Hydrogen sulfide cytoprotective signaling is endothelial nitric oxide synthase-nitric oxide dependent

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 8, 2014, Pages 3182-3187

  King, Adrienne L ^a   Polhemus, David J ^b   Bhushan, Shashi ^b   Otsuka, Hiroyuki ^b   Kondo, Kazuhisa ^a   Nicholson, Chad K ^a   Bradley, Jessica M ^b   Islam, Kazi N ^b   Calvert, John W ^a   Tao, Ya Xiong ^c   Dugas, Tammy R ^d   Kelley, Eric E ^e   Elrod, John W ^f   Huang, Paul L ^g   Wang, Rui ^h   Lefer, David J ^b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AUBURN UNIVERSITY   (United States)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^f TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

^h LAKEHEAD UNIVERSITY   (Canada)

Author keywords

Cth; Cystathionase; eNOS uncoupling; Myocardial infarction; Nitrite

Indexed keywords

8 ISOPROSTANE; CYCLIC GMP; CYSTATHIONINE GAMMA LYASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN SULFIDE; NITRIC OXIDE; NITRITE; SODIUM SULFIDE; SULFIDE; TROPONIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CELL PROTECTION; CONTROLLED STUDY; GAS CHROMATOGRAPHY; GENE INACTIVATION; HEART INFARCTION; HEART MUSCLE ISCHEMIA; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; LIVER INJURY; LIVER ISCHEMIA; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY;

CTH; CYSTATHIONASE; ENOS UNCOUPLING; MYOCARDIAL INFARCTION; NITRITE;

ALANINE TRANSAMINASE; ANALYSIS OF VARIANCE; ANIMALS; ASPARTATE AMINOTRANSFERASES; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYSTATHIONINE GAMMA-LYASE; CYTOPROTECTION; HYDROGEN SULFIDE; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; OXYGEN CONSUMPTION; SIGNAL TRANSDUCTION; TROPONIN I;

EID: 84896861005     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321871111     Document Type: Article

References (49)

1. Zhao W, Zhang J, Lu Y, Wang R (2001) The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20(21):6008-6016. (Pubitemid 33049276)
2. Szabó C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6(11):917-935.
3. Wallace JL, Caliendo G, Santagada V, Cirino G (2010) Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346). Br J Pharmacol 159(6):1236-1246.
4. Wang R (2012) Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiol Rev 92(2):791-896.
5. Kondo K, et al. (2013) H2S protects against pressure overload-induced heart failure via up-regulation of endothelial nitric oxide synthase. Circulation 127(10):1116-1127.
6. Ali MY, et al. (2006) Regulation of vascular nitric oxide in vitro and in vivo: A new role for endogenous hydrogen sulphide? Br J Pharmacol 149(6):625-634. (Pubitemid 44748055)
7. Elrod JW, et al. (2007) Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104(39):15560-15565. (Pubitemid 47502956)
8. Predmore BL, et al. (2012) The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability. Am J Physiol Heart Circ Physiol 302(11):H2410-H2418.
9. Elrod JW, Calvert JW, Gundewar S, Bryan NS, Lefer DJ (2008) Nitric oxide promotes distant organ protection: Evidence for an endocrine role of nitric oxide. Proc Natl Acad Sci USA 105(32):11430-11435.
10. Jha S, Calvert JW, Duranski MR, Ramachandran A, Lefer DJ (2008) Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: Role of antioxidant and antiapoptotic signaling. Am J Physiol Heart Circ Physiol 295(2):H801-H806.
11. Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18(10):1165-1167. (Pubitemid 39561558)
12. Peake BF, et al. (2013) Hydrogen sulfide preconditions The db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner. Am J Physiol Heart Circ Physiol 304(9):H1215-H1224.
13. Calvert JW, et al. (2009) Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 105(4):365-374.
14. Calvert JW, et al. (2010) Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice. Circulation 122(1):11-19.
15. Lefer AM, Peck RC (1984) Cardioprotective effects of enalapril in acute myocardial ischemia. Pharmacology 29(2):61-69. (Pubitemid 14086074)
16. Fiorucci S, et al. (2005) Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 129(4):1210-1224. (Pubitemid 41446861)
17. Chan MV, Wallace JL (2013) Hydrogen sulfide-based therapeutics and gastrointestinal diseases: Translating physiology to treatments. Am J Physiol Gastrointest Liver Physiol 305(7):G467-G473.
18. Campolo M, et al. (2013) A hydrogen sulfide-releasing cyclooxygenase inhibitor markedly accelerates recovery from experimental spinal cord injury. FASEB J 27(11):4489-4499.
19. Coletta C, et al. (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci USA 109(23):9161-9166.
20. Altaany Z, Yang G, Wang R (2013) Crosstalk between hydrogen sulfide and nitric oxide in endothelial cells. J Cell Mol Med 17(7):879-888.
21. Zanardo RC, et al. (2006) Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20(12):2118-2120.
22. Paul BD, Snyder SH (2012) H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13(8):499-507.
23. Yang G, et al. (2008) H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine gamma-lyase. Science 322(5901):587-590.
24. Kovačić D, et al. (2012) Total plasma sulfide in congestive heart failure. J Card Fail 18(7):541-548.
25. Lin MI, et al. (2003) Phosphorylation of threonine 497 in endothelial nitric-oxide synthase coordinates the coupling of L-arginine metabolism to efficient nitric oxide production. J Biol Chem 278(45):44719-44726. (Pubitemid 37377229)
26. Boo YC, et al. (2002) Shear stress stimulates phosphorylation of endothelial nitricoxide synthase at Ser1179 by Akt-independent mechanisms: Role of protein kinase A. J Biol Chem 277(5):3388-3396. (Pubitemid 34953207)
27. Mount PF, Kemp BE, Power DA (2007) Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 42(2):271-279. (Pubitemid 46135596)
28. Bucci M, et al. (2012) cGMP-dependent protein kinase contributes to hydrogen sulfide-stimulated vasorelaxation. PLoS ONE 7(12):e53319.
29. Polhemus DJ, et al. (2013) Hydrogen sulfide attenuates cardiac dysfunction after heart failure via induction of angiogenesis. Circ Heart Fail 6(5):1077-1086.
30. Dimmeler S, et al. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399(6736):601-605.
31. Gao F, et al. (2002) Nitric oxide mediates the antiapoptotic effect of insulin in myocardial ischemia-reperfusion: The roles of PI3-kinase, Akt, and endothelial nitric oxide synthase phosphorylation. Circulation 105(12):1497-1502. (Pubitemid 34263284)
32. Hafezi-Moghadam A, et al. (2002) Acute cardiovascular protective effects of corticosteroids are mediated by non-transcriptional activation of endothelial nitric oxide synthase. Nat Med 8(5):473-479. (Pubitemid 34546749)
33. Bell RM, Yellon DM (2003) Bradykinin limits infarction when administered as an adjunct to reperfusion in mouse heart: The role of PI3K, Akt and eNOS. J Mol Cell Cardiol 35(2):185-193. (Pubitemid 36269192)
34. Alp NJ, Channon KM (2004) Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 24(3):413-420. (Pubitemid 38326132)
35. Silberman GA, et al. (2010) Uncoupled cardiac nitric oxide synthase mediates diastolic dysfunction. Circulation 121(4):519-528.
36. Takimoto E, et al. (2005) Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 115(5):1221-1231. (Pubitemid 40629040)
37. Landmesser U, et al. (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111(8):1201-1209. (Pubitemid 36519937)
38. Sarti P, Arese M, Forte E, Giuffrè A, Mastronicola D (2012) Mitochondria and nitric oxide: Chemistry and pathophysiology. Adv Exp Med Biol 942:75-92.
39. + signaling pathway, and the transduction of nitrosative to oxidative cell signals: An alternative function for cytochrome C oxidase. Free Radic Biol Med 32(4):370-374.
40. Shiva S, Brookes PS, Patel RP, Anderson PG, Darley-Usmar VM (2001) Nitric oxide partitioning into mitochondrial membranes and the control of respiration at cytochrome c oxidase. Proc Natl Acad Sci USA 98(13):7212-7217. (Pubitemid 32567928)
41. Yin MC, Hwang SW, Chan KC (2002) Nonenzymatic antioxidant activity of four organosulfur compounds derived from garlic. J Agric Food Chem 50(21):6143- 6147.
42. Grudzinski IP, Frankiewicz-Jozko A, Bany J (2001) Diallyl sulfide - a flavour component from garlic (Allium sativum) attenuates lipid peroxidation in mice infected with Trichinella spiralis. Phytomedicine 8(3):174-177. (Pubitemid 32506290)
43. Atochin D, et al. (2007) The phosphorylation state of eNOS modulates vascular reactivity and outcome of cerebral ischemia in vivo. The Journal of Clinical Investigation 117(7):1961-1967. (Pubitemid 47036330)
44. Committee on Care and Use of Laboratory Animals (1985) Guide for the Care and Use of Laboratory Animals (Natl Inst Health, Bethesda), DHHS Publ No (NIH) 85-23.
45. Elrod JW, et al. (2006) Cardiomyocyte-specific overexpression of NO synthase-3 protects against myocardial ischemia-reperfusion injury. Arterioscler Thromb Vasc Biol 26(7):1517-1523. (Pubitemid 44288977)
46. Duranski MR, et al. (2006) Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 291(6):H2980-H2986. (Pubitemid 44904099)
47. Stokes KY, et al. (2009) Dietary nitrite prevents hypercholesterolemic microvascular inflammation and reverses endothelial dysfunction. Am J Physiol Heart Circ Physiol 296(5):H1281-H1288.
48. Islam KN, et al. (1997) TGF-beta1 triggers oxidative modifications and enhances apoptosis in HIT cells through accumulation of reactive oxygen species by suppression of catalase and glutathione peroxidase. Free Radic Biol Med 22(6):1007-1017. (Pubitemid 27084138)
49. Khoo NK, et al. (2012) Obesity-induced tissue free radical generation: An in vivo immuno-spin trapping study. Free Radic Biol Med 52(11-12):2312-2319.