Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel α1 subunit and reduced ischemia/reperfusion injury

Circulation Research

Volumn 98, Issue 3, 2006, Pages 403-411

  Sun, Junhui ^a   Picht, Eckard ^b   Ginsburg, Kenneth S ^b   Bers, Donald M ^b   Steenbergen, Charles ^c   Murphy, Elizabeth ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Endothelial nitric oxide synthase; Gender; Ischemia; L type Ca2+ channel; Neuronal nitric oxide synthase; S nitrosylation

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL L TYPE ALPHA1; CAVEOLIN 3; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ISOPRENALINE; NEURONAL NITRIC OXIDE SYNTHASE; S NITROSOTHIOL; UNCLASSIFIED DRUG;

ADRENERGIC STIMULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; FEMALE; GENDER; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MALE; MOUSE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CARDIOTONIC AGENTS; FEMALE; ISOPROTERENOL; MALE; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; SEX CHARACTERISTICS;

EID: 33646813330     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000202707.79018.0a     Document Type: Article

References (34)

1. Hare JM. Nitric oxide and excitation-contraction coupling. J Mol Cell Cardiol. 2003;35:719-729.
2. Massion PB, Feron O, Dessy C, Balligand JL. Nitric oxide and cardiac function: ten years after, and continuing. Circ Res. 2003;93:388-398.
3. Bredt DS, Snyder SH. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem. 1994;63:175-195.
4. Ignarro LJ, Napoli C, Loscalzo J. Nitric oxide donors and cardiovascular agents modulating the bioactivity of nitric oxide: an overview. Circ Res. 2002;90:21-28.
5. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, Kobeissi ZA, Hobai IA, Lemmon CA, Burnett AL, O'Rourke B, Rodriguez ER, Huang PL, Lima JA, Berkowitz DE, Hare JM. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 2002;416:337-339.
6. Stamler JS, Lamas S, Fang FC. Nitrosylation: the prototypic redox-based signaling mechanism. Cell. 2001;106:675-683.
7. Xu L, Eu JP, Meissner G, Stamler JS. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science. 1998;279:234-237.
8. Xu KY, Huso DL, Dawson TM, Bredt DS, Becker LC. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc Natl Acad Sci U S A. 1999;96:657-662.
9. Khan SA, Skaf MW, Harrison RW, Lee K, Minhas KM, Kumar A, Fradley M, Shoukas AA, Berkowitz DE, Hare JM. Nitric oxide regulation of myocardial contractility and calcium cycling: independent impact of neuronal and endothelial nitric oxide synthases. Circ Res. 2003;92:1322-1329.
10. Campbell DL, Stamler JS, Strauss HC. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol 1996;108:277-293.
11. 2+ channels by S-nitrosothiol nitric oxide donors. Circ Res. 1997;81:742-752.
12. 2+ channels. J Biol Chem. 2001;276:14797-14803.
13. Crabbe DL, Dipla K, Ambati S, Zafeiridis A, Gaughan JP, Houser SR, Margulies KB. Gender differences in post-infarction hypertrophy in end-stage failing hearts. J Am Coll Cardiol. 2003;41:300-306.
14. Barrett-Connor E. Sex differences in coronary heart disease: why are women so superior? Circulation. 1995;95:252-264.
15. 2+ loading and adrenergic stimulation reveal male/female differences in susceptibility to ischemia-reperfusion injury. Am J Physiol. 2002;283:H481-H489.
16. Chen J, Petranka J, Yamamura K, London RE, Steenbergen C, Murphy E. Gender differences in sarcoplasmic reticulum calcium loading after isoproterenol. Am J Physiol. 2003;285:H2657-H2662.
17. 2+ cycling. Curr Opin Drug Discov Devel. 2003;6:658-666.
18. 2+ management in cardiac myocytes. Ann N Y Acad Sci. 2004;1015:28-38.
19. 2+ current. Circ Res. 2001;88:195-201.
20. Eisner DA, Choi HS, Diaz ME, O'Neill SC, Trafford AW. Integrative analysis of calcium cycling in cardiac muscle. Circ Res. 2000;87:1087-1094.
21. Jaffrey SR, Snyder SH. The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE. 2001;86:PL1.
22. 2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice. Circ Res. 1998;83:1215-1223.
23. 5-(1-Imino-3-butenyl)-L-ornithine. A neuronal isoform selective mechanism-based inactivator of nitric oxide synthase. J Biol Chem. 1998;273:8882-8889.
24. Tong H, Imahashi K, Steenbergen C, Murphy E. Phosphorylation of glycogen synthase kinase-3β during preconditioning through a phosphatidylinositol-3- kinase-dependent pathway is cardioprotective. Circ Res. 2002;90:377-379.
25. Ghelardoni S, Frascarelli S, Ronca-Testoni S, Zucchi R. S-nitrosothiol detection in isolated perfused rat heart. Mol Cell Biochem. 2003;252:347-357.
26. DeSantiago J, Maier LS, Bers DM. Frequency-dependent acceleration of relaxation in the heart depends on CaMKII, but not phospholamban. J Mol Cell Cardiol. 2002;34:975-984.
27. Champin HC, Georgakopoulos D, Takimoto E, Isoda T, Wang Y, Kass DA. Modulation of in vivo cardiac function by myocyte-specific nitric oxide synthase-3. Circ Res. 2004;94:657-663.
28. Feron O, Dessy C, Opel DJ, Arstall MA, Kelly RA, Michel T. Modulation of the endothelial nitric-oxide synthase-caveolin interaction in cardiac myocytes. Implications for the autonomic regulation of heart rate. J Biol Chem. 1998;273:30249-30254.
29. Hare JM, Lofthouse RA, Juang GJ, Colman L, Ricker KM, Kim B, Senzaki H, Cao S, Tunin RS, Kass DA. Contribution of caveolin protein abundance to augmented nitric oxide signaling in conscious dogs with pacing-induced heart failure. Circ Res. 2000;86:1085-1092.
30. Damy T, Ratajczak P, Robidel E, Bendall JK, Oliviéro P, Boczkowski J, Ebrahimian T, Marotte F, Samuel J, Heymes C. Up-regulation of cardiac nitric oxide synthase 1-derived nitric oxide after myocardial infarction in senescent rats. FASEB J. 2003;17:1934-1936.
31. Damy T, Ratajczak P, Shah AM, Camors E, Marty I, Hasenfuss G, Marotte F, Samuel J, Heymes C. Increased neuronal nitric oxide synthase-derived NO production in the failing human heart. Lancet. 2004;363:1365-1367.
32. Sears CE, Bryant SM, Ashley EA, Lygate CA, Rakovic S, Wallis HL, Neubauer S, Terrar DA, Casadei B. Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ Res. 2003;92:e52-e59.
33. 2+] in rat cardiac myocytes. Pflugers Arch. 2001;441:709-716.
34. Ziolo MT, Bers DM. The real estate of NOS signaling: location, location, location. Circ Res. 2003;92:1279-1281.