Cystathionine γ-lyase is expressed in human atherosclerotic plaque microvessels and is involved in micro-angiogenesis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Van Den Born, J C ^a   Mencke, R ^a   Conroy, S ^a   Zeebregts, C J ^a   Van Goor, H ^a   Hillebrands, J L ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE GAMMA LYASE;

AGED; ATHEROSCLEROTIC PLAQUE; BIOSYNTHESIS; CLINICAL TRIAL; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; HUMAN; MALE; MICROVASCULATURE; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; CYSTATHIONINE GAMMA-LYASE; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MALE; MICROVESSELS; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; PLAQUE, ATHEROSCLEROTIC;

EID: 84990821392     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep34608     Document Type: Article

References (38)

1. World Health Organisation. In (World Health Organization, Geneva, 2014).
2. Glass, C. K. & Witztum, J. L. Atherosclerosis. the road ahead. Cell 104, 503-516 (2001).
3. McCarthy, M. J. et al. Angiogenesis and the atherosclerotic carotid plaque: an association between symptomatology and plaque morphology. J. Vasc. Surg. 30, 261-268 (1999).
4. Hermus, L., Lefrandt, J. D., Tio, R. A., Breek, J. C. & Zeebregts, C. J. Carotid plaque formation and serum biomarkers. Atherosclerosis 213, 21-29 (2010).
5. Cai, W. J. et al. The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc. Res. 76, 29-40 (2007).
6. Szabo, C. & Papapetropoulos, A. Hydrogen sulphide and angiogenesis: mechanisms and applications. Br. J. Pharmacol. 164, 853-865 (2011).
7. Wang, R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 16, 1792-1798 (2002).
8. Yang, G. et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322, 587-590 (2008).
9. Bian, J. S. et al. Role of hydrogen sulfide in the cardioprotection caused by ischemic preconditioning in the rat heart and cardiac myocytes. J. Pharmacol. Exp. Ther. 316, 670-678 (2006).
10. Zhao, W., Zhang, J., Lu, Y. & Wang, R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J. 20, 6008-6016 (2001)
11. Bos, E. M. et al. Cystathionine gamma-lyase protects against renal ischemia/reperfusion by modulating oxidative stress. J. Am. Soc. Nephrol. 24, 759-770 (2013).
12. Papapetropoulos, A. et al. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci. USA. 106, 21972-21977 (2009).
13. Calvert, J. W. et al. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ. Res. 105, 365-374 (2009).
14. Wang, Y. et al. Role of hydrogen sulfide in the development of atherosclerotic lesions in apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol. 29, 173-179 (2009).
15. Yang, G. et al. Cystathionine gamma-lyase deficiency and overproliferation of smooth muscle cells. Cardiovasc. Res. 86, 487-495 (2010).
16. Mani, S. et al. Decreased endogenous production of hydrogen sulfide accelerates atherosclerosis. Circulation 127, 2523-2534 (2013).
17. Yang, G. et al. Increased neointimal formation in cystathionine gamma-lyase deficient mice: role of hydrogen sulfide in alpha5beta1- integrin and matrix metalloproteinase-2 expression in smooth muscle cells. J. Mol. Cell. Cardiol. 52, 677-688 (2012).
18. Redgrave, J. N., Lovett, J. K., Gallagher, P. J. & Rothwell, P. M. Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms: the Oxford plaque study. Circulation 113, 2320-2328 (2006).
19. Redgrave, J. N., Gallagher, P., Lovett, J. K. & Rothwell, P. M. Critical cap thickness and rupture in symptomatic carotid plaques: the oxford plaque study. Stroke 39, 1722-1729 (2008).
20. Martinet, W., De Meyer, G. R., Herman, A. G. & Kockx, M. M. RNA damage in human atherosclerosis: pathophysiological significance and implications for gene expression studies. RNA Biol. 2, 4-7 (2005).
21. Tao, B. B. et al. VEGFR2 functions as an H2S-targeting receptor protein kinase with its novel Cys1045-Cys1024 disulfide bond serving as a specific molecular switch for hydrogen sulfide actions in vascular endothelial cells. Antioxid. Redox Signal. 19, 448-464 (2013).
22. Zhou, Y. et al. Hydrogen sulfide promotes angiogenesis by downregulating miR-640 via the VEGFR2/mTOR pathway. Am. J. Physiol. Cell. Physiol. 310, C305-C317 (2016).
23. Hellings, W. E. et al. Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: a prognostic study. Circulation 121, 1941-1950 (2010).
24. Moreno, P. R. et al. Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation 110, 2032-2038 (2004).
25. Cheng, C., Chrifi, I., Pasterkamp, G. & Duckers, H. J. Biological mechanisms of microvessel formation in advanced atherosclerosis: the big five. Trends Cardiovasc. Med. 23, 153-164 (2013).
26. Virmani, R. et al. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler. Thromb. Vasc. Biol. 25, 2054-2061 (2005).
27. Tripatara, P. et al. Generation of endogenous hydrogen sulfide by cystathionine gamma-lyase limits renal ischemia/reperfusion injury and dysfunction. Lab. Invest. 88, 1038-1048 (2008).
28. Tripatara, P. et al. Characterisation of cystathionine gamma-lyase/hydrogen sulphide pathway in ischaemia/reperfusion injury of the mouse kidney: an in vivo study. Eur. J. Pharmacol. 606, 205-209 (2009).
29. Wang, M., Guo, Z. & Wang, S. Regulation of cystathionine gamma-lyase in mammalian cells by hypoxia. Biochem. Genet. 52, 29-37 (2014).
30. Mani, S., Untereiner, A., Wu, L. & Wang, R. Hydrogen sulfide and the pathogenesis of atherosclerosis. Antioxid. Redox Signal. 20, 805-817 (2014).
31. Cheung, S. H., Kwok, W. K., To, K. F. & Lau, J. Y. Anti-atherogenic effect of hydrogen sulfide by over-expression of cystathionine gamma-lyase (CSE) gene. PLoS One 9, e113038 (2014).
32. Liu, Z. et al. The hydrogen sulfide donor, GYY4137, exhibits anti-atherosclerotic activity in high fat fed apolipoprotein E(-/-) mice. Br. J. Pharmacol. 169, 1795-1809 (2013).
33. Kolluru, G. K. et al. Cystathionine gamma-lyase regulates arteriogenesis through NO-dependent monocyte recruitment. Cardiovasc. Res. 107, 590-600 (2015).
34. Wang, Y. et al. Gene delivery of soluble vascular endothelial growth factor receptor-1 (sFlt-1) inhibits intra-plaque angiogenesis and suppresses development of atherosclerotic plaque. Clin. Exp. Med. 11, 113-121 (2011).
35. Winnik, S. et al. Systemic VEGF inhibition accelerates experimental atherosclerosis and disrupts endothelial homeostasis - implications for cardiovascular safety. Int. J. Cardiol. 168, 2453-2461 (2013).
36. Ades, E. W. et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99, 683-690 (1992).
37. Li, L. et al. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117, 2351-2360 (2008).
38. Watanabe, N. et al. Urinary protein as measured with a pyrogallol red-molybdate complex, manually and in a Hitachi 726 automated analyzer. Clin. Chem. 32, 1551-1554 (1986).