Hydrogen sulphide and angiogenesis: Mechanisms and applications

British Journal of Pharmacology

Volumn 164, Issue 3, 2011, Pages 853-865

  Szabó, Csaba ^a   Papapetropoulos, Andreas ^b  

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

^b UNIVERSITY OF PATRAS   (Greece)

Author keywords

blood vessels; cell differentiation; cell migration; cysteine; endothelium; ischaemia; kinases; nitric oxide

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; BIOLOGICAL MARKER; CASPASE; CYCLIC AMP; CYSTATHIONINE GAMMA LYASE; CYSTEINE; ENZYME INHIBITOR; GLIBENCLAMIDE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HYDROGEN SULFIDE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHODIESTERASE; PHOSPHOTRANSFERASE; PROTEIN KINASE B; VASCULOTROPIN;

ANGIOGENESIS; ANTIOXIDANT ACTIVITY; BIOLOGICAL ACTIVITY; BLOOD VESSEL; CALCIUM CELL LEVEL; CELL LEVEL; CELL MIGRATION; CELL PROLIFERATION; CELL PROTECTION; CELL STIMULATION; CHEMICAL REACTION; CHICKEN; CHORIOALLANTOIS; CONCENTRATION RESPONSE; CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; GAS ANALYSIS; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIMB ISCHEMIA; MOLECULAR DYNAMICS; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; VASODILATATION; WOUND HEALING;

ANIMALS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; HYDROGEN SULFIDE; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION;

EID: 80052020182     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.01191.x     Document Type: Review

References (77)

1. Adams DJ, Hill MA, (2004). Potassium channels and membrane potential in the modulation of intracellular calcium in vascular endothelial cells. J Cardiovasc Electrophysiol 15: 598-610. (Pubitemid 38621914)
2. Bauer CC, Boyle JP, Porter KE, Peers C, (2010). Modulation of Ca(2+) signalling in human vascular endothelial cells by hydrogen sulfide. Atherosclerosis 209: 374-380.
3. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, et al,. (2007). Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A 104: 17977-17982. (Pubitemid 350210806)
4. Breslin JW, Pappas PJ, Cerveira JJ, Hobson RW 2nd, Durán WN, (2003). VEGF increases endothelial permeability by separate signaling pathways involving ERK-1/2 and nitric oxide. Am J Physiol Heart Circ Physiol 284: H92-H100. (Pubitemid 36076274)
5. Broadhead MW, Kharbanda RK, Peters MJ, MacAllister RJ, (2004). KATP channel activation induces ischemic preconditioning of the endothelium in humans in vivo. Circulation 110: 2077-2082. (Pubitemid 39372482)
6. Bucci M, Papapetropoulos A, Vellecco V, Zhou Z, Pyriochou A, Roussos C, et al,. (2010). Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol 30: 1998-2004.
7. Budde MW, Roth MB, (2010). Hydrogen sulfide increases hypoxia-inducible factor-1 activity independently of von Hippel-Lindau tumor suppressor-1 in C. elegans. Mol Biol Cell 21: 212-217.
8. Cai WJ, Wang MJ, Moore PK, Jin HM, Yao T, Zhu YC, (2007). The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc Res 76: 29-40. (Pubitemid 47362041)
9. Calvert JW, Coetzee WA, Lefer DJ, (2010). Novel insights into hydrogen sulfide-mediated cytoprotection. Antioxid Redox Signal 12: 1203-1217.
10. Cheang WS, Wong WT, Shen B, Lau CW, Tian XY, Tsang SY, et al,. (2010). 4-aminopyridine-sensitive K+ channels contributes to NaHS-induced membrane hyperpolarization and relaxation in the rat coronary artery. Vascul Pharmacol 53: 94-98.
11. Cheng Y, Ndisang JF, Tang G, Cao K, Wang R, (2004). Hydrogen sulfide-induced relaxation of resistance mesenteric artery beds of rats. Am J Physiol Heart Circ Physiol 287: H2316-H2323. (Pubitemid 39430772)
12. De Val S, Black BL, (2009). Transcriptional control of endothelial cell development. Dev Cell 16: 180-195.
13. Dimmeler S, Dernbach E, Zeiher AM, (2000). Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett 477: 258-262. (Pubitemid 30450177)
14. Eble JA, Niland S, (2009). The extracellular matrix of blood vessels. Curr Pharm Des 15: 1385-1400.
15. Elsey DJ, Fowkes RC, Baxter GF, (2010). Regulation of cardiovascular cell function by hydrogen sulfide (H(2)S). Cell Biochem Funct 28: 95-106.
16. Figura M, Chilton L, Liacini A, Viskovic MM, Phan V, Knight D, et al,. (2009). Blockade of K(ATP) channels reduces endothelial hyperpolarization and leukocyte recruitment upon reperfusion after hypoxia. Am J Transplant 9: 687-696.
17. Fiorucci S, Distrutti E, Cirino G, Wallace JL, (2006). The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology 131: 259-271. (Pubitemid 44043128)
18. Folkman J, (2006). Antiangiogenesis in cancer therapy-endostatin and its mechanisms of action. Exp Cell Res 312: 594-607. (Pubitemid 43290336)
19. Frank RN, (2009). Treating diabetic retinopathy by inhibiting growth factor pathways. Curr Opin Investig Drugs 10: 327-335.
20. Gadalla MM, Snyder SH, (2010). Hydrogen sulfide as a gasotransmitter. J Neurochem 113: 14-26.
21. Grossi L, (2009). Hydrogen sulfide induces nitric oxide release from nitrite. Bioorg Med Chem Lett 19: 6092-6094.
22. Grossini E, Molinari C, Caimmi PP, Uberti F, Vacca G, (2009). Levosimendan induces NO production through p38 MAPK, ERK and Akt in porcine coronary endothelial cells: role for mitochondrial K(ATP) channel. Br J Pharmacol 156: 250-261.
23. 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: 527-531. (Pubitemid 27434718)
24. Jackson WF, (2005). Potassium channels in the peripheral microcirculation. Microcirculation 12: 113-127. (Pubitemid 40450623)
25. Jiang B, Tang G, Cao K, Wu L, Wang R, (2010). Molecular mechanism for H(2)S-induced activation of K(ATP) channels. Antioxid Redox Signal 12: 1167-1178.
26. Kimura H, (2010). Hydrogen sulfide: from brain to gut. Antioxid Redox Signal 12: 1111-1123.
27. Li HB, Ge YK, Zhang L, Zheng XX, (2006). Astragaloside IV improved barrier dysfunction induced by acute high glucose in human umbilical vein endothelial cells. Life Sci 79: 1186-1193. (Pubitemid 44128584)
28. Liu YH, Bian JS, (2010). Bicarbonate-dependent effect of hydrogen sulfide on vascular contractility in rat aortic rings. Am J Physiol Cell Physiol 299: C866-C872.
29. Liu X, Pan L, Wang X, Gong Q, Deng H, Zheng H, et al,. (2010a). Hydrogen Sulfide Improves Cardiac Function through Anti-inflammation and Neovascularization in a Rat Model of Heart Failure. Biol Pharm Bull in press.
30. Liu X, Pan L, Zhuo Y, Gong Q, Rose P, Zhu Y, (2010b). Hypoxia-inducible factor-1alpha is involved in the pro-angiogenic effect of hydrogen sulfide under hypoxic stress. Biol Pharm Bull 33: 1550-1554.
31. Malester B, Tong X, Ghiu I, Kontogeorgis A, Gutstein DE, Xu J, et al,. (2007). Transgenic expression of a dominant negative K(ATP) channel subunit in the mouse endothelium: effects on coronary flow and endothelin-1 secretion. FASEB J 21: 2162-2172. (Pubitemid 47026451)
32. Minamishima S, Bougaki M, Sips PY, Yu JD, Minamishima YA, Elrod JW, et al,. (2009). Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation 120: 888-896.
33. Morbidelli L, Donnini S, Ziche M, (2003). Role of nitric oxide in the modulation of angiogenesis. Curr Pharm Des 9: 521-530. (Pubitemid 36221720)
34. Morbidelli L, Pyriochou A, Filippi S, Vasileiadis I, Roussos C, Zhou Z, et al,. (2010). The soluble guanylyl cyclase inhibitor NS-2028 reduces vascular endothelial growth factor-induced angiogenesis and permeability. Am J Physiol Regul Integr Comp Physiol 298: R824-R832.
35. ATP channel subunits in mouse and rat cardiac myocytes and the coronary vasculature. BMC Physiol 5: 1.
36. Nicholson BP, Schachat AP, (2010). A review of clinical trials of anti-VEGF agents for diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 248: 915-930.
37. Niu G, Chen X, (2010). Vascular endothelial growth factor as an anti-angiogenic target for cancer therapy. Curr Drug Targets 11: 1000-1017.
38. Olson KR, (2009). Is hydrogen sulfide a circulating 'gasotransmitter' in vertebrate blood? Biochim Biophys Acta 1787: 856-863.
39. Ozsvári B, Puskás LG, Nagy LI, Kanizsai I, Gyuris M, Madácsi R, et al,. (2010). A cell-microelectronic sensing technique for the screening of cytoprotective compounds. Int J Mol Med 25: 525-530.
40. Papapetropoulos A, García-Cardeña G, Madri JA, Sessa WC, (1997). Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 100: 3131-3139. (Pubitemid 28022851)
41. Papapetropoulos A, Pyriochou A, Altaany Z, Yang G, Marazioti A, Zhou Z, et al,. (2009). Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci U S A 106: 21972-21977.
42. Parenti A, Morbidelli L, Cui XL, Douglas JG, Hood JD, Granger HJ, et al,. (1998). Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase1/2 activation in postcapillary endothelium. J Biol Chem 273: 4220-4226. (Pubitemid 28103293)
43. Predmore BL, Lefer DJ, (2010). Development of hydrogen sulfide-based therapeutics for cardiovascular disease. J Cardiovasc Transl Res 3: 487-498.
44. Pyriochou A, Beis D, Koika V, Potytarchou C, Papadimitriou E, Zhou Z, et al,. (2006). Soluble guanylyl cyclase activation promotes angiogenesis. J Pharmacol Exp Ther 319: 663-671.
45. Pyriochou A, Vassilakopoulos T, Zhou Z, Papapetropoulos A, (2007a). cGMP-dependent and -independent angiogenesis-related properties of nitric oxide. Life Sci 81: 1549-1554. (Pubitemid 350081039)
46. Pyriochou A, Zhou Z, Koika V, Petrou C, Cordopatis P, Sessa WC, et al,. (2007b). The phosphodiesterase 5 inhibitor sildenafil stimulates angiogenesis through a protein kinase G/MAPK pathway. J Cell Physiol 211: 197-204. (Pubitemid 46363910)
47. Reynolds AR, (2010). Potential relevance of bell-shaped and u-shaped dose-responses for the therapeutic targeting of angiogenesis in cancer. Dose Response 8: 253-284.
48. Ruegg C, Mutter N, (2007). Anti-angiogenic therapies in cancer: achievements and open questions. Bull Cancer 94: 753-762. (Pubitemid 47605603)
49. Shimizu S, Kageyama M, Yasuda M, Sasaki D, Naito S, Yamamoto T, et al,. (2004). Stimulation of in vitro angiogenesis by nitric oxide through the induction of transcription factor ETS-1. Int J Biochem Cell Biol 36: 114-122. (Pubitemid 37338477)
50. Siebert N, Cantré D, Eipel C, Vollmar B, (2008). H2S contributes to the hepatic arterial buffer response and mediates vasorelaxation of the hepatic artery via activation of K(ATP) channels. Am J Physiol Gastrointest Liver Physiol 295: G1266-G1273.
51. Silvestre JS, Mallat Z, Tedgui A, Lévy BI, (2008). Post-ischaemic neovascularization and inflammation. Cardiovasc Res 78: 242-249. (Pubitemid 351556102)
52. Szabo C, (2007). Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6: 917-935. (Pubitemid 350042399)
53. Szabo S, Gombos Z, Sandor Z, (1999). Growth factors in gastrointestinal diseases. BioDrugs 12: 27-41. (Pubitemid 29334254)
54. Tajima M, Ishizuka N, Saitoh K, Sakagami H, (2008). Nicorandil enhances the effect of endothelial nitric oxide under hypoxia-reoxygenation: role of the KATP channel. Eur J Pharmacol 579: 86-92.
55. Takano H, Dora KA, Spitaler MM, Garland CJ, (2004). Spreading dilatation in rat mesenteric arteries associated with calcium-independent endothelial cell hyperpolarization. J Physiol 556: 887-903. (Pubitemid 38660321)
56. Tang G, Wu L, Wang R, (2010). Interaction of hydrogen sulfide with ion channels. Clin Exp Pharmacol Physiol 37: 753-763.
57. Tarnawski AS, (2005). Cellular and molecular mechanisms of gastrointestinal ulcer healing. Dig Dis Sci 50: S24-S33. (Pubitemid 41380795)
58. Thejass P, Kuttan G, (2007). Inhibition of angiogenic differentiation of human umbilical vein endothelial cells by diallyl disulfide (DADS). Life Sci 80: 515-521. (Pubitemid 46038323)
59. Tomaskova Z, Cacanyiova S, Benco A, Kristek F, Dugovicova L, Hrbac J, et al,. (2009). Lipids modulate H(2)S/HS(-) induced NO release from S-nitrosoglutathione. Biochem Biophys Res Commun 390: 1241-1244.
60. Toombs CF, Insko MA, Wintner EA, Deckwerth TL, Usansky H, Jamil K, et al,. (2010). Detection of exhaled hydrogen sulphide gas in healthy human volunteers during intravenous administration of sodium sulphide. Br J Clin Pharmacol 69: 626-636.
61. Wallace JL, Vong L, McKnight W, Dicay M, Martin GR, (2009). Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology 137: 569-578.
62. Wang R, (2003). The gasotransmitter role of hydrogen sulfide. Antioxid Redox Signal 5: 493-501. (Pubitemid 37087410)
63. Wang MJ, Cai WJ, Li N, Ding YJ, Chen Y, Zhu YC, (2010). The hydrogen sulfide donor NaHS promotes angiogenesis in a rat model of hind limb ischemia. Antioxid Redox Signal 12: 1065-1077.
64. White R, Hiley CR, (2000). Hyperpolarisation of rat mesenteric endothelial cells by ATP-sensitive K(+) channel openers. Eur J Pharmacol 397: 279-290. (Pubitemid 30323779)
65. Whiteman M, Li L, Kostetski I, Chu SH, Siau JL, Bhatia M, et al,. (2006). Evidence for the formation of a novel nitrosothiol from the gaseous mediators nitric oxide and hydrogen sulphide. Biochem Biophys Res Commun 343: 303-310.
66. Whitfield NL, Kreimier EL, Verdial FC, Skovgaard N, Olson KR, (2008). Reappraisal of H2S/sulfide concentration in vertebrate blood and its potential significance in ischemic preconditioning and vascular signaling. Am J Physiol Regul Integr Comp Physiol 294: R1930-R1937.
67. Wintner EA, Deckwerth TL, Langston W, Bengtsson A, Leviten D, Hill P, et al,. (2010). A monobromobimane-based assay to measure the pharmacokinetic profile of reactive sulphide species in blood. Br J Pharmacol 160: 941-957.
68. Xiao D, Li M, Herman-Antosiewicz A, Antosiewicz J, Xiao H, Lew KL, et al,. (2006). Diallyl trisulfide inhibits angiogenic features of human umbilical vein endothelial cells by causing Akt inactivation and down-regulation of VEGF and VEGF-R2. Nutr Cancer 55: 94-107. (Pubitemid 44477050)
69. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, et al,. (2008). H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322: 587-590.
70. Yang W, Yang G, Jia X, Wu L, Wang R, (2005). Activation of KATP channels by H2S in rat insulin-secreting cells and the underlying mechanisms. J Physiol 569: 519-531. (Pubitemid 41830119)
71. Yong QC, Hu LF, Wang S, Huang D, Bian JS, (2010). Hydrogen sulfide interacts with nitric oxide in the heart: possible involvement of nitroxyl. Cardiovasc Res 88: 482-489.
72. ATP Channels in Human Coronary Artery Endothelial Cells consist of a Heteromultimeric Complex of Kir6.1, Kir6.2, and SUR2B Subunits. J Mol Cell Cardiol 37: 857-869. (Pubitemid 39232076)
73. Yusof M, Kamada K, Kalogeris T, Gaskin FS, Korthuis RJ, (2009). Hydrogen sulfide triggers late-phase preconditioning in postischemic small intestine by an NO- and p38 MAPK-dependent mechanism. Am J Physiol Heart Circ Physiol 296: H868-H876.
74. Zachary I, Gliki G, (2001). Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res 49: 568-581. (Pubitemid 32146420)
75. 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: 6008-6016. (Pubitemid 33049276)
76. Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, et al,. (1997). Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99: 2625-2634. (Pubitemid 27259809)
77. Zuidema MY, Yang Y, Wang M, Kalogeris T, Liu Y, Meininger CJ, et al,. (2010). Antecedent hydrogen sulfide elicits an anti-inflammatory phenotype in postischemic murine small intestine: role of BK channels. Am J Physiol Heart Circ Physiol 299: H1554-H1567.