SERCA Cys674 sulphonylation and inhibition of L-type Ca2+ influx contribute to cardiac dysfunction in endotoxemic mice, independent of cGMP synthesis

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 8, 2013, Pages

  Hobai, Ion A ^a,b   Buys, Emmanuel S ^b   Morse, Justin C ^a   Edgecomb, Jessica ^a   Weiss, Eric H ^b   Armoundas, Antonis A ^b   Hou, Xiuyun ^a   Khandelwal, Alok R ^a   Siwik, Deborah A ^a   Brouckaert, Peter ^c   Cohen, Richard A ^a   Colucci, Wilson S ^a  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Cardiomyopathy; Contractility; Cysteine; Oxidative stress; Sarco(endo)plasmic reticulum Ca2+ ATPase; Sarcoplasmic reticulum; Sepsis

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CYCLIC GMP; GUANYLATE CYCLASE; IODOACETAMIDE; PHOSPHOLAMBAN; RYANODINE RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; CALCIUM; CALCIUM BINDING PROTEIN; CALCIUM CHANNEL L TYPE; CYSTEINE; LIPOPOLYSACCHARIDE; SODIUM CALCIUM EXCHANGE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CARDIOMYOPATHY; CONTROLLED STUDY; ENDOTOXEMIA; ENZYME SYNTHESIS; GENOTYPE; IMMUNOHISTOCHEMISTRY; MOUSE; MYOFILAMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SARCOMERE; SEPSIS; SODIUM CALCIUM EXCHANGE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENETICS; HEART; HEART MUSCLE; HEART MUSCLE CELL; KNOCKOUT MOUSE; MALE; METABOLISM; MUSCLE CONTRACTILITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SARCO(ENDO)PLASMIC RETICULUM CA2+-ATPASE; SARCOPLASMIC RETICULUM;

CARDIOMYOPATHY; CONTRACTILITY; CYSTEINE; OXIDATIVE STRESS; SARCO(ENDO)PLASMIC RETICULUM CA2+-ATPASE; SARCOPLASMIC RETICULUM; SEPSIS;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM-BINDING PROTEINS; CYCLIC GMP; CYSTEINE; ENDOTOXEMIA; GUANYLATE CYCLASE; HEART; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN PROCESSING, POST-TRANSLATIONAL; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOMERES; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SODIUM-CALCIUM EXCHANGER;

EID: 84885587677     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00392.2012     Document Type: Article

References (41)

1. 2-ATPase function and lowers tyrosine nitration in hypercholesterolemia and improves nitric oxide-induced relaxation. Circ Res 90: 1114-1121, 2002.
2. Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schoneich C, Cohen RA. S-glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 10: 1200-1207, 2004.
3. Bassani JW, Bassani RA, Bers DM. Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476: 279-293, 1994.
4. Bruni FD, Komwatana P, Soulsby ME, Hess ML. Endotoxin and myocardial failure: role of the myofibril and venous return. Am J Physiol Heart Circ Physiol 235: H150-H156, 1978.
5. 1 attenuates cardiac dysfunction and mortality in murine inflammatory shock models. Am J Physiol Heart Circ Physiol 297: H654-H663, 2009.
6. Buys ES, Sips P, Vermeersch P, Raher MJ, Rogge E, Ichinose F, Dewerchin M, Bloch KD, Janssens S, Brouckaert P. Gender-specific hypertension and responsiveness to nitric oxide in sGC 1 knockout mice. Cardiovasc Res 79: 179-186, 2008.
7. Comini L, Boraso A, Bachetti T, Bernocchi P, Pasini E, Bastianon D, Curello S, Terracciano CM, Ceconi C, Ferrari R. Effects of endotoxic shock on neuronal NOS and calcium transients in rat cardiac myocytes. Pharmacol Res 51: 409-417, 2005.
8. Cui X, Besch V, Khaibullina A, Hergen A, Quezado M, Eichacker P, Quezado ZM. Neuronal nitric oxide synthase deficiency decreases survival in bacterial peritonitis and sepsis. Intensive Care Med 33: 1993-2003, 2007.
9. Cuzzocrea S, McDonald MC, Mazzon E, Filipe HM, Centorrino T, Lepore V, Terranova ML, Ciccolo A, Caputi AP, Thiemermann C. Beneficial effects of tempol, a membrane-permeable radical scavenger, on the multiple organ failure induced by zymosan in the rat. Crit Care Med 29: 102-111, 2001.
10. 2generation by rat heart mitochondria. Mol Cell Biochem 309: 77-85, 2008.
11. Fischmeister R, Castro L, Abi-Gerges A, Rochais F, Vandecasteele G. Speciesand tissue-dependent effects of NO and cyclic GMP on cardiac ion channels. Comp Biochem Physiol A Mol Integr Physiol 142: 136-143, 2005.
12. Flynn A, Chokkalingam Mani B, Mather PJ. Sepsis-induced cardiomyopathy: a review of pathophysiologic mechanisms. Heart Fail Rev 15: 605-611, 2010.
13. Galley HF, Howdle PD, Walker BE, Webster NR. The effects of intravenous antioxidants in patients with septic shock. Free Radic Biol Med 23: 768-774, 1997.
14. Hobai IA, O'Rourke B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 103: 1577-1584, 2001.
15. Ichinose F, Bloch KD, Wu JC, Hataishi R, Aretz HT, Picard MH, Scherrer-Crosbie M. Pressure overload-induced LV hypertrophy and dysfunction in mice are exacerbated by congenital NOS3 deficiency. Am J Physiol Heart Circ Physiol 286: H1070-H1075, 2004.
16. Ichinose F, Buys ES, Neilan TG, Furutani EM, Morgan JG, Jassal DS, Graveline AR, Searles RJ, Lim CC, Kaneki M, Picard MH, ScherrerCrosbie M, Janssens S, Liao R, Bloch KD. Cardiomyocyte-specific overexpression of nitric oxide synthase 3 prevents myocardial dysfunction in murine models of septic shock. Circ Res 100: 130-139, 2007.
17. Jozefowicz E, Brisson H, Rozenberg S, Mebazaa A, Gele P, Callebert J, Lebuffe G, Vallet B, Bordet R, Tavernier B. Activation of peroxisome proliferator-activated receptor-alpha by fenofibrate prevents myocardial dysfunction during endotoxemia in rats. Crit Care Med 35: 856-863, 2007.
18. Kumar A, Brar R, Wang P, Dee L, Skorupa G, Khadour F, Schulz R, Parrillo JE. Role of nitric oxide and cGMP in human septic seruminduced depression of cardiac myocyte contractility. Am J Physiol Regul Integr Comp Physiol 276: R265-R276, 1999.
19. 2+ depletion in cardiac myocytes. Free Radic Biol Med 48: 1182-1187, 2010.
20. Lancel S, Tissier S, Mordon S, Marechal X, Depontieu F, Scherpereel A, Chopin C, Neviere R. Peroxynitrite decomposition catalysts prevent myocardial dysfunction and inflammation in endotoxemic rats. J Am Coll Cardiol 43: 2348-2358, 2004.
21. Lancel S, Zhang J, Evangelista A, Trucillo MP, Tong X, Siwik DA, Cohen RA, Colucci WS. Nitroxyl activates SERCA in cardiac myocytes via glutathiolation of cysteine 674. Circ Res 104: 720-723, 2009.
22. Landry DW, Oliver JA. The pathogenesis of vasodilatory shock. N Engl J Med 345: 588-595, 2001.
23. Layland J, Cave AC, Warren C, Grieve DJ, Sparks E, Kentish JC, Solaro RJ, Shah AM. Protection against endotoxemia-induced contractile dysfunction in mice with cardiac-specific expression of slow skeletal troponin I. FASEB J 19: 1137-1139, 2005.
24. Lopez A, Lorente JA, Steingrub J, Bakker J, McLuckie A, Willatts S, Brockway M, Anzueto A, Holzapfel L, Breen D, Silverman MS, Takala J, Donaldson J, Arneson C, Grove G, Grossman S, Grover R. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit Care Med 32: 21-30, 2004.
25. Martins TJ, Mumby MC, Beavo JA. Purification and characterization of a cyclic GMP-stimulated cyclic nucleotide phosphodiesterase from bovine tissues. J Biol Chem 257: 1973-1979, 1982.
26. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
27. q-overexpressing transgenic mice. Circ Heart Fail 3: 306-313, 2010.
28. Rudiger A, Singer M. Mechanisms of sepsis-induced cardiac dysfunction. Crit Care Med 35: 1599-1608, 2007.
29. 2+ leak-load relationship. Circ Res 91: 594-600, 2002.
30. Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, Surdo NC, Craig MA, Smith G, Hamilton G, Zaccolo M. cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ Res 108: 929-939, 2011.
31. Tatsumi T, Keira N, Akashi K, Kobara M, Matoba S, Shiraishi J, Yamanaka S, Mano A, Takeda M, Nishikawa S, Asayama J, Fliss H, Nakagawa M. Nitric oxide-cGMP pathway is involved in endotoxin-induced contractile dysfunction in rat hearts. J Appl Physiol 96: 853-860, 2004.
32. 2+ sensitivity but normal mitochondrial function in septic heart. Am J Respir Crit Care Med 163: 362-367, 2001.
33. Turdi S, Han X, Huff AF, Roe ND, Hu N, Gao F, Ren J. Cardiacspecific overexpression of catalase attenuates lipopolysaccharide-induced myocardial contractile dysfunction: role of autophagy. Free Radic Biol Med 53: 1327-1338, 2012.
34. Ullrich R, Scherrer-Crosbie M, Bloch KD, Ichinose F, Nakajima H, Picard MH, Zapol WM, Quezado ZM. Congenital deficiency of nitric oxide synthase 2 protects against endotoxin-induced myocardial dysfunction in mice. Circulation 102: 1440-1446, 2000.
35. Wu LL, Ji Y, Dong LW, Liu MS. Calcium uptake by sarcoplasmic reticulum is impaired during the hypodynamic phase of sepsis in the rat heart. Shock 15: 49-55, 2001.
36. Wu LL, Liu MS. Impaired calcium uptake by cardiac sarcoplasmic reticulum and its underlying mechanism in endotoxin shock. Mol Cell Biochem 108: 9-17, 1991.
37. Wu LL, Tang C, Dong LW, Liu MS. Altered phospholamban-calcium ATPase interaction in cardiac sarcoplasmic reticulum during the progression of sepsis. Shock 17: 389-393, 2002.
38. 2 ATPase in diabetic pig aorta. Free Radic Biol Med 45: 756-762, 2008.
39. Yu XW, Liu MY, Kennedy RH, Liu SJ. Both cGMP and peroxynitrite mediate chronic interleukin-6-induced negative inotropy in adult rat ventricular myocytes. J Physiol 566: 341-353, 2005.
40. Zhong J, Hwang TC, Adams HR, Rubin LJ. Reduced L-type calcium current in ventricular myocytes from endotoxemic guinea pigs. Am J Physiol Heart Circ Physiol 273: H2312-H2324, 1997.
41. 2+ handling and shortening in sepsis. Crit Care Med 33: 598-604, 2005.