Doxycycline ameliorates 2K-1C hypertension-induced vascular dysfunction in rats by attenuating oxidative stress and improving nitric oxide bioavailability

Nitric Oxide - Biology and Chemistry

Volumn 26, Issue 3, 2012, Pages 162-168

  Castro, Michele M ^a   Rizzi, Elen ^a   Ceron, Carla S ^a   Guimaraes, Danielle A ^a   Rodrigues, Gerson J ^a   Bendhack, Lusiane M ^a   Gerlach, Raquel F ^a   Tanus Santos, Jose Eduardo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

2K 1C hypertension; Arterial endothelial dysfunction; Doxycycline; Matrix metalloproteinases; Oxidative stress; Reactive oxygen species

Indexed keywords

CALCIMYCIN; DOXYCYCLINE; MATRIX METALLOPROTEINASE; NITRIC OXIDE; PHORBOL 13 ACETATE 12 MYRISTATE; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RENOVASCULAR DISEASE; RENOVASCULAR HYPERTENSION; SHAM PROCEDURE; TWO KIDNEY ONE CLIP HYPERTENSION; VASODILATATION; ZYMOGRAPHY;

ANIMALS; AORTA; BLOOD PRESSURE; CALCIMYCIN; CALCIUM IONOPHORES; DISEASE MODELS, ANIMAL; DOXYCYCLINE; HYPERTENSION, RENAL; KIDNEY; LINEAR MODELS; MALE; MATRIX METALLOPROTEINASE 9; NEUTROPHILS; NITRIC OXIDE; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

RATTUS;

EID: 84859099989     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2012.01.009     Document Type: Article

References (46)

1. J.D. Humphrey Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress Hypertension 52 2008 195 200
2. C.A. Lemarie, P.L. Tharaux, and S. Lehoux Extracellular matrix alterations in hypertensive vascular remodeling J. Mol. Cell. Cardiol. 48 2009 433 439
3. H.D. Intengan, and E.L. Schiffrin Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis Hypertension 38 2001 581 587
4. V.J. Dzau, G.H. Gibbons, Endothelium and growth factors in vascular remodeling of hypertension, Hypertension 18 (1991) III115-III121.
5. R.M. Touyz, and A.M. Briones Reactive oxygen species and vascular biology: implications in human hypertension Hypertens. Res. 34 2010 5 14
6. K.K. Griendling, and G.A. FitzGerald Oxidative stress and cardiovascular injury: Part II: animal and human studies Circulation 108 2003 2034 2040
7. N. Escobales, and M.J. Crespo Oxidative-nitrosative stress in hypertension Curr. Vasc. Pharmacol. 3 2005 231 246
8. M.M. Castro, E. Rizzi, G.J. Rodrigues, C.S. Ceron, L.M. Bendhack, R.F. Gerlach, and J.E. Tanus-Santos Antioxidant treatment reduces matrix metalloproteinase-2-induced vascular changes in renovascular hypertension Free Radic. Biol. Med. 46 2009 1298 1307
9. Yasmin, C.M. McEniery, S. Wallace, Z. Dakham, P. Pulsalkar, K. Maki-Petaja, M.J. Ashby, J.R. Cockcroft, I.B. Wilkinson, Matrix metalloproteinase-9 (MMP-9), MMP-2, and serum elastase activity are associated with systolic hypertension and arterial stiffness. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 372-378.
10. S.H. Ahmed, L.L. Clark, W.R. Pennington, C.S. Webb, D.D. Bonnema, A.H. Leonardi, C.D. McClure, F.G. Spinale, and M.R. Zile Matrix metalloproteinases/ tissue inhibitors of metalloproteinases: relationship between changes in proteolytic determinants of matrix composition and structural, functional, and clinical manifestations of hypertensive heart disease Circulation 113 2006 2089 2096
11. C. Bouvet, L.A. Gilbert, D. Girardot, D. deBlois, and P. Moreau Different involvement of extracellular matrix components in small and large arteries during chronic NO synthase inhibition Hypertension 45 2005 432 437
12. S.W. Watts, C. Rondelli, K. Thakali, X. Li, B. Uhal, M.H. Pervaiz, R.E. Watson, and G.D. Fink Morphological and biochemical characterization of remodeling in aorta and vena cava of DOCA-salt hypertensive rats Am. J. Physiol. Heart Circ. Physiol. 292 2007 H2438 H2448
13. S. Lehoux, C.A. Lemarie, B. Esposito, H.R. Lijnen, and A. Tedgui Pressure-induced matrix metalloproteinase-9 contributes to early hypertensive remodeling Circulation 109 2004 1041 1047
14. M. Flamant, S. Placier, C. Dubroca, B. Esposito, I. Lopes, C. Chatziantoniou, A. Tedgui, J.C. Dussaule, and S. Lehoux Role of matrix metalloproteinases in early hypertensive vascular remodeling Hypertension 50 2007 212 218
15. M.M. Castro, E. Rizzi, L. Figueiredo-Lopes, K. Fernandes, L.M. Bendhack, D.L. Pitol, R.F. Gerlach, and J.E. Tanus-Santos Metalloproteinase inhibition ameliorates hypertension and prevents vascular dysfunction and remodeling in renovascular hypertensive rats Atherosclerosis 198 2008 320 331
16. E. Rizzi, M.M. Castro, K. Fernandes, F. Barbosa Jr., G.M. Arisi, N. Garcia-Cairasco, L.M. Bendhack, J.E. Tanus-Santos, and R.F. Gerlach Evidence of early involvement of matrix metalloproteinase-2 in lead-induced hypertension Arch. Toxicol. 83 2009 439 449
17. M.M. Castro, E. Rizzi, C.M. Prado, M.A. Rossi, J.E. Tanus-Santos, and R.F. Gerlach Imbalance between matrix metalloproteinases and tissue inhibitor of metalloproteinases in hypertensive vascular remodeling Matrix Biol. 29 2009 194 201
18. A.C. Newby Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substrates Cardiovasc. Res. 69 2006 614 624
19. Z.S. Galis, and J.J. Khatri Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly Circ. Res. 90 2002 251 262
20. T. Okamoto, T. Akaike, T. Sawa, Y. Miyamoto, A. van der Vliet, and H. Maeda Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation J. Biol. Chem. 276 2001 29596 29602
21. S. Viappiani, A.C. Nicolescu, A. Holt, G. Sawicki, B.D. Crawford, H. Leon, T. van Mulligen, and R. Schulz Activation and modulation of 72 kDa matrix metalloproteinase-2 by peroxynitrite and glutathione Biochem. Pharmacol. 77 2009 826 834
22. L. Hao, T. Nishimura, H. Wo, and C. Fernandez-Patron Vascular responses to alpha1-adrenergic receptors in small rat mesenteric arteries depend on mitochondrial reactive oxygen species Arterioscler. Thromb. Vasc. Biol. 26 2006 819 825
23. L.M. Golub, H.M. Lee, M.E. Ryan, W.V. Giannobile, J. Payne, and T. Sorsa Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms Adv Dent Res 12 1998 12 26
24. H.M. Lee, S.G. Ciancio, G. Tuter, M.E. Ryan, E. Komaroff, and L.M. Golub Subantimicrobial dose doxycycline efficacy as a matrix metalloproteinase inhibitor in chronic periodontitis patients is enhanced when combined with a non-steroidal anti-inflammatory drug J. Periodontol. 75 2004 453 463
25. M.M. Castro, J.E. Tanus-Santos, and R.F. Gerlach Matrix metalloproteinases: targets for doxycycline to prevent the vascular alterations of hypertension Pharmacol. Res. 64 2011 567 572
26. D.A. Guimaraes, E. Rizzi, C.S. Ceron, A.M. Oliveira, D.M. Oliveira, M.M. Castro, C.R. Tirapelli, R.F. Gerlach, and J.E. Tanus-Santos Doxycycline dose-dependently Inhibits MMP-2-mediated vascular changes in 2K1C hypertension Basic Clin. Pharmacol. Toxicol. 108 2011 318 325
27. H.C. Lai, Y.C. Yeh, C.T. Ting, W.L. Lee, H.W. Lee, L.C. Wang, K.Y. Wang, H.C. Lai, A. Wu, and T.J. Liu Doxycycline suppresses doxorubicin-induced oxidative stress and cellular apoptosis in mouse hearts Eur. J. Pharmacol. 644 2010 176 187
28. Y.C. Yeh, H.C. Lai, C.T. Ting, W.L. Lee, L.C. Wang, K.Y. Wang, H.C. Lai, and T.J. Liu Protection by doxycycline against doxorubicin-induced oxidative stress and apoptosis in mouse testes Biochem. Pharmacol. 74 2007 969 980
29. M.O. Griffin, E. Fricovsky, G. Ceballos, and F. Villarreal Tetracyclines: a pleitropic family of compounds with promising therapeutic properties. Review of the literature Am. J. Physiol. Cell Physiol. 299 2010 C539 C548
30. F.A. DeLano, and G.W. Schmid-Schonbein Proteinase activity and receptor cleavage: mechanism for insulin resistance in the spontaneously hypertensive rat Hypertension 52 2008 415 423
31. D. Hoeben, C. Burvenich, and R. Heyneman Antibiotics commonly used to treat mastitis and respiratory burst of bovine polymorphonuclear leukocytes J. Dairy Sci. 81 1998 403 410
32. N.S. Ramamurthy, A.T. Vernillo, R.A. Greenwald, H.M. Lee, T. Sorsa, L.M. Golub, and B.R. Rifkin Reactive oxygen species activate and tetracyclines inhibit rat osteoblast collagenase J. Bone Miner. Res. 8 1993 1247 1253
33. A.P. Oliveira, C.N. Lunardi, G.J. Rodrigues, and L.M. Bendhack Relaxation induced by calcium ionophore is impaired in carotid arteries from 2K-1C rats due to failed effect of nitric oxide on the smooth muscle cells Vasc. Pharmacol. 50 2009 153 159
34. G.J. Rodrigues, C.B. Restini, C.N. Lunardi, A. Neto Mdos, J.E. Moreira, and L.M. Bendhack Decreased number of caveolae in endothelial cells impairs the relaxation induced by acetylcholine in hypertensive rat aortas Eur. J. Pharmacol. 627 2009 251 257
35. Z. Li, J. Froehlich, Z.S. Galis, and E.G. Lakatta Increased expression of matrix metalloproteinase-2 in the thickened intima of aged rats Hypertension 33 1999 116 123
36. C. Fernandez-Patron, M.W. Radomski, and S.T. Davidge Vascular matrix metalloproteinase-2 cleaves big endothelin-1 yielding a novel vasoconstrictor Circ. Res. 85 1999 906 911
37. C. Fernandez-Patron, K.G. Stewart, Y. Zhang, E. Koivunen, M.W. Radomski, and S.T. Davidge Vascular matrix metalloproteinase-2-dependent cleavage of calcitonin gene-related peptide promotes vasoconstriction Circ. Res. 87 2000 670 676
38. A. Martinez, H.R. Oh, E.J. Unsworth, C. Bregonzio, J.M. Saavedra, W.G. Stetler-Stevenson, and F. Cuttitta Matrix metalloproteinase-2 cleavage of adrenomedullin produces a vasoconstrictor out of a vasodilator Biochem. J. 383 2004 413 418
39. A. Kladna, I. Kruk, T. Michalska, P. Berczynski, H.Y. Aboul-Enein, Characterization of the superoxide anion radical scavenging activity by tetracycline antibiotics in aprotic media, Luminescence (2011).
40. A.W. Chung, H.H. Yang, M.W. Radomski, and C. van Breemen Long-term doxycycline is more effective than atenolol to prevent thoracic aortic aneurysm in marfan syndrome through the inhibition of matrix metalloproteinase-2 and -9 Circ. Res. 102 2008 e73 e85
41. A.K. Prall, G.M. Longo, W.G. Mayhan, E.A. Waltke, B. Fleckten, R.W. Thompson, and B.T. Baxter Doxycycline in patients with abdominal aortic aneurysms and in mice. comparison of serum levels and effect on aneurysm growth in mice J. Vasc. Surg. 35 2002 923 929
42. N. Yaras, M. Sariahmetoglu, A. Bilginoglu, A. Aydemir-Koksoy, A. Onay-Besikci, B. Turan, and R. Schulz Protective action of doxycycline against diabetic cardiomyopathy in rats Br. J. Pharmacol. 155 2008 1174 1184
43. E.N. Zeydanli, H.B. Kandilci, and B. Turan Doxycycline ameliorates vascular endothelial and contractile dysfunction in the thoracic aorta of diabetic rats Cardiovasc. Toxicol. 11 2011 134 147
44. R. Schulz Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches Annu. Rev. Pharmacol. Toxicol. 47 2007 211 242
45. F. Valentin, J.L. Bueb, P. Kieffer, E. Tschirhart, and J. Atkinson Oxidative stress activates MMP-2 in cultured human coronary smooth muscle cells Fundam. Clin. Pharmacol. 19 2005 661 667
46. K. Grote, I. Flach, M. Luchtefeld, E. Akin, S.M. Holland, H. Drexler, and B. Schieffer Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species Circ. Res. 92 2003 e80 e86