Testosterone induces leucocyte migration by NADPH oxidase-driven ROS- and COX2-dependent mechanisms

Clinical Science

Volumn 129, Issue 1, 2015, Pages 39-48

  Chignalia, Andreia Z ^a   Oliveira, Maria Aparecida ^a   Debbas, Victor ^a   Dull, Randal O ^b   Laurindo, Francisco R M ^a   Touyz, Rhian M ^c   Carvalho, Maria Helena C ^a   Fortes, Zuleica B ^a   Tostes, Rita C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Androgens; Cardiovascular risk; Inflammation; Leucocyte migration; Oxidative stress; Testosterone

Indexed keywords

APOCYNIN; CELL ADHESION MOLECULE; CYCLOOXYGENASE 2; FLUTAMIDE; HYDROETHIDINE; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SALICYLATE SODIUM; SODIUM CHLORIDE; TESTOSTERONE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE; ACETOPHENONE DERIVATIVE; ANDROGEN; ENZYME INHIBITOR; N-(2-CYCLOHEXYLOXY-4-NITROPHENYL)METHANESULFONAMIDE; NITROBENZENE DERIVATIVE; SULFONAMIDE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FLUORESCENCE; INTRAVITAL MICROSCOPY; LEUKOCYTE MIGRATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TESTOSTERONE BLOOD LEVEL; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL MOTION; CYTOLOGY; DRUG EFFECTS; INTRAPERITONEAL DRUG ADMINISTRATION; LEUKOCYTE; MESENTERIC VEIN; METABOLISM; PROCEDURES; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VIDEO MICROSCOPY; WESTERN BLOTTING; WISTAR RAT;

ACETOPHENONES; ANDROGENS; ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; CELLS, CULTURED; CYCLOOXYGENASE 2; ENZYME INHIBITORS; INJECTIONS, INTRAPERITONEAL; LEUKOCYTES; MALE; MESENTERIC VEINS; MICROSCOPY, VIDEO; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; NITROBENZENES; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SULFONAMIDES; SUPEROXIDES; TESTOSTERONE;

EID: 84937511683     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20140548     Document Type: Article

References (44)

1. Hyde, Z., Norman, P.E., Flicker, L., Hankey, G.J., Almeida, O.P., McCaul, K.A., Chubb, S.A. and Yeap, B.B. (2012) Low free testosterone predicts mortality from cardiovascular disease but not other causes: the health in men study. J. Clin. Endocrinol. Metab. 97, 179-189.
2. Ruige, J.B., Mahmoud, A.M., De Bacquer, D. and Kaufman, J.M. (2011) Endogenous testosterone and cardiovascular disease in healthy men: a meta-analysis. Heart 97, 870-875.
3. Basaria, S., Coviello, A.D., Travison, T.G., Storer, T.W., Farwell, W.R., Jette, A.M., Eder, R., Tennstedt, S., Ulloor, J., Zhang, A. et al. (2010) Adverse events associated with testosterone administration. N. Engl. J. Med. 363, 109-122.
4. Ziemens, B., Wallaschofski, H., Volzke, H., Rettig, R., Dorr, M., Nauck, M., Keevil, B.G., Brabant, G. and Haring, R. (2013) Positive association between testosterone, blood pressure, and hypertension in women: longitudinal findings from the study of health in pomerania. J. Hypertens. 31, 1106-1113.
5. Nahrendorf, M., Frantz, S., Hu, K., von zur Muhlen, C., Tomaszewski, M., Scheuermann, H., Kaiser, R., Jazbutyte, V., Beer, S., Bauer, W. et al. (2003) Effect of testosterone on post-myocardial infarction remodeling and function. Cardiovasc Res. 57, 370-378.
6. Ammar, E.M., Said, S.A. and Hassan, M.S. (2004) Enhanced vasoconstriction and reduced vasorelaxation induced by testosterone and nandrolone in hypercholesterolemic rabbits. Pharmacol. Res. 50, 253-259.
7. Barton, M., Prossnitz, E.R. and Meyer, M.R. (2012) Testosterone and secondary hypertension: new pieces to the puzzle. Hypertension 59, 1101-1103.
8. Heistad, D.D., Wakisaka, Y., Miller, J., Chu, Y. and Pena-Silva, R. (2009) Novel aspects of oxidative stress in cardiovascular diseases. Circ. J. 73, 201-207.
9. Chignalia, A.Z., Schuldt, E.Z., Camargo, L.L., Montezano, A.C., Callera, G.E., Laurindo, F.R., Lopes, L.R., Avellar, M.C., Carvalho, M.H., Fortes, Z.B. et al. (2012) Testosterone induces vascular smooth muscle cell migration by NADPH oxidase and c-Src-dependent pathways. Hypertension 59, 1263-1271.
10. Hopkins, P.N. (2013) Molecular biology of atherosclerosis. Physiol. Rev. 93, 1317-1542.
11. Cook-Mills, J.M. (2006) Hydrogen peroxide activation of endothelial cell-associated MMPs during VCAM-1-dependent leukocyte migration. Cell. Mol. Biol. 52, 8-16.
12. Jalkanen, S., Karikoski, M., Mercier, N., Koskinen, K., Henttinen, T., Elima, K., Salmivirta, K. and Salmi, M. (2007) The oxidase activity of vascular adhesion protein-1 (VAP-1) induces endothelial E-and P-selectins and leukocyte binding. Blood 110, 1864-1870.
13. Filgueira, F.P., Lobato, N.S., DosSantos, R.A., Oliveira, M.A., Akamine, E.H., Tostes, R.C., Fortes, Z.B. and Carvalho, M.H. (2012) Endogenous testosterone increases leukocyte-endothelial cell interaction in spontaneously hypertensive rats. Life Sci. 90, 689-694.
14. Ganesan, K., Balachandran, C., Manohar, B.M. and Puvanakrishnan, R. (2012) Effects of testosterone, estrogen and progesterone on TNF-α mediated cellular damage in rat arthritic synovial fibroblasts. Rheumatol. Int. 32, 3181-3188.
15. Yue, T.L. and Varma, D.R. (1982) Pharmacokinetics, metabolism and disposition of salicylate in protein-deficient rats. Drug. Metab. Dispos. 10, 147-152.
16. Fortes, Z.B., Farsky, S.P., Oliveira, M.A. and Garcia-Leme, J. (1991) Direct vital microscopic study of defective leukocyte-endothelial interaction in diabetes mellitus. Diabetes 40, 1267-1273.
17. Fernandes, D.C., Wosniak, Jr, J., Pescatore, L.A., Bertoline, M.A., Liberman, M., Laurindo, F.R. and Santos, C.X. (2007) Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems. Am. J. Physiol. Cell Physiol. 292, C413-C422.
18. Touyz, R.M., Wu, X.H., He, G., Park, J.B., Chen, X., Vacher, J., Rajapurohitam, V. and Schiffrin, E.L. (2001) Role of c-Src in the regulation of vascular contraction and Ca2+ signaling by angiotensin II in human vascular smooth muscle cells. J. Hypertens 19, 441-449.
19. Callera, G.E., Montezano, A.C., Yogi, A., Tostes, R.C., He, Y., Schiffrin, E.L. and Touyz, R.M. (2005) c-Src-dependent nongenomic signaling responses to aldosterone are increased in vascular myocytes from spontaneously hypertensive rats. Hypertension 46, 1032-1038.
20. Kvietys, P.R. and Granger, D.N. (2012) Role of reactive oxygen and nitrogen species in the vascular responses to inflammation. Free Radic Biol. Med. 52, 556-592.
21. Kim, G.Y., Lee, J.W., Ryu, H.C., Wei, J.D., Seong, C.M. and Kim, J.H. (2010) Proinflammatory cytokine IL-1beta stimulates IL-8 synthesis in mast cells via a leukotriene B4 receptor 2-linked pathway, contributing to angiogenesis. J. Immunol. 184, 3946-3954.
22. Park, H.S., Chun, J.N., Jung, H.Y., Choi, C. and Bae, Y.S. (2006) Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells. Cardiovasc. Res. 72, 447-455.
23. Swindle, E.J. and Metcalfe, D.D. (2007) The role of reactive oxygen species and nitric oxide in mast cell-dependent inflammatory processes. Immunol. Rev. 217, 186-205.
24. Paul-Clark, M.J., McMaster, S.K., Sorrentino, R., Sriskandan, S., Bailey, L.K., Moreno, L., Ryffel, B., Quesniaux, V.F. and Mitchell, J.A. (2009) Toll-like receptor 2 is essential for the sensing of oxidants during inflammation. Am. J. Respir. Crit. Care Med. 179, 299-306.
25. Chao, T.C., Van Alten, P.J. and Walter, R.J. (1994) Steroid sex hormones and macrophage function: modulation of reactive oxygen intermediates and nitrite release. Am. J. Reprod. Immunol. 32, 43-52.
26. Mohan, P.F. and Jacobson, M.S. (1993) Inhibition of macrophage superoxide generation by dehydroepiandrosterone. Am. J. Med. Sci. 306, 10-15.
27. Juliet, P.A., Hayashi, T., Daigo, S., Matsui-Hirai, H., Miyazaki, A., Fukatsu, A., Funami, J., Iguchi, A. and Ignarro, L.J. (2004) Combined effect of testosterone and apocynin on nitric oxide and superoxide production in PMA-differentiated THP-1 cells. Biochim. Biophys. Acta 1693, 185-191.
28. Makarenko, V.V., Usatyuk, P.V., Yuan, G., Lee, M.M., Nanduri, J., Natarajan, V., Kumar, G.K. and Prabhakar, N.R. (2014) Intermittent hypoxia-induced endothelial barrier dysfunction requires ROS-dependent MAP kinase activation. Am. J. Physiol. Cell. Physiol. 306, C745-C752.
29. Butcher, E.C. (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67, 1033-1036.
30. Springer, T.A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76, 301-314.
31. Alvarez, A., Cerda-Nicolas, M., Naim Abu Nabah, Y., Mata, M., Issekutz, A.C., Panes, J., Lobb, R.R. and Sanz, M.J. (2004) Direct evidence of leukocyte adhesion in arterioles by angiotensin II. Blood 104, 402-408.
32. Chang, M.C., Lin, L.D., Zwei-Ching Chang, J., Huang, C.F., Chuang, F.H., Lee, J.J., Jeng, P.Y., Wang, T.M. and Jeng, J.H. (2012) Regulation of vascular cell adhesion molecule-1 in dental pulp cells by interleukin-1β: the role of prostanoids. J. Endod. 38, 774-779.
33. Lee, S., Felts, K.A., Parry, G.C., Armacost, L.M. and Cobb, R.R. (1997) Inhibition of 5-lipoxygenase blocks IL-1 beta-induced vascular adhesion molecule-1 gene expression in human endothelial cells. J. Immunol. 158, 3401-3407.
34. Amalfi, S., Velez, L.M., Heber, M.F., Vighi, S., Ferreira, S.R., Orozco, A.V., Pignataro, O. and Motta, A.B. (2012) Prenatal hyperandrogenization induces metabolic and endocrine alterations which depend on the levels of testosterone exposure. PLoS One 7, e37658.
35. Wang, X., Shen, C.L., Dyson, M.T., Eimerl, S., Orly, J., Hutson, J.C. and Stocco, D.M. (2005) Cyclooxygenase-2 regulation of the age-related decline in testosterone biosynthesis. Endocrinology 146, 4202-4208.
36. de Menezes, G.B., dos Reis, W.G., Santos, J.M., Duarte, I.D. and de Francischi, J.N. (2005) Inhibition of prostaglandin F(2alpha) by selective cyclooxygenase 2 inhibitors accounts for reduced rat leukocyte migration. Inflammation 29, 163-169.
37. Choi, S.H., Aid, S., Choi, U. and Bosetti, F. (2010) Cyclooxygenases-1 and-2 differentially modulate leukocyte recruitment into the inflamed brain. Pharmacogenomics J 10, 448-457.
38. Menezes, G.B., Rezende, R.M., Pereira-Silva, P.E., Klein, A., Cara, D.C. and Francischi, J.N. (2008) Differential involvement of cyclooxygenase isoforms in neutrophil migration in vivo and in vitro. Eur. J. Pharmacol. 598, 118-122.
39. Asako, H., Kubes, P., Wallace, J., Wolf, R.E. and Granger, D.N. (1992) Modulation of leukocyte adhesion in rat mesenteric venules by aspirin and salicylate. Gastroenterology 103, 146-152.
40. Martinez-Revelles, S., Avendano, M.S., Garcia-Redondo, A.B., Alvarez, Y., Aguado, A., Perez-Giron, J.V., Garcia-Redondo, L., Esteban, V., Redondo, J.M., Alonso, M.J. et al. (2013) Reciprocal relationship between reactive oxygen species and cyclooxygenase-2 and vascular dysfunction in hypertension. Antioxid. Redox Signal. 18, 51-65.
41. Furst, S.M., Khan, K.N., Komocsar, W.J., Fan, L. and Mennear, J. (2005) Screening new drugs for immunotoxic potential: II. Assessment of the effects of selective and nonselective COX-2 inhibitors on complement activation, superoxide anion production and leukocyte chemotaxis and migration through endothelial cells. J. Immunotoxicol. 2, 85-96.
42. Meyer, M.R., Haas, E. and Barton, M. (2006) Gender differences of cardiovascular disease: new perspectives for estrogen receptor signaling. Hypertension 47, 1019-1026.
43. Ghorashi, V. and Sheikhvatan, M. (2008) The relationship between serum concentration of free testosterone and pre-eclampsia. Endokrynol. Pol. 59, 390-392.
44. Szydlarska, D., Grzesiuk, W., Kondracka, A., Bartoszewicz, Z. and Bar-Andziak, E. (2012) Measuring salivary androgens as a useful tool in the diagnosis of polycystic ovary syndrome. Endokrynol. Pol. 63, 183-190.