Female SHR have greater blood pressure sensitivity and renal T cell infiltration following chronic NOS inhibition than males

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 7, 2013, Pages

  Brinson, Krystal N ^a   Elmarakby, Ahmed A ^a,b   Tipton, Ashlee J ^a   Ryan Crislip, G ^a   Yamamoto, Tatsuo ^c   Baban, Babak ^b   Sullivan, Jennifer C ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b AUGUSTA UNIVERSITY   (United States)

^c Numazu City Hospital   (Japan)

Author keywords

Hypertension; Inflammation; Kidney injury; Nitric oxide synthase; Sex

Indexed keywords

CELL ADHESION MOLECULE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CELL INFILTRATION; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; HYPERTENSION; IMMUNITY; INFLAMMATION; KIDNEY CORTEX; KIDNEY INJURY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY T LYMPHOCYTE; SEX DIFFERENCE; SPONTANEOUSLY HYPERTENSIVE RAT; T LYMPHOCYTE; TH17 CELL;

HYPERTENSION; INFLAMMATION; KIDNEY INJURY; NITRIC OXIDE SYNTHASE; SEX;

ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; CELL ADHESION MOLECULES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG THERAPY, COMBINATION; ENZYME INHIBITORS; FEMALE; HYPERTENSION; INFLAMMATION; KIDNEY; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RATS; RATS, INBRED SHR; SEX FACTORS; T-LYMPHOCYTES; TIME FACTORS;

EID: 84884941427     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00226.2013     Document Type: Article

References (39)

1. Baban B, Chandler PR, Johnson BA, 3rd, Huang L, Li M, Sharpe ML, Francisco LM, Sharpe AH, Blazar BR, Munn DH, Mellor AL. Physiologic control of IDO competence in splenic dendritic cells. J Immunol 187: 2329-2335, 2011.
2. Barhoumi T, Kasal DA, Li MW, Shbat L, Laurant P, Neves MF, Paradis P, Schiffrin EL. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 57: 469-476, 2011.
3. Baylis C. Nitric oxide deficiency in chronic kidney disease. Am J Physiol Renal Physiol 294: F1-F9, 2008.
4. Baylis C, Mitruka B, Deng A. Chronic blockade of nitric oxide synthesis in the rat produces systemic hypertension and glomerular damage. J Clin Invest 90: 278-281, 1992.
5. Benter IF, Yousif MH, Anim JT, Cojocel C, Diz DI. Angiotensin-(1-7) prevents development of severe hypertension and end-organ damage in spontaneously hypertensive rats treated with L-NAME. Am J Physiol Heart Circ Physiol 290: H684-H691, 2006.
6. Chen C, Mobley JL, Dwir O, Shimron F, Grabovsky V, Lobb RR, Shimizu Y, Alon R. High affinity very late antigen-4 subsets expressed on T cells are mandatory for spontaneous adhesion strengthening but not for rolling on VCAM-1 in shear flow. J Immunol 162: 1084-1095, 1999.
7. Cheng S, Xanthakis V, Sullivan LM, Vasan RS. Blood pressure tracking over the adult life course: patterns and correlates in the framingham heart study. Hypertension 60: 1393-1399, 2012.
8. Chogle AR, Chakravarty A. Cardiovascular events in systemic lupus erythematosus and rheumatoid arthritis: emerging concepts, early diagnosis and management. J Assoc Physicians India 55: 32-40, 2007.
9. De Caterina R, Libby P, Peng HB, Thannickal VJ, Rajavashisth TB, Gimbrone MA, Jr, Shin WS, Liao JK. Nitric oxide decreases cytokineinduced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest 96: 60-68, 1995.
10. De Miguel C, Guo C, Lund H, Feng D, Mattson DL. Infiltrating T lymphocytes in the kidney increase oxidative stress and participate in the development of hypertension and renal disease. Am J Physiol Renal Physiol 300: F734-F742, 2011.
11. Forte P, Kneale BJ, Milne E, Chowienczyk PJ, Johnston A, Benjamin N, Ritter JM. Evidence for a difference in nitric oxide biosynthesis between healthy women and men. Hypertension 32: 730-734, 1998.
12. Fujihara CK, Avancini Costa, Malheiros DM, de Lourdes Noronha II, De Nucci G, Zatz R. Mycophenolate mofetil reduces renal injury in the chronic nitric oxide synthase inhibition model. Hypertension 37: 170-175, 2001.
13. Gamboa A, Shibao C, Diedrich A, Choi L, Pohar B, Jordan J, Paranjape S, Farley G, Biaggioni I. Contribution of endothelial nitric oxide to blood pressure in humans. Hypertension 49: 170-177, 2007.
14. Glushkovskaya-Semyachkina OV, Anishchenko TG, Sindyakova TA, Leksina OV, Berdnikova VA. Sex-related differences in nitric oxide content in healthy and hypertensive rats at rest and under stress conditions. Bull Exp Biol Med 142: 9-11, 2006.
15. Harrison CB, Drummond GR, Sobey CG, Selemidis S. Evidence that nitric oxide inhibits vascular inflammation and superoxide production via a p47phox-dependent mechanism in mice. Clin Exp Pharmacol Physiol 37: 429-434, 2010.
16. Harrison DG, Guzik TJ, Lob HE, Madhur MS, Marvar PJ, Thabet SR, Vinh A, Weyand CM. Inflammation, immunity, and hypertension. Hypertension 57: 132-140, 2011.
17. Hsieh NK, Wang JY, Liu JC, Wang SD, Chen HI. Nitric oxide inhibition accelerates hypertension and induces perivascular inflammation in rats. Clin Exp Pharmacol Physiol 31: 212-218, 2004.
18. Ikeda H, Tsuruya K, Toyonaga J, Masutani K, Hayashida H, Hirakata H, Iida M. Spironolactone suppresses inflammation and prevents L-NAME-induced renal injury in rats. Kidney Int 75: 147-155, 2009.
19. Kamari Y, Peleg E, Leibowitz A, Grossman E. Blunted blood pressure response and elevated plasma adiponectin levels in female Sprague Dawley rats. Am J Hypertens 25: 612-619, 2012.
20. Kang KT, Sullivan JC, Spradley FT, d'Uscio LV, Katusic ZS, Pollock JS. Antihypertensive therapy increases tetrahydrobiopterin levels and NO/cGMP signaling in small arteries of angiotensin II-infused hypertensive rats. Am J Physiol Heart Circ Physiol 300: H718-H724, 2011.
21. Koeners MP, van Faassen EE, Wesseling S, de Sain-van der Velden M, Koomans HA, Braam B, Joles JA. Maternal supplementation with citrulline increases renal nitric oxide in young spontaneously hypertensive rats and has long-term antihypertensive effects. Hypertension 50: 1077-1084, 2007.
22. Madhur MS, Lob HE, McCann LA, Iwakura Y, Blinder Y, Guzik TJ, Harrison DG. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 55: 500-507, 2010.
23. Majmudar NG, Robson SC, Ford GA. Effects of the menopause, gender, and estrogen replacement therapy on vascular nitric oxide activity. J Clin Endocrinol Metab 85: 1577-1583, 2000.
24. Ono H, Ono Y, Takanohashi A, Matsuoka H, Frohlich ED. Apoptosis and glomerular injury after prolonged nitric oxide synthase inhibition in spontaneously hypertensive rats. Hypertension 38: 1300-1306, 2001.
25. Pober JS, Doukas J, Hughes CC, Savage CO, Munro JM, Cotran RS. The potential roles of vascular endothelium in immune reactions. Hum Immunol 28: 258-262, 1990.
26. Quiroz Y, Pons H, Gordon KL, Rincon J, Chavez M, Parra G, Herrera-Acosta J, Gomez-Garre D, Largo R, Egido J, Johnson RJ, Rodriguez-Iturbe B. Mycophenolate mofetil prevents salt-sensitive hypertension resulting from nitric oxide synthesis inhibition. Am J Physiol Renal Physiol 281: F38-F47, 2001.
27. Reckelhoff JF, Zhang H, Srivastava K. Gender differences in development of hypertension in spontaneously hypertensive rats: role of the renin-angiotensin system. Hypertension 35: 480-483, 2000.
28. Renkonen R, Turunen JP, Rapola J, Hayry P. Characterization of high endothelial-like properties of peritubular capillary endothelium during acute renal allograft rejection. Am J Pathol 137: 643-651, 1990.
29. Rodrigues SF, de Oliveira MA, dos Santos RA, Soares AG, de Cassia Tostes R, Carvalho MH, Fortes ZB. Hydralazine reduces leukocyte migration through different mechanisms in spontaneously hypertensive and normotensive rats. Eur J Pharmacol 589: 206-214, 2008.
30. Sainz J, Osuna A, Wangensteen R, de Dios Luna J, Rodriguez-Gomez I, Duarte J, Moreno JM, andVargas F. Role of sex, gonadectomy and sex hormones in the development of nitric oxide inhibition-induced hypertension. Exp Physiol 89: 155-162, 2004.
31. Sullivan JC, Bhatia K, Yamamoto T, Elmarakby AA. Angiotensin (1-7) receptor antagonism equalizes angiotensin II-induced hypertension in male and female spontaneously hypertensive rats. Hypertension 56: 658-666, 2010.
32. Sullivan JC, Pardieck JL, Hyndman KA, Pollock JS. Renal NOS activity, expression, and localization in male and female spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 298: R61-R69, 2010.
33. Sullivan JC, Semprun-Prieto L, Boesen EI, Pollock DM, Pollock JS. Sex and sex hormones influence the development of albuminuria and renal macrophage infiltration in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 293: R1573-R1579, 2007.
34. Tipton AJ, Baban B, Sullivan JC. Female spontaneously hypertensive rats have greater renal anti-inflammatory T lymphocyte infiltration than males. Am J Physiol Regul Integr Comp Physiol 303: R359-R367, 2012.
35. Verhagen AM, Attia DM, Koomans HA, Joles JA. Male gender increases sensitivity to proteinuria induced by mild NOS inhibition in rats: role of sex hormones. Am J Physiol Renal Physiol 279: F664-F670, 2000.
36. Wang YR, Yen CH, Sun YF, Laun YT. Gender-dependent response in blood pressure changes following the inhibition of nitric oxide synthase. Chin J Physiol 46: 91-94, 2003.
37. Whitacre CC. Sex differences in autoimmune disease. Nature Immunol 2: 777-780, 2001.
38. Wu Y, Huang A, Sun D, Falck JR, Koller A, Kaley G. Gender-specific compensation for the lack of NO in the mediation of flow-induced arteriolar dilation. Am J Physiol Heart Circ Physiol 280: H2456-H2461, 2001.
39. Wuthrich RP. Vascular cell adhesion molecule-1 (VCAM-1) expression in murine lupus nephritis. Kidney Int 42: 903-914, 1992.