Absence of SOCS3 in the cardiomyocyte increases mortality in a gp130-dependent manner accompanied by contractile dysfunction and ventricular arrhythmias

Circulation

Volumn 124, Issue 24, 2011, Pages 2690-2701

  Yajima, Toshitaka ^a   Murofushi, Yoshiteru ^a   Zhou, Hanbing ^a   Park, Stanley ^a   Housman, Jonathan ^a   Zhong, Zhao Hua ^b   Nakamura, Michinari ^a   MacHida, Mitsuyo ^a   Hwang, Kyung Kuk ^a   Gu, Yusu ^a   Dalton, Nancy D ^a   Yajima, Tomoko ^a   Yasukawa, Hideo ^c   Peterson, Kirk L ^a   Knowlton, Kirk U ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

cardiomyopathy; gp130; heart failure; myofilament Ca 2+ sensitivity; SOCS3; SR Ca 2+ overload; ventricular arrhythmia

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; CALSEQUESTRIN; CRE RECOMBINASE; GLYCOPROTEIN GP 130; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOLAMBAN; PROTEIN KINASE B; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; SYNAPTOPHYSIN; TROPONIN I; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE COURSE; HEART DISEASE; HEART FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE ARRHYTHMIA; HEART WEIGHT; MORTALITY; MOUSE; MUSCLE FIBRIL; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALCIUM SIGNALING; CARDIOMYOPATHY, DILATED; CYTOKINE RECEPTOR GP130; DISEASE MODELS, ANIMAL; HEART FAILURE; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; SODIUM CHANNELS; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 83455168966     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.028498     Document Type: Article

References (42)

1. Ernst M. Acquiring signalling specificity from the cytokine receptor gp130. Trends Genet. 2004;20:23-32. (Pubitemid 38032817)
2. Hilfiker-Kleiner D, Shukla P, Klein G, Schaefer A, Stapel B, Hoch M, Muller W, Scherr M, Theilmeier G, Ernst M, Hilfiker A, Drexler H. Continuous glycoprotein-130-mediated signal transducer and activator of transcription-3 activation promotes inflammation, left ventricular rupture, and adverse outcome in subacute myocardial infarction. Circulation. 2010;122:145-155.
3. Yajima T, Knowlton KU. Viral myocarditis: from the perspective of the virus. Circulation. 2009;119:2615-2624.
4. Hirota H, Chen J, Betz UA, Rajewsky K, Gu Y, Ross J Jr, Muller W, Chien KR. Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress. Cell. 1999;97:189-198. (Pubitemid 29194270)
5. Roberts AW, Robb L, Rakar S, Hartley L, Cluse L, Nicola NA, Metcalf D, Hilton DJ, Alexander WS. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc Natl Acad Sci USA. 2001;98:9324-9329. (Pubitemid 32743915)
6. Takahashi Y, Carpino N, Cross JC, Torres M, Parganas E, Ihle JN. Socs3: an essential regulator of lif receptor signaling in trophoblast giant cell differentiation. EMBO J. 2003;22:372-384. (Pubitemid 36193583)
7. Finkel MS, Oddis CV, Jacob TD, Watkins SC, Hattler BG, Simmons RL. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science. 1992;257:387-389.
8. Hedayat M, Mahmoudi MJ, Rose NR, Rezaei N. Proinflammatory cytokines in heart failure: double-edged swords. Heart Failure Rev. 2010;15: 543-562.
9. Szabo-Fresnais N, Lefebvre F, Germain A, Fischmeister R, Pomérance M. A new regulation of ILl-6 production in adult cardiomyocytes by-adrenergic and IL-1f receptors and induction of cellular hypertrophy by IL-6 trans-signalling. Cell Signal. 2010;22:1143-1152.
10. Hirota H, Izumi M, Hamaguchi T, Sugiyama S, Murakami E, Kunisada K, Fujio Y, Oshima Y, Nakaoka Y, Yamauchi-Takihara K. Circulating interleukin-6 family cytokines and their receptors in patients with congestive heart failure. Heart Vessels. 2004;19:237-241. (Pubitemid 39335083)
11. MacGowan GA, Mann DL, Kormos RL, Feldman AM, Murali S. Circulating interleukin-6 in severe heart failure. Am J Cardiol. 1997;79: 1128-1131. (Pubitemid 27221935)
12. Maeda K, Tsutamoto T, Wada A, Mabuchi N, Hayashi M, Tsutsui T, Ohnishi M, Sawaki M, Fujii M, Matsumoto T, Kinoshita M. High levels of plasma brain natriuretic peptide and interleukin-6 after optimized treatment for heart failure are independent risk factors for morbidity and mortality in patients with congestive heart failure. J Am Coll Cardiol. 2000;36:1587-1593.
13. Vasan RS, Sullivan LM, Roubenoff R, Dinarello CA, Harris T, Benjamin EJ, Sawyer DB, Levy D, Wilson PW, D'Agostino RB. Inflammatory markers and risk of heart failure in elderly subjects without prior myocardial infarction: The Framingham Heart Study. Circulation. 2003;107: 1486-1491. (Pubitemid 36378485)
14. Bulcao CF, D'Souza KM, Malhotra R, Staron M, Duffy JY, Pandalai PK, Jeevanandam V, Akhter SA. Activation of jak-stat and nitric oxide signaling as a mechanism for donor heart dysfunction. J Heart Lung Transplant. 2010;29:346-351.
15. Mann DL, Topkara VK, Evans S, Barger PM. Innate immunity in the adult mammalian heart: for whom the cell tolls. Trans Am Clin Climatol Assoc. 2010;121:34.
16. Margulies KB, Matiwala S, Cornejo C, Olsen H, Craven WA, Bednarik D. Mixed messages: transcription patterns in failing and recovering human myocardium. Circ Res. 2005;96:592-599. (Pubitemid 40463469)
17. Podewski EK. Alterations in janus kinase (jak)-signal transducers and activators of transcription (stat) signaling in patients with end-stage dilated cardiomyopathy. Circulation. 2003;107:798-802. (Pubitemid 36241034)
18. Fourouclas N, Li J, Gilby DC, Campbell PJ, Beer PA, Boyd EM, Goodeve AC, Bareford D, Harrison CN, Reilly JT, Green AR, Bench AJ. Methylation of the suppressor of cytokine signaling 3 gene (socs3) in myeloproliferative disorders. Haematologica. 2008;93:1635-1644.
19. Isomoto H. Epigenetic alterations in cholangiocarcinoma-sustained IL-6/stat3 signaling in cholangio-carcinoma due to socs3 epigenetic silencing. Digestion. 2009;79(Suppl 1):2-8.
20. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, Hirano T, Chien KR, Yoshimura A. IL-6 induces an anti-inflammatory response in the absence of socs3 in macrophages. Nat Immunol. 2003;4:551-556. (Pubitemid 36701338)
21. Yajima T, Yasukawa H, Jeon ES, Xiong D, Dorner A, Iwatate M, Nara M, Zhou H, Summers-Torres D, Hoshijima M, Chien KR, Yoshimura A, Knowlton KU. Innate defense mechanism against virus infection within the cardiac myocyte requiring gp130-stat3 signaling. Circulation. 2006; 114:2364-2373. (Pubitemid 44847453)
22. Kondo RP. Comparison of contraction and calcium handling between right and left ventricular myocytes from adult mouse heart: a role for repolarization waveform. J Physiol. 2005;571:131-146.
23. McDonough PM, Stella SL, Glembotski CC. Involvement of cytoplasmic calcium and protein kinases in the regulation of atrial natriuretic factor secretion by contraction rate and endothelin. J Biol Chem. 1994;269: 9466-9472.
24. Yasukawa H, Hoshijima M, Gu YS, Nakamura T, Pradervand S, Hanada T, Hanakawa Y, Yoshimura A, Ross J, Chien KR. Suppressor of cytokine signaling-3 is a biomechanical stress-inducible gene that suppresses gp130-mediated cardiac myocyte hypertrophy and survival pathways. J Clin Invest. 2001;108:1459-1467. (Pubitemid 33091983)
25. Fischer P, Hilfiker-Kleiner D. Survival pathways in hypertrophy and heart failure: the gp130-stat3 axis. Basic Res Cardiol. 2007;102:279-297. (Pubitemid 46909707)
26. Kinugawa K, Takahashi T, Kohmoto O, Yao A, Aoyagi T, Momomura S, Hirata Y, Serizawa T. Nitric oxide-mediated effects of interleukin-6 on Ca2r(i) and cell contraction in cultured chick ventricular myocytes. Circ Res. 1994;75:285-295.
27. Yu X. Jak2/stat3, not erk1/2, mediates interleukin-6-induced activation of inducible nitric-oxide synthase and decrease in contractility of adult ventricular myocytes. J Biol Chem. 2003;278:16304-16309. (Pubitemid 36799756)
28. Yu XW. Inhibition of sarcoplasmic reticular function by chronic interleukin-6 exposure via inos in adult ventricular myocytes. J Physiol. 2005;566:327-340.
29. Croker BA, Krebs DL, Zhang JG, Wormald S, Willson TA, Stanley EG, Robb L, Greenhalgh CJ, Forster I, Clausen BE, Nicola NA, Metcalf D, Hilton DJ, Roberts AW, Alexander WS. Socs3 negatively regulates IL-6 signaling in vivo. Nat Immunol. 2003;4:540-545. (Pubitemid 36701336)
30. Lang R, Pauleau AL, Parganas E, Takahashi Y, Mages J, Ihle JN, Rutschman R, Murray PJ. Socs3 regulates the plasticity of gp130 signaling. Nat Immunol. 2003;4:546-550. (Pubitemid 36701337)
31. Bezzina CR, Remme CA. Dilated cardiomyopathy due to sodium channel dysfunction: what is the connection? Circ Arrhythm Electrophysiol. 2008; 1:80-82.
32. Bers DM, Barry WH, Despa S. Intracellular Na2 regulation in cardiac myocytes. Cardiovasc Res. 2003;57:897-912. (Pubitemid 36324595)
33. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415: 198-205. (Pubitemid 34059525)
34. Solaro RJ, van der Velden J. Why does troponin I have so many phosphorylation sites? Fact and fancy. J Mol Cell Cardiol. 2010;48:810-816.
35. Yasuda S, Coutu P, Sadayappan S, Robbins J, Metzger JM. Cardiac transgenic and gene transfer strategies converge to support an important role for troponin I in regulating relaxation in cardiac myocytes. Circ Res. 2007;101:377-386. (Pubitemid 47267706)
36. Bodor GS, Oakeley AE, Allen PD, Crimmins DL, Ladenson JH, Anderson PA. Troponin I phosphorylation in the normal and failing adult human heart. Circulation. 1997;96:1495-1500. (Pubitemid 27375342)
37. Messer AE, Jacques AM, Marston SB. Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J Mol Cell Cardiol. 2007;42:247-259. (Pubitemid 44970468)
38. Bristow MR, Ginsburg R, Minobe W, Cubicciotti RS, Sageman WS, Lurie K, Billingham ME, Harrison DC, Stinson EB. Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N Engl J Med. 1982;307:205-211. (Pubitemid 12079105)
39. Buerger A, Rozhitskaya O, Sherwood MC, Dorfman AL, Bisping E, Abel ED, Pu WT, Izumo S, Jay PY. Dilated cardiomyopathy resulting from high-level myocardial expression of cre-recombinase. J Card Fail. 2006; 12:392-398. (Pubitemid 43817587)
40. Loonstra A, Vooijs M, Beverloo HB, Al Allak B, van Drunen E, Kanaar R, Berns A, Jonkers J. Growth inhibition and DNA damage induced by cre recombinase in mammalian cells. Proc Natl Acad Sci USA. 2001; 98:9209-9214. (Pubitemid 32743895)
41. Schmidt EE, Taylor DS, Prigge JR, Barnett S, Capecchi MR. Illegitimate cre-dependent chromosome rearrangements in transgenic mouse spermatids. Proc Natl Acad Sci USA. 2000;97:13702-13707.
42. Silver DP, Livingston DM. Self-excising retroviral vectors encoding the cre recombinase overcome cre-mediated cellular toxicity. Mol Cell. 2001;8:233-243. (Pubitemid 32772921)