The hydrogen sulfide donor NaHS promotes angiogenesis in a rat model of hind limb ischemia

Antioxidants and Redox Signaling

Volumn 12, Issue 9, 2010, Pages 1065-1077

  Wang, Ming Jie ^a   Cai, Wen Jie ^b   Li, Na ^a   Ding, Ying Jiong ^a   Chen, Ying ^a   Zhu, Yi Chun ^a  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF SHANGHAI FOR SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; HYDROGEN SULFIDE; PROTEIN KINASE B; SODIUM HYDROSULFIDE; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; CAPILLARY DENSITY; CELL INFILTRATION; CELL INTERACTION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMORAL ARTERY; HINDLIMB ISCHEMIA; INFLAMMATORY CELL; LIMB ISCHEMIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SKELETAL MUSCLE; TISSUE BLOOD FLOW; VASCULAR ENDOTHELIUM;

ANIMALS; CELL COMMUNICATION; ENDOTHELIAL CELLS; EXTREMITIES; HEMODYNAMICS; HYDROGEN SULFIDE; ISCHEMIA; MALE; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SULFIDES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

RATTUS;

EID: 77950796610     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2009.2945     Document Type: Article

References (42)

1. Ali MY, Ping CY, Mok YY, Ling L, Whiteman M, Bhatia M, and Moore PK. Regulation of vascular nitric oxide in vitro and in vivo; A new role for endogenous hydrogen sulphide? Br J Pharmacol 149: 625-634, 2006.
2. Cai WJ, Wang MJ, Moore PK, Jin HM, Yao T, and Zhu YC. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res 76: 29-40, 2007.
3. Carmeliet P. Angiogenesis in health and disease. Nat Med 9: 653-660, 2003.
4. Chang DS, Su H, Tang GL, Brevetti LS, Sarkar R, Wang R, Kan YW, and Messina LM. Adeno-associated viral vectormediated gene transfer of VEGF normalizes skeletal muscle oxygen tension and induces arteriogenesis in ischemic rat hind limb. Mol Ther 7: 44-51, 2003.
5. Dallabrida SM, Ismail N, Oberle JR, Himes BE, and Rupnick MA. Angiopoietin-1 promotes cardiac and skeletal myocyte survival through integrins. Circ Res 96: e8-24, 2005.
6. Dombkowski RA, Russell MJ, and Olson KR. Hydrogen sulfide as an endogenous regulator of vascular smooth muscle tone in trout.AmJPhysiolRegul IntegrCompPhysiol 286: R678-685, 2004.
7. Duan J, Murohara T, Ikeda H, Sasaki K-I, Shintani S, Akita T, Shimada T, and Imaizumi T. Hyperhomocysteinemia impairs angiogenesis in response to hind limb ischemia. Arterioscler Thromb Vasc Biol 20: 2579-2585, 2000.
8. Engelmann GL. Coordinate gene expression during neonatal rat heart development. A possible role for the myocyte in extracellular matrix biogenesis and capillary angiogenesis. Cardiovasc Res 27: 1598-1605, 1993.
9. Erickson PF, Maxwell IH, Su LJ, Baumann M, and Glode LM. Sequence of cDNA for rat cystathionine gamma-lyase and comparison of deduced amino acid sequence with related Escherichia coli enzymes. Biochem J 269: 335-340, 1990.
10. Ferrara N, Gerber HP, and LeCouter J. The biology of VEGF and its receptors. Nat Med 9: 669-676, 2003.
11. Hoefer IE. Something is rotten in the state of angiogenesis- H2S as gaseous stimulator of angiogenesis. Cardiovasc Res 76: 1-2, 2007.
12. Hosoki R, Matsuki N, and Kimura H. The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237: 527-531, 1997.
13. Jacobi J, Tam BYY, Wu G, Hoffman J, Cooke JP, and Kuo CJ. Adenoviral gene transfer with soluble vascular endothelial growth factor receptors impairs angiogenesis and perfusion in a murine model of hind limb ischemia. Circulation 110: 2424-2429, 2004.
14. Jiang BH, Aoki M, Zheng JZ, Li J, and Vogt PK. Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt=protein kinase B. Proc Natl Acad Sci USA 96: 2077-2081, 1999.
15. Kamoun P. Endogenous production of hydrogen sulfide in mammals. Amino Acids 26: 243-254, 2004.
16. Kery V, Bukovska G, and Kraus JP. Transsulfuration depends on heme in addition to pyridoxal 5'-phosphate. Cystathionine beta-synthase is a heme protein. J Biol Chem 269: 25283-25288, 1994.
17. Li L, Bhatia M, Zhu YZ, Zhu YC, Ramnath RD, Wang ZJ, Anuar FBM, Whiteman M, Salto-Tellez M, and Moore PK. Hydrogen sulfide is a novel mediator of lipopolysaccharideinduced inflammation in the mouse. FASEB J 19: 1196-1198, 2005.
18. Li L, Hsu A, and Moore PK. Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation - a tale of three gases! Pharmacol Ther 123: 386-400, 2009.
19. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan C-H, and Moore PK. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): New insights into the biology of hydrogen sulfide. Circulation 117: 2351-2360, 2008.
20. Nessa A, Latif SA, Siddiqui NI, Hussain MA, Bhuiyan MR, Hossain MA, Akther A, and Rahman M. Angiogenesis: A novel therapeutic approach for ischemic heart disease. Mymensingh Med J 18: 264-272, 2009.
21. Pyiochou A, Papapetropoulos A, Olah G, Wintner E, Jeschke M, Branski L, Herndon D, Traber D, and Szabo C. The hydrogen sulfide donor IK-1001 stimulates neovascularization and improves wound healing. FASEB J 22: 91242, 2008.
22. Schwarz ER, Speakman MT, Patterson M, Hale SS, Isner JM, Kedes LH, and Kloner RA. Evaluation of the effects of intramyocardial injection of DNA expressing vascular endothelial growth factor (VEGF) in a myocardial infarction model in the rat-Angiogenesis and angioma formation. J Am Coll Cardiol 35: 1323-1330, 2000.
23. Shi Y-X, Chen Y, Zhu Y-Z, Huang G-Y, Moore PK, Huang S-H, Yao T, and Zhu Y-C. Chronic sodium hydrosulfide treatment decreases medial thickening of intramyocardial coronary arterioles, interstitial fibrosis, and ROS production in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 293: H2093-2100, 2007.
24. Smith RS, Jr., Lin K-F, Agata J, Chao L, and Chao J. Human endothelial nitric oxide synthase gene delivery promotes angiogenesis in a rat model of hind limb ischemia. Arterioscler Thromb Vasc Biol 22: 1279-1285, 2002.
25. Stipanuk MH and Beck PW. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 206: 267-277, 1982.
26. Sugano M, Tsuchida K, and Makino N. Intramuscular gene transfer of soluble tumor necrosis factor-{alpha} receptor 1 activates vascular endothelial growth factor receptor and accelerates angiogenesis in a rat model of hind limb ischemia. Circulation 109: 797-802, 2004.
27. Sun Y-G, Cao Y-X, Wang W-W, Ma S-F, Yao T, and Zhu Y-C. Hydrogen sulphide is an inhibitor of L-type calcium channels and mechanical contraction in rat cardiomyocytes. Cardiovasc Res79: 632-641, 2008.
28. Swaroop M, Bradley K, Ohura T, Tahara T, Roper MD, Rosenberg LE, and Kraus JP. Rat cystathionine betasynthase: Gene organization and alternative splicing. J Biol Chem 267: 11455-11461, 1992.
29. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6: 917-935, 2007.
30. Takahashi H and Shibuya M. The vascular endothelial growth factor (VEGF)=VEGF receptor system and its role under physiological and pathological conditions. Clin. Sci. 109: 227-241, 2005.
31. Takeshita S, Zheng LP, Brogi E, Kearney M, Pu LQ, Bunting S, Ferrara N, Symes JF, and Isner JM. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest 93: 662-670, 1994.
32. Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, and Alexander RW. Role of gp91phox (Nox2)- containing NAD(P)H oxidase in angiogenesis in response to hind limb ischemia. Circulation 111: 2347-2355, 2005.
33. Tritsaris K, Myren M, Ditlev SB, Hubschmann MV, van der Blom I, Hansen AJ, Olsen UB, Cao R, Zhang J, Jia T, Wahlberg E, Dissing S, and Cao Y. IL-20 is an arteriogenic cytokine that remodels collateral networks and improves functions of ischemic hind limbs. Proc Natl Acad Sci USA 104: 15364-15369, 2007.
34. Westerweel PE, Rookmaaker MB, van Zonneveld AJ, Bleys RL, Rabelink TJ, and Verhaar MC. A study of neovascularization in the rat ischemic hind limb using Araldite casting and Spalteholtz tissue clearing. Cardiovasc Pathol 14: 294-297, 2005.
35. Whiteman M and Moore PK. Hydrogen sulfide and the vasculature: A novel vasculoprotective entity and regulator of nitric oxide bioavailability? J Cell Mol Med 13: 488-507, 2009.
36. Wu G, Mannam AP, Wu J, Kirbis S, Shie J-L, Chen C, Laham RJ, Sellke FW, and Li J. Hypoxia induces myocytedependent COX-2 regulation in endothelial cells: Role of VEGF. Am J Physiol Heart Circ Physiol 285: H2420-2429, 2003.
37. Yan H, Du J, and Tang C. The possible role of hydrogen sulfide on the pathogenesis of spontaneous hypertension in rats. Biochem Biophys Res Commun 313: 22-27, 2004. (Pubitemid 37524019)
38. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, and Wang R. H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine {gamma}-lyase. Science 322: 587-590, 2008.
39. Yla-Herttuala S and Alitalo K. Gene transfer as a tool to induce therapeutic vascular growth. Nat Med 9: 694-701, 2003.
40. Zanardo RCO, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, and Wallace JL. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 20: 2118-2120, 2006.
41. Zhao W, Zhang J, Lu Y, and Wang R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20: 6008-6016, 2001.
42. Ziche M, Morbidelli L, Masini E, Amerini S, Granger HJ, Maggi CA, Geppetti P, and Ledda F. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 94: 2036-2044, 1994.