dietary sodium intake, hemodynamics, and cardiac mass in SHR and WKY rats. Am J Physiol Regul Integr Comp Physiol 264: R30-R34, 1993.
11. Gan XT, Gong XQ, Xue J, Haist JV, Bai D, Karmazyn M. Sodiumhydrogen exchange inhibition attenuates glycoside-induced hypertrophy in rat ventricular myocytes. Cardiovasc Res 85: 79-89, 2010.
12. 2+ release channel dysfunction. Circ Res 98: 88-97, 2006.
13. + pump. Am J Physiol Regul Integr Comp Physiol 290: R1142-R1150, 2006.
14. Grépin C, Dagnino L, Robitaille L, Haberstroh L, Antakly T, Nemer M. A hormone-encoding gene identifies a pathway for cardiac but not skeletal muscle gene transcription. Mol Cell Biol 14: 3115-3129, 1994.
15. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10: 32-42, 2009.
16. Hamm LL, Hering-Smith KS. Pivotal role of the kidney in hypertension. Am J Med Sci 340: 30-32, 2010.
17. Han J, Molkentin JD. Regulation of MEF2 by p38 MAPK and its implication in cardiomyocyte biology. Trends Cardiovasc Med 10: 19-22, 2000.
18. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7: 589-600, 2006.
19. 2+ release is a nexus for hypertrophic signaling in cardiac myocytes. Mol Cell 33: 472-482, 2009.
20. Jaleel M, McBride A, Lizcano JM, Deak M, Toth R, Morrice NA, Alessi DR. Identification of the sucrose non-fermenting related kinase SNRK, as a novel LKB1 substrate. FEBS Lett 579: 1417-1423, 2005.
21. Katoh Y, Takemori H, Doi J, Okamoto M. Identification of the nuclear localization domain of salt-inducible kinase. Endocr Res 28: 315-318, 2002.
22. Kent RL, Hoober JK, Cooper G 4th. Load responsiveness of protein synthesis in adult mammalian myocardium: role of cardiac deformation linked to sodium influx. Circ Res 64: 74-85, 1989.
23. 2+ exchanger in response to cardiac pressure overload. Am J Physiol Heart Circ Physiol 265: H1024-H1029, 1993.
24. Kertesz N, Samson J, Debacker C, Wu H, Labastie MC. Cloning and characterization of human and mouse SNRK sucrose non-fermenting protein (SNF-1)-related kinases. Gene 294: 13-24, 2002.
25. Kino T, Takatori H, Manoli I, Wang Y, Tiulpakov A, Blackman MR, Su YA, Chrousos GP, DeCherney AH, Segars JH. Brx mediates the response of lymphocytes to osmotic stress through the activation of NFAT5. Sci Signal 2: ra5, 2009.
26. Lee Y, Nadal-Ginard B, Mahdavi V, Izumo S. Myocyte-specific enhancer factor 2 and thyroid hormone receptor associate and synergistically activate the alpha-cardiac myosin heavy-chain gene. Mol Cell Biol 17: 2745-2755, 1997.
27. Lin Q, Schwarz J, Bucana C, Olson EN. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276: 1404-1407, 1997.
28. Lin X, Takemori H, Katoh Y, Doi J, Horike N, Makino A, Nonaka Y, Okamoto M. Salt-inducible kinase is involved in the ACTH/cAMPdependent protein kinase signaling in Y1 mouse adrenocortical tumor cells. Mol Endocrinol 15: 1264-1276, 2001.
29. 2+ /calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Invest 119: 1230-1240, 2009.
30. Lorell BH, Carabello BA. Left ventricular hypertrophy: pathogenesis, detection, and prognosis. Circulation 102: 470-479, 2000.
31. Molkentin JD. Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovasc Res 63: 467-475, 2004.
32. Morin S, Charron F, Robitaille L, Nemer M. GATA-dependent recruitment of MEF2 proteins to target promoters. EMBO J 19: 2046-2055, 2000.
33. Nebbioso A, Manzo F, Miceli M, Conte M, Manente L, Baldi A, De Luca A, Rotili D, Valente S, Mai A, Usiello A, Gronemeyer H, Altucci L. Selective class II HDAC inhibitors impair myogenesis by modulating the stability and activity of HDAC-MEF2 complexes. EMBO Rep 10: 776-782, 2009.
34. Paloschi V, Kurtovic S, Folkersen L, Gomez D, Wågsäter D, Roy J, Petrini J, Eriksson MJ, Caidahl K, Hamsten A, Liska J, Michel JB, Franco-Cereceda A, Eriksson P. Impaired splicing of fibronectin is associated with thoracic aortic aneurysm formation in patients with bicuspid aortic valve. Arterioscler Thromb Vasc Biol 31: 691-697, 2011.
35. Pinto V, Pinho MJ, Hopfer U, Jose PA, Soares-da-Silva P. Oxidative stress and the genomic regulation of aldosterone-stimulated NHE1 activity in SHR renal proximal tubular cells. Mol Cell Biochem 310: 191-201, 2008.
36. Putt ME, Hannenhalli S, Lu Y, Haines P, Chandrupatla HR, Morrisey EE, Margulies KB, Cappola TP. Evidence for coregulation of myocardial gene expression by MEF2 and NFAT in human heart failure. Circ Cardiovasc Genet 2: 212-219, 2009.
37. kip2. Plos ONE 5: e9029, 2010.
38. Roth I, Leroy V, Kwon HM, Martin PY, Féraille E, Hasler U. The osmoprotective transcription factor NFAT5/TonEBP Mmodulates NF-B activity. Mol Biol Cell 21: 3459-3474, 2009.
39. Ruiz JC, Conlon FL, Robertson EJ. Identification of novel protein kinases expressed in the myocardium of the developing mouse heart. Mech Dev 48: 153-164, 1994.
40. Schmieder RE, Messerli FH, Caravaglia GE, Nunez BD. Dietary salt intake. A determinant of cardiac involvement in essential hypertension. Circulation 78: 951-956, 1988.
41. Schulz RA, Yutzey KE. Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev Biol 266: 1-16, 2004.
42. Shin HH, Seoh JY, Chung HY, Choi SJ, Hahn MJ, Kang JS, Choi MS, Han TH. Requirement of MEF2D in the induced differentiation of HL60 promyeloid cells. Mol Immunol 36: 1209-1214, 1999.
43. Sjöström M, Stenström K, Eneling K, Zwiller J, Katz AI, Takemori H, Bertorello AM. SIK1 is part of a cell sodium-sensing network that regulates active sodium transport through a calcium-dependent process. Proc Natl Acad Sci USA 104: 16922-16927, 2007.
44. Stenström K, Takemori H, Bianchi G, Katz AI, Bertorello AM. Blocking the salt-inducible kinase 1 network prevents the increases in cell sodium transport caused by a hypertension-linked mutation in human α-adducin. J Hypertens 27: 2452-2457, 2009.
45. Takeda Y, Yoneda T, Demura M, Miyamori I, Mabuchi H. Sodiuminduced cardiac aldosterone synthesis causes cardiac hypertrophy. Endocrinology 141: 1901-1904, 2000.
46. Takemori H, Kajimura J, Okamoto M. TORC-SIK cascade regulates CREB activity through the basic leucine zipper domain. FEBS J 274: 3202-3209, 2007.
47. Takemori H, Katoh Y, Hashimoto Y, Nakae J, Olson EN, Okamoto M. Inactivation of HDAC5 by SIK1 in AICAR-treated C2C12 myoblasts. Endocr J 56: 121-130, 2009.
48. van der Linden AM, Wiener S, You YJ, Kim K, Avery L, Sengupta P. The EGL-4 PKG acts with KIN-29 salt-inducible kinase and protein kinase A to regulate chemoreceptor gene expression and sensory behaviors in Caenorhabditis elegans. Genetics 180: 1475-1491, 2008.
49. Wang Z, Takemori H, Halder SK, Nonaka Y, Okamoto M. Cloning of a novel kinase (SIK) of the SNF1/AMPK family from high salt diet-treated rat adrenal. FEBS Lett 453: 135-139, 1999.
50. White SM, Constantin PE, Claycomb WC. Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 286: H823-H829, 2004.
51. Wilkins BJ, Molkentin JD. Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochem Biophys Res Commun 322: 1178-1191, 2004.
52. Witcher DR, Kovacs RJ, Schulman H, Cefali DC, Jones LR. Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem 266: 11144-11152, 1991.
53. + -ATPase to hypertrophy and its marker genes in cardiac myocytes. J Biol Chem 274: 19323-19328, 1999.
54. Yamamoto K, Ikeda U, Seino Y, Tsuruya Y, Oguchi A, Okada K, Ishikawa Saito T S, Kawakami K, Hara Y, Shimada K. Regulation of Na, K-adenosine triphosphatase gene expression by sodium ions in cultured neonatal rat cardiocytes. J Clin Invest 92: 1889-1895, 1993.
55. 1325 S mice. Am J Physiol Cell Physiol 301: C577-C586, 2011.
56. Youn HD, Chatila TA, Liu JO. Integration of calcineurin and MEF2 signals by the coactivator p300 during T-cell apoptosis. EMBO J 19: 4323-4331, 2000.
57. Zhang CL, McKinsey TA, Chang S, Antos CL, Hill JA, Olson EN. Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110: 479-488, 2002.