Increased endogenous H2S generation by CBS, CSE, and 3MST gene therapy improves ex vivo renovascular relaxation in hyperhomocysteinemia

American Journal of Physiology - Cell Physiology

Volumn 303, Issue 1, 2012, Pages

  Sen, Utpal ^a   Sathnur, Pushpakumar B ^a   Kundu, Sourav ^a   Givvimani, Srikanth ^a   Coley, Denise M ^a   Mishra, Paras K ^a   Qipshidze, Natia ^a   Tyagi, Neetu ^a   Metreveli, Naira ^a   Tyagi, Suresh C ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

3 mercaptopyruvate sulfurtransferase; Cystathionine synthase; Cystathionine lyase; Hydrogen sulfide; Mitophagy

Indexed keywords

3 MERCAPTOPYRUVATE SULFURTRANSFERASE; CD31 ANTIGEN; COLLAGENASE 3; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; ENDOSTATIN; HOMOCYSTEINE; HYDROGEN SULFIDE; PROTEIN KINASE B; SULFURTRANSFERASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; VASCULOTROPIN; 3 MERCAPTOPYRUVATE SULPHURTRANSFERASE; 3-MERCAPTOPYRUVATE SULPHURTRANSFERASE; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; EX VIVO STUDY; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; HYPERHOMOCYSTEINEMIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KIDNEY BLOOD FLOW; KIDNEY BLOOD VESSEL; MITOPHAGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RENAL ARTERY; RISK FACTOR; TISSUE CULTURE; VASCULAR DISEASE; VASODILATATION; ANIMAL; BIOSYNTHESIS; BLOOD VESSEL INJURY; C57BL MOUSE; GENETICS; METABOLISM; ORGAN CULTURE TECHNIQUE; RENOVASCULAR HYPERTENSION;

ANIMALS; ANTIGENS, CD31; CELLS, CULTURED; CYSTATHIONINE BETA-SYNTHASE; CYSTATHIONINE GAMMA-LYASE; ENDOSTATINS; FORKHEAD TRANSCRIPTION FACTORS; GENE THERAPY; HOMOCYSTEINE; HYDROGEN SULFIDE; HYPERHOMOCYSTEINEMIA; HYPERTENSION, RENOVASCULAR; MATRIX METALLOPROTEINASE 13; MICE; MICE, INBRED C57BL; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RENAL ARTERY; SULFURTRANSFERASES; TISSUE INHIBITOR OF METALLOPROTEINASE-1; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR SYSTEM INJURIES;

EID: 84863528233     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00398.2011     Document Type: Article

References (61)

1. Ahmed AK, Haylor JL, El Nahas AM, Johnson TS. Localization of matrix metalloproteinases and their inhibitors in experimental progressive kidney scarring. Kidney Int 71: 755-763, 2007.
2. Beard RS Jr, Bearden SE. Vascular complications of cystathionine β-synthase deficiency: future directions for homocysteine-to-hydrogen sulfide research. Am J Physiol Heart Circ Physiol 300: H13-H26, 2011.
3. Border WA, Noble NA. TGF-beta in kidney fibrosis: a target for gene therapy. Kidney Int 51: 1388-1396, 1997.
4. Chambers JC, McGregor A, Jean-Marie J, Obeid OA, Kooner JS. Demonstration of rapid onset vascular endothelial dysfunction after hyperhomocysteinemia: an effect reversible with vitamin C therapy. Circulation 99: 1156-1160, 1999.
5. Chang L, Geng B, Yu F, Zhao J, Jiang H, Du J, Tang C. Hydrogen sulfide inhibits myocardial injury induced by homocysteine in rats. Amino Acids 34: 573-585, 2008.
6. Chang PY, Lu SC, Lee CM, Chen YJ, Dugan TA, Huang WH, Chang SF, Liao WS, Chen CH, Lee YT. Homocysteine inhibits arterial endothelial cell growth through transcriptional downregulation of fibroblast growth factor-2 involving G protein and DNA methylation. Circ Res 102: 933-941, 2008.
7. Chen C, Halkos ME, Surowiec SM, Conklin BS, Lin PH, Lumsden AB. Effects of homocysteine on smooth muscle cell proliferation in both cell culture and artery perfusion culture models. J Surg Res 88: 26-33, 2000.
8. Chen H, Chan DC. Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum Mol Genet 18: R169-176, 2009.
9. Chiku T, Padovani D, Zhu W, Singh S, Vitvitsky V, Banerjee R. H2S biogenesis by human cystathionine gamma-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J Biol Chem 284: 11601-11612, 2009.
10. Csordas A, Kreutmayer S, Ploner C, Braun PR, Karlas A, Backovic A, Wick G, Bernhard D. Cigarette smoke extract induces prolonged endoplasmic reticulum stress and autophagic cell death in human umbilical vein endothelial cells. Cardiovasc Res 92: 141-148, 2011.
11. Dawson TL, Gores GJ, Nieminen AL, Herman B, Lemasters JJ. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am J Physiol Cell Physiol 264: C961-C967, 1993.
12. Degtyarev M, De Maziere A, Orr C, Lin J, Lee BB, Tien JY, Prior WW, van Dijk S, Wu H, Gray DC, Davis DP, Stern HM, Murray LJ, Hoeflich KP, Klumperman J, Friedman LS, Lin K. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 183: 101-116, 2008.
13. Demuth K, Drunat S, Girerd X, Moatti N, Paul JL, Safar M, Boutouyrie P. Homocysteine is the only plasma thiol associated with carotid artery remodeling. Atherosclerosis 165: 167-174, 2002.
14. Distrutti E, Mencarelli A, Santucci L, Renga B, Orlandi S, Donini A, Shah V, Fiorucci S. The methionine connection: homocysteine and hydrogen sulfide exert opposite effects on hepatic microcirculation in rats. Hepatology 47: 659-667, 2008.
15. Edirimanne VE, Woo CW, Siow YL, Pierce GN, Xie JYOK. Homocysteine stimulates NADPH oxidase-mediated superoxide production leading to endothelial dysfunction in rats. Can J Physiol Pharmacol 85: 1236-1247, 2007.
16. Faraci FM, Lentz SR. Hyperhomocysteinemia, oxidative stress, and cerebral vascular dysfunction. Stroke 35: 345-347, 2004.
17. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 9: 669-676, 2003.
18. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. PI3K/Akt and apoptosis: size matters. Oncogene 22: 8983-8998, 2003.
19. Givvimani S, Munjal C, Gargoum R, Sen U, Tyagi N, Vacek JC, Tyagi SC. Hydrogen sulfide mitigates transition from compensatory hypertrophy to heart failure. J Appl Physiol 110: 1093-1100, 2011.
20. Hajitou A, Grignet-Debrus C, Devy L, Berndt S, Blacher S, Deroanne CF, Bajou K, Fong T, Chiang YW, Foidart JM, Noel A. The antitumoral effect of endostatin and angiostatin is associated with a downregulation of vascular endothelial growth factor expression in tumor cells. FASEB J 16: 1802-+, 2002.
21. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 18: 1926-1945, 2004.
22. Ishii I, Akahoshi N, Yu XN, Kobayashi Y, Namekata K, Komaki G, Kimura H. Murine cystathionine gamma-lyase: complete cDNA and genomic sequences, promoter activity, tissue distribution and developmental expression. Biochem J 381: 113-123, 2004.
23. Jakubowski H. Protein homocysteinylation: possible mechanism underlying pathological consequences of elevated homocysteine levels. FASEB J 13: 2277-2283, 1999.
24. Joseph J, Kennedy RH, Devi S, Wang J, Joseph L, Hauer-Jensen M. Protective role of mast cells in homocysteine-induced cardiac remodeling. Am J Physiol Heart Circ Physiol 288: H2541-H2545, 2005.
25. Kato M, Yuan H, Xu ZG, Lanting L, Li SL, Wang M, Hu MC, Reddy MA, Natarajan R. Role of the Akt/FoxO3a pathway in TGF-beta1-mediated mesangial cell dysfunction: a novel mechanism related to diabetic kidney disease. J Am Soc Nephrol 17: 3325-3335, 2006.
26. Kim I, Rodriguez-Enriquez S, Lemasters JJ. Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462: 245-253, 2007.
27. Kimura H. Hydrogen sulfide: its production, release and functions. Amino Acids 41: 113-121, 2011.
28. Lan A, Liao X, Mo L, Yang C, Yang Z, Wang X, Hu F, Chen P, Feng J, Zheng D, Xiao L. Hydrogen sulfide protects against chemical hypoxiainduced injury by inhibiting ROS-activated ERK1/2 and p38MAPK signaling pathways in PC12 cells. PLos One 6: e25921, 2011.
29. Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441: 523-540, 2012.
30. Lenz O, Elliot SJ, Stetler-Stevenson WG. Matrix metalloproteinases in renal development and disease. J Am Soc Nephrol 11: 574-581, 2000.
31. Loscalzo J. Homocysteine-mediated thrombosis and angiostasis in vascular pathobiology. J Clin Invest 119: 3203-3205, 2009.
32. Mustafa AK, Sikka G, Gazi SK, Steppan J, Jung SM, Bhunia AK, Barodka VM, Gazi FK, Barrow RK, Wang R, Amzel LM, Berkowitz DE, Snyder SH. Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 109: 1259-1268, 2011.
33. Nagai Y, Tsugane M, Oka J, Kimura H. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18: 557-559, 2004.
34. Outinen PA, Sood SK, Pfeifer SI, Pamidi S, Podor TJ, Li J, Weitz JI, Austin RC. Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells. Blood 94: 959-967, 1999.
35. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, Jeschke MG, Branski LK, Herndon DN, Wang R, Szabo C. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci USA 106: 21972-21977, 2009.
36. Sen U, Basu P, Abe OA, Givvimani S, Tyagi N, Metreveli N, Shah KS, Passmore JC, Tyagi SC. Hydrogen sulfide ameliorates hyperhomocysteinemia-associated chronic renal failure. Am J Physiol Renal Physiol 297: F410-F419, 2009.
37. Sen U, Givvimani S, Abe OA, Lederer ED, Tyagi SC. Cystathionine beta-synthase and cystathionine gamma-lyase double gene transfer ameliorate homocysteine-mediated mesangial inflammation through hydrogen sulfide generation. Am J Physiol Cell Physiol 300: C155-C163, 2011.
38. Sen U, Mishra PK, Tyagi N, Tyagi SC. Homocysteine to hydrogen sulfide or hypertension. Cell Biochem Biophys 57: 49-58, 2010.
39. Sen U, Munjal C, Qipshidze N, Abe O, Gargoum R, Tyagi SC. Hydrogen sulfide regulates homocysteine-mediated glomerulosclerosis. Am J Nephrol 31: 442-455, 2010.
40. Sen U, Rodriguez WE, Tyagi N, Kumar M, Kundu S, Tyagi SC. Ciglitazone, a PPARγ agonist, ameliorates diabetic nephropathy in part through homocysteine clearance. Am J Physiol Endocrinol Metab 295: E1205-E1212, 2008.
41. Sen U, Vacek TP, Hughes WM, Kumar M, Moshal KS, Tyagi N, Metreveli N, Hayden MR, Tyagi SC. Cardioprotective role of sodium thiosulfate on chronic heart failure by modulating endogenous H2S generation. Pharmacology 82: 201-213, 2008.
42. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem 284: 28319-28331, 2009.
43. Sharma R, Suzuki K, Nagase H, Savin VJ. Matrix metalloproteinase (stromelysin-1) increases the albumin permeability of isolated rat glomeruli. J Lab Clin Med 128: 297-303, 1996.
44. Shibuya N, Mikami Y, Kimura Y, Nagahara N, Kimura H. Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J Biochem 146: 623-626, 2009.
45. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11: 703-714, 2009.
46. Stabler SP, Steegborn C, Wahl MC, Oliveriusova J, Kraus JP, Allen RH, Wagner C, Mudd SH. Elevated plasma total homocysteine in severe methionine adenosyltransferase I/III deficiency. Metabolism 51: 981-988, 2002.
47. Stroylova YY, Zimny J, Yousefi R, Chobert JM, Jakubowski H, Muronetz VI, Haertle T. Aggregation and structural changes of alpha(S1)-, beta-and kappa-caseins induced by homocysteinylation. Biochim Biophys Acta 1814: 1234-1245, 2011.
48. Szabo C, Papapetropoulos A. Hydrogen sulphide and angiogenesis: mechanisms and applications. Br J Pharmacol 164: 853-865, 2011.
49. Tanaka M, Takayama A, Ito E, Sunami H, Yamamoto S, Shimomura M. Effect of pore size of self-organized honeycomb-patterned polymer films on spreading, focal adhesion, proliferation, and function of endothelial cells. J Nanosci Nanotechnol 7: 763-772, 2007.
50. Tang XQ, Shen XT, Huang YE, Chen RQ, Ren YK, Fang HR, Zhuang YY, Wang CY. Inhibition of endogenous hydrogen sulfide generation is associated with homocysteine-induced neurotoxicity: role of ERK1/2 activation. J Mol Neurosci 45: 60-67, 2011.
51. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106: 2781-2786, 2002.
52. Torres L, Garcia-Trevijano ER, Rodriguez JA, Carretero MV, Bustos M, Fernandez E, Eguinoa E, Mato JM, Avila MA. Induction of TIMP-1 expression in rat hepatic stellate cells and hepatocytes: a new role for homocysteine in liver fibrosis. Biochim Biophys Acta 1455: 12-22, 1999.
53. Tummalapalli CM, Tyagi SC. Responses of vascular smooth muscle cell to extracellular matrix degradation. J Cell Biochem 75: 515-527, 1999.
54. Tyagi N, Qipshidze N, Sen U, Rodriguez W, Ovechkin A, Tyagi SC. Cystathionine beta synthase gene dose dependent vascular remodeling in murine model of hyperhomocysteinemia. Int J Physiol Pathophysiol Pharmacol 3: 210-222, 2011.
55. Tyagi N, Vacek JC, Givvimani S, Sen U, Tyagi SC. Cardiac specific deletion of N-methyl-D-aspartate receptor 1 ameliorates mtMMP-9 mediated autophagy/mitophagy in hyperhomocysteinemia. J Recept Signal Transduct Res 30: 78-87, 2010.
56. Wallner EI, Yang Q, Peterson DR, Wada J, Kanwar YS. Relevance of extracellular matrix, its receptors, and cell adhesion molecules in mammalian nephrogenesis. Am J Physiol Renal Physiol 275: F467-F477, 1998.
57. Weiss N, Heydrick S, Zhang YY, Bierl C, Cap A, Loscalzo J. Cellular redox state and endothelial dysfunction in mildly hyperhomocysteinemic cystathionine beta-synthase-deficient mice. Arterioscler Thromb Vasc Biol 22: 34-41, 2002.
58. Xu P, Das M, Reilly J, Davis RJ. JNK regulates FoxO-dependent autophagy in neurons. Genes Dev 25: 310-322, 2011.
59. Yang ZZ, Zou AP. Homocysteine enhances TIMP-1 expression and cell proliferation associated with NADH oxidase in rat mesangial cells. Kidney Int 63: 1012-1020, 2003.
60. Yi F, Xia M, Li N, Zhang C, Tang L, Li PL. Contribution of guanine nucleotide exchange factor Vav2 to hyperhomocysteinemic glomerulosclerosis in rats. Hypertension 53: 90-96, 2009.
61. Zent R, Pozzi A. Antiangiogenic therapy in diabetic nephropathy. J Am Soc Nephrol 17: 325-327, 2006.