Regulation of vascular tone, angiogenesis and cellular bioenergetics by the 3-mercaptopyruvate sulfurtransferase/H2S pathway: Functional impairment by hyperglycemia and restoration by dl-α-lipoic acid

Molecular Medicine

Volumn 21, Issue , 2015, Pages 1-14

  Coletta, Ciro ^a   Módis, Katalin ^a,c   Szczesny, Bartosz ^a   Brunyánszki, Attila ^a   Oláh, Gábor ^a   Rios, Ester C S ^a   Yanagi, Kazunori ^a   Ahmad, Akbar ^a   Papapetropoulos, Andreas ^b   Szabo, Csaba ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF ATHENS   (Greece)

^c LAKEHEAD UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 MERCAPTOPYRUVIC ACID; 3 MERCAPTOPYRUVIC ACID SULFURTRANSFERASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYTOCHROME C OXIDASE; DIHYDROLIPOATE; GLUCOSE; HYDROGEN SULFIDE; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SULFURTRANSFERASE; THIOCTIC ACID; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; 3-MERCAPTOPYRUVATE SULPHURTRANSFERASE; 3-MERCAPTOPYRUVIC ACID; CYSTEINE; VASODILATOR AGENT;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTERIAL PRESSURE; ARTICLE; BIOENERGY; BLOOD LEVEL; BLOOD VESSEL TONE; CAPILLARY ENDOTHELIAL CELL; CELL FREE SYSTEM; CONCENTRATION RESPONSE; DIABETIC ANGIOPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRIAL DYNAMICS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; SKIN BLOOD FLOW; SKIN CAPILLARY; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; VASODILATATION; WOUND HEALING; WOUND HEALING IMPAIRMENT; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CELL LINE; DIABETES MELLITUS; DISEASE MODEL; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; CELL LINE; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYSTEINE; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENERGY METABOLISM; HYDROGEN SULFIDE; HYPERGLYCEMIA; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE; MITOCHONDRIA; NEOVASCULARIZATION, PHYSIOLOGIC; OXYGEN CONSUMPTION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SULFURTRANSFERASES; THIOCTIC ACID; VASODILATOR AGENTS;

EID: 84930637752     PISSN: 10761551     EISSN: 15283658     Source Type: Journal    
DOI: 10.2119/molmed.2015.00035     Document Type: Article

References (70)

1. Fiorucci S, Distrutti E, Cirino G, Wallace JL. (2006) The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology. 131:259–71
2. Szabo C. (2007) Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 6:917–35
3. Whiteman M, Winyard PG. (2011) Hydrogen sulfide and inflammation: the good, the bad, the ugly and the promising. Expert Rev. Clin. Pharmacol. 4:13–32
4. Bucci M, Cirino G. (2011) Hydrogen sulphide in heart and systemic circulation. Inflamm. Allergy Drug Targets. 10:103–8
5. Wang R. (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol. Rev. 92:791–896
6. Módis K, Wolanska K, Vozdek R. (2013) H2S in cell signaling, signal transduction, cellular bioenergetics and physiology in C. Elegans. Gen. Physiol. Biophys. 32:1–22
7. Polhemus DJ, Lefer DJ. (2014) Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease. Circ. Res. 114:730–7
8. Jain SK, et al. (2010) Low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocin-treated rats causes vascular inflammation? Antioxid. Redox. Signal. 12:1333–7
9. Whiteman M, et al. (2010) Adiposity is a major determinant of plasma levels of the novel vasodilator hydrogen sulphide. Diabetologia. 53:1722–6
10. Suzuki K, et al. (2011) Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc. Natl. Acad. Sci. U. S. A. 108:13829–34
11. Ahmad FU, et al. (2012) Exogenous hydrogen sulfide (H2S) reduces blood pressure and prevents the progression of diabetic nephropathy in spontaneously hypertensive rats. Ren. Fail. 34:203–10
12. Xue H, et al. (2013) H2S inhibits hyperglycemiainduced intrarenal renin-angiotensin system activation via attenuation of reactive oxygen species generation. PLoS One. 8:e74366
13. Manna P, Jain SK. (2013) L-cysteine and hydrogen sulfide increase PIP3 and AMPK/PPARγ expression and decrease ROS and vascular inflammation markers in high glucose treated human U937 monocytes. J. Cell. Biochem. 114:2334–45
14. Si YF, et al. (2013) Treatment with hydrogen sulfide alleviates streptozotocin-induced diabetic retinopathy in rats. Br. J. Pharmacol. 169:619–31
15. Yamamoto J, et al. (2013) Distribution of hydrogen sulfide (H2S)-producing enzymes and the roles of the H2S donor sodium hydrosulfide in diabetic nephropathy. Clin. Exp. Nephrol. 17:32–40
16. Wei WB, Hu X, Zhuang XD, Liao LZ, Li WD. (2014) GYY4137, a novel hydrogen sulfide-releasing molecule, likely protects against high glucose-induced cytotoxicity by activation of the AMPK/mTOR signal pathway in H9c2 cells. Mol. Cell. Biochem. 389:249–56
17. Shibuya N, Mikami Y, Kimura Y, Nagahara N, Kimura H. (2009) Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J. Biochem. 146:623–6
18. Sen U, et al. (2012) Increased endogenous H2S generation by CBS, CSE, and 3MST gene therapy improves ex vivo renovascular relaxation in hyperhomocysteinemia. Am. J. Physiol. Cell Physiol. 303:C41–51
19. Madden JA, Ahlf SB, Dantuma MW, Olson KR, Roerig DL. (2012) Precursors and inhibitors of hydrogen sulfide synthesis affect acute hypoxic pulmonary vasoconstriction in the intact lung. J. Appl. Physiol. (1985). 112:411–8
20. Módis K, Asimakopoulou A, Coletta C, Papapetropoulos A, Szabo C. (2013) Oxidative stress suppresses the cellular bioenergetic effect of the 3-mercaptopyruvate sulfurtransferase/hydrogen sulfide pathway. Biochem. Biophys. Res. Commun. 433:401–7
21. Módis K, et al. (2014) Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part II. Pathophysiological and therapeutic aspects. Br. J. Pharmacol. 171:2123–46
22. Hosoki R, Matsuki N, Kimura H. (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem. Biophys. Res. Commun. 237:527–31
23. Zhao W, Wang R. (2002) H2S-induced vasorelaxation and underlying cellular and molecular mechanisms. Am. J. Physiol. Heart Circ. Physiol. 283:H474–80
24. Bucci M, et al. (2010) Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler. Thromb. Vasc. Biol. 30:1998–2004
25. d’Emmanuele di Villa Bianca R, et al. (2011) Hydrogen sulfide-induced dual vascular effect involves arachidonic acid cascade in rat mesenteric arterial bed. J. Pharmacol. Exp. Ther. 337:59–64
26. Mustafa AK, et al. (2011) Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 109:1259–68
27. 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. U. S. A. 109:9161–6
28. Bucci M, et al. (2012) cGMP-dependent protein kinase contributes to hydrogen sulfide-stimulated vasorelaxation. PLoS One.7:e53319
29. Bełtowski J, Jamroz-Wiśniewska A. (2014) Hydrogen sulfide and endothelium-dependent vasorelaxation. Molecules 19:21183–99
30. Cai WJ, et al. (2007) The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc. Res. 76:29–40
31. Papapetropoulos A, et al. (2009) Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 106:21972–7
32. Wang MJ, et al. (2010) The hydrogen sulfide donor NaHS promotes angiogenesis in a rat model of hind limb ischemia. Antioxid. Redox. Signal. 12:1065–77
33. Szabo C, Papapetropoulos A. (2011) Hydrogen sulphide and angiogenesis: mechanisms and applications. Br. J. Pharmacol. 164:853–65
34. Polhemus DJ, et al. (2013) Hydrogen sulfide attenuates cardiac dysfunction after heart failure via induction of angiogenesis. Circ. Heart Fail. 6:1077–86
35. Szabo C, et al. (2013) Tumor-derived hydrogen sulfide, produced by cystathionine-β-synthase, stimulates bioenergetics, cell proliferation, and angiogenesis in colon cancer. Proc. Natl. Acad. Sci. U. S. A. 110:12474–9
36. Liu F, et al. (2014) Hydrogen sulfide improves wound healing via restoration of endothelial progenitor cell functions and activation of angiopoietin- 1 in type 2 diabetes. Diabetes. 63:1763–78
37. Goubern M, Andriamihaja M, Nübel T, Blachier F, Bouillaud F. (2007) Sulfide, the first inorganic substrate for human cells. FASEB J. 21:1699–706
38. Módis K, Coletta C, Erdélyi K, Papapetropoulos A, Szabo C. (2013) Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J. 27:601–11
39. Módis K, Panopoulos P, Coletta C, Papapetropoulos A, Szabo C. (2013) Hydrogen sulfide-mediated stimulation of mitochondrial electron transport involves inhibition of the mitochondrial phosphodiesterase 2A, elevation of cAMP and activation of protein kinase A. Biochem. Pharmacol. 86:1311–9
40. Szczesny B, et al. (2014) AP39, a novel mitochondria- targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cytoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide.41:120–30
41. Helmy N, et al. (2014) Oxidation of hydrogen sulfide by human liver mitochondria. Nitric Oxide. 41:105–12
42. Szabo C, et al. (2014) Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part I. Biochemical and physiological mechanisms. Br. J. Pharmacol. 171:2099–122
43. Mikami Y, et al. (2011) Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem. J. 439:479–85
44. Cameron NE, Jack AM, Cotter MA. (2001) Effect of alpha-lipoic acid on vascular responses and nociception in diabetic rats. Free Radic. Biol. Med. 31:125–35
45. Nebbioso M, Pranno F, Pescosolido N. (2013) Lipoic acid in animal models and clinical use in diabetic retinopathy. Expert Opin. Pharmacother. 14:1829–38
46. Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Institute for Laboratory Animal Research, Division on Earth and Life Studies, National Research Council of the National Academies. (2011) Guide for the Care and Use of Laboratory Animals. 8th edition. Washington (DC): National Academies Press.
47. Warner TD. (1990) Simultaneous perfusion of rat isolated superior mesenteric arterial and venous beds: comparison of their vasoconstrictor and vasodilator responses to agonists. Br. J. Pharmacol. 99:427–33
48. Ferreira FM, Palmeira CM, Seiça R, Moreno AJ, Santos MS. (2003) Diabetes and mitochondrial bioenergetics: alterations with age. J. Biochem. Mol. Toxicol. 17:214–22
49. Szabo C. (2009) Role of nitrosative stress in the pathogenesis of diabetic vascular dysfunction. Br. J. Pharmacol. 156:713–27
50. Sivitz WI, Yorek MA. (2010) Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid. Redox. Signal. 12:537–77
51. Giacco F, Brownlee M. (2010) Oxidative stress and diabetic complications. Circ. Res. 107:1058–70
52. Papanas N, Ziegler D. (2014) Efficacy of α-lipoic acid in diabetic neuropathy. Expert Opin. Pharmacother. 15:2721–31
53. Nebbioso M, Pranno F, Pescosolido N. (2013) Lipoic acid in animal models and clinical use in diabetic retinopathy. Expert Opin. Pharmacother. 14:1829–38
54. Kiguchi S. (1983) Metabolism of 3-mercaptopyruvate in rat tissues. Acta Med. Okayama. 37:85–91
55. Shibuya N, et al. (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox. Signal. 11:703–14
56. Nagahara N, Katayama A. (2005) Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteine-sulfenate in the maintenance of redox homeostasis. J. Biol. Chem. 280:34569–76
57. Miyamoto R, Otsuguro K, Yamaguchi S, Ito S. (2014) Contribution of cysteine aminotransferase and mercaptopyruvate sulfurtransferase to hydrogen sulfide production in peripheral neurons. J. Neurochem. 130:29–40
58. Nagahara N, Nirasawa T, Yoshii T, Niimura Y. (2012) Is novel signal transducer sulfur oxide involved in the redox cycle of persulfide at the catalytic site cysteine in a stable reaction intermediate of mercaptopyruvate sulfurtransferase? Antioxid. Redox. Signal. 16:747–53
59. Nagahara N. (2013) Regulation of mercaptopyruvate sulfurtransferase activity via intrasubunit and intersubunit redox-sensing switches. Antioxid. Redox. Signal. 19:1792–802
60. Yadav PK, Yamada K, Chiku T, Koutmos M, Banerjee R. (2013) Structure and kinetic analysis of H2S production by human mercaptopyruvate sulfurtransferase. J. Biol. Chem. 288:20002–13
61. Flannigan KL, Ferraz JG, Wang R, Wallace JL. (2013) Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: a site-specific, pro-resolution mechanism. PLoS One. 8:e71962
62. Nie LH, et al. (2013) Effects of intrauterine cigarette smoking exposure on expression of 3-mercaptopyruvate sulfurtransferase in medulla oblongata of neonatal rats [in Chinese]. Sichuan Da Xue Xue Bao Yi Xue Ban. 44:526–30
63. Li M, et al. (2013) Chronic intermittent hypoxia promotes expression of 3-mercaptopyruvate sulfurtransferase in adult rat medulla oblongata. Auton. Neurosci. 179:84–9
64. Zhao H, Chan SJ, Ng YK, Wong PT. (2013) Brain 3-mercaptopyruvate sulfurtransferase (3MST): cellular localization and downregulation after acute stroke. PLoS One. 8:e67322
65. Nagahara N, et al. (2013) Antioxidant enzyme, 3-mercaptopyruvate sulfurtransferase-knockout mice exhibit increased anxiety-like behaviors: a model for human mercaptolactate-cysteine disulfiduria. Sci. Rep. 3:1986
66. Yusuf M, et al. (2005) Streptozotocin-induced diabetes in the rat is associated with enhanced tissue hydrogen sulfide biosynthesis. Biochem. Biophys. Res. Commun. 333:1146–52
67. Szabo C. (2012) Roles of hydrogen sulfide in the pathogenesis of diabetes mellitus and its complications. Antioxid. Redox. Signal. 17:68–80
68. Langouche L, Mesotten D, Vanhorebeek I. (2010) Endocrine and metabolic disturbances in critical illness: relation to mechanisms of organ dysfunction and adverse outcome. Verh. K. Acad Geneeskd. Belg. 72:149–63
69. Rizk M, Witte M, Barbul A. (2004) Nitric oxide and wound healing. World J. Surg. 28:301–6
70. Buganza Tepole A, Kuhl E. (2013) Systems-based approaches toward wound healing. Pediatr Res. 73:553–63.