Oxidative stress contributes to sex differences in blood pressure in adult growth-restricted offspring

Hypertension

Volumn 60, Issue 1, 2012, Pages 114-122

  Ojeda, Norma B ^a,b   Hennington, Bettye Sue ^b,c   Williamson, Danielle T ^c   Hill, Melanie L ^c   Betson, Nicole E E ^c   Sartori Valinotti, Julio C ^a   Reckelhoff, Jane F ^a,b   Royals, Thomas P ^a   Alexander, Barbara T ^a,b  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

^c TOUGALOO COLLEGE   (United States)

Author keywords

Antioxidant; Blood pressure; Intrauterine growth restriction

Indexed keywords

BIOLOGICAL MARKER; CATALASE; GLUTATHIONE PEROXIDASE; SUPEROXIDE DISMUTASE; TEMPOL; AMINE OXIDE; ANTIOXIDANT; SUPEROXIDE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD PRESSURE; BLOOD PRESSURE MEASUREMENT; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GROWTH RETARDATION; HYPERTENSION; KIDNEY; KIDNEY FUNCTION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; TELEMETRY; ANIMAL; DRUG EFFECT; INTRAUTERINE GROWTH RETARDATION; METABOLISM; METHODOLOGY; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; SPIN LABELING; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; BLOOD PRESSURE; BLOOD PRESSURE DETERMINATION; CATALASE; CYCLIC N-OXIDES; FEMALE; FETAL GROWTH RETARDATION; GLUTATHIONE PEROXIDASE; HYPERTENSION; KIDNEY; MALE; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SPIN LABELS; SUPEROXIDE DISMUTASE; SUPEROXIDES; TELEMETRY;

EID: 84865824983     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.112.192955     Document Type: Article

References (49)

1. Ergaz Z, Avgil M, Ornoy A. Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? Reprod Toxicol. 2005;20:301-322.
2. Barker DJ. In utero programming of chronic disease. Clin Sci (Lond). 1998;95:115-128.
3. Ojeda NB, Grigore D, Alexander BT. Developmental programming of hypertension: insight from animal models of nutritional manipulation. Hypertension. 2008;52:44-50.
4. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298:564-567.
5. Mohan Kumar SM, King A, Shin AC, Sirivelu MP, Mohan Kumar PS, Fink GD. Developmental programming of cardiovascular disorders: focus on hypertension. Rev Endocr Metab Disord. 2007;8:115-125.
6. Dagan A, Kwon HM, Dwarakanath V, Baum M. Effect of renal denervation on prenatal programming of hypertension and renal tubular transporter abundance. Am J Physiol Renal Physiol. 2008;295:F29-F34.
7. Alexander BT, Hendon AE, Ferril G, Dwyer TM. Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension. 2005;45:754-758.
8. Rasch R, Skriver E, Woods LL. The role of the RAS in programming of adult hypertension. Acta Physiol Scand. 2004;181:537-542.
9. Ojeda NB, Grigore D, Yanes LL, Iliescu R, Robertson EB, Zhang H, Alexander BT. Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am J Physiol Regul Integr Comp Physiol. 2007;292:R758-R763.
10. Stewart T, Jung FF, Manning J, Vehaskari VM. Kidney immune cell infiltration and oxidative stress contribute to prenatally programmed hypertension. Kidney Int. 2005;68:2180-2188.
11. Franco Mdo C, Dantas AP, Akamine EH, Kawamoto EM, Fortes ZB, Scavone C, Tostes RC, Carvalho MH, Nigro D. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. J Cardiovasc Pharmacol. 2002;40:501-509.
12. Reckelhoff JF. Gender differences in the regulation of blood pressure. Hypertension. 2001;37:1199-1208.
13. Davies AA, Smith GD, May MT, Ben-Shlomo Y. Association between birth weight and blood pressure is robust, amplifies with age, and may be underestimated. Hypertension. 2006;48:431-436.
14. Jarvelin MR, Sovio U, King V, Lauren L, Xu B, McCarthy MI, Hartikainen AL, Laitinen J, Zitting P, Rantakallio P, Elliott P. Early life factors and blood pressure at age 31 years in the 1966 northern Finland birth cohort. Hypertension. 2004;44:838-846.
15. Jones A, Beda A, Osmond C, Godfrey KM, Simpson DM, Phillips DI. Sex-specific programming of cardiovascular physiology in children. Eur Heart J. 2008;29:2164-2170.
16. Hallan S, Euser AM, Irgens LM, Finken MJ, Holmen J, Dekker FW. Effect of intrauterine growth restriction on kidney function at young adult age: the Nord Trondelag Health (HUNT 2) Study. Am J Kidney Dis. 2008;51:10-20.
17. Andersson SW, Lapidus L, Niklasson A, Hallberg L, Bengtsson C, Hulthen L. Blood pressure and hypertension in middle-aged women in relation to weight and length at birth: a follow-up study. J Hypertens. 2000;18:1753-1761.
18. Alexander BT. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension. 2003;41:457-462.
19. Ojeda NB, Johnson WR, Dwyer TM, Alexander BT. Early renal denervation prevents development of hypertension in growth-restricted offspring. Clin Exp Pharmacol Physiol. 2007;34:1212-1216.
20. Briones AM, Touyz RM. Oxidative stress and hypertension: current concepts. Curr Hypertens Rep. 2010;12:135-142.
21. Park JB, Touyz RM, Chen X, Schiffrin EL. Chronic treatment with a superoxide dismutase mimetic prevents vascular remodeling and progression of hypertension in salt-loaded stroke-prone spontaneously hypertensive rats. Am J Hypertens. 2002;15:78-84.
22. Dobrian AD, Davies MJ, Schriver SD, Lauterio TJ, Prewitt RL. Oxidative stress in a rat model of obesity-induced hypertension. Hypertension. 2001;37:554-560.
23. Lopez-Ruiz A, Sartori-Valinotti J, Yanes LL, Iliescu R, Reckelhoff JF. Sex differences in control of blood pressure: role of oxidative stress in hypertension in females. Am J Physiol Heart Circ Physiol. 2008;295:H466-H474.
24. Moritz KM, Mazzuca MQ, Siebel AL, Mibus A, Arena D, Tare M, Owens JA, Wlodek ME. Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J Physiol. 2009;587:2635-2646.
25. Wlodek ME, Westcott K, Siebel AL, Owens JA, Moritz KM. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008;74:187-195.
26. Woods LL, Ingelfinger JR, Rasch R. Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol. 2005;289:R1131-R1136.
27. Roghair RD, Segar JL, Volk KA, Chapleau MW, Dallas LM, Sorenson AR, Scholz TD, Lamb FS. Vascular nitric oxide and superoxide anion contribute to sex-specific programmed cardiovascular physiology in mice. Am J Physiol Regul Integr Comp Physiol. 2009;296:R651-R662.
28. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-Iso prostaglandin f2α Hypertension. 1999;33:424-428.
29. Sartori-Valinotti JC, Iliescu R, Yanes LL, Dorsett-Martin W, Reckelhoff JF. Sex differences in the pressor response to angiotensin II when the endogenous renin-angiotensin system is blocked. Hypertension. 2008;51:1170-1176.
30. Touyz RM. Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance? Hypertension. 2004;44:248-252.
31. Wilcox CS. Reactive oxygen species: roles in blood pressure and kidney function. Curr Hypertens Rep. 2002;4:160-166.
32. Iliescu R, Cucchiarelli VE, Yanes LL, Iles JW, Reckelhoff JF. Impact of androgen-induced oxidative stress on hypertension in male SHR. Am J Physiol Regul Integr Comp Physiol. 2007;292:R731-R735.
33. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G. Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc Biol Sci. 2007;274:819-825.
34. Dantas AP, Franco Mdo C, Silva-Antonialli MM, Tostes RC, Fortes ZB, Nigro D, Carvalho MH. Gender differences in superoxide generation in microvessels of hypertensive rats: role of NAD (P) H-oxidase. Cardiovasc Res. 2004;61:22-29.
35. Ojeda NB, Grigore D, Robertson EB, Alexander BT. Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension. 2007;50:679-685.
36. Bureau I, Gueux E, Mazur A, Rock E, Roussel AM, Rayssiguier Y. Female rats are protected against oxidative stress during copper deficiency. J Am Coll Nutr. 2003;22:239-246.
37. Busserolles J, Mazur A, Gueux E, Rock E, Rayssiguier Y. Metabolic syndrome in the rat: females are protected against the pro-oxidant effect of a high sucrose diet. Exp Biol Med (Maywood). 2002;227:837-842.
38. Katalinic V, Modun D, Music I, Boban M. Gender differences in antioxidant capacity of rat tissues determined by 2, 2=-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp Biochem Physiol C Toxicol Pharmacol. 2005;140:47-52.
39. Azevedo RB, Lacava ZG, Miyasaka CK, Chaves SB, Curi R. Regulation of antioxidant enzyme activities in male and female rat macrophages by sex steroids. Braz J Med Biol Res. 2001;34:683-687.
40. Zhou X, Smith AM, Failla ML. Estrogen status alters tissue distribution or oral dose of 76 Se-selenite and liver mRNA levels of SelP and GPx[abstract]. FASEB J. 2007;21:696-A6.
41. Rush JW, Sandiford SD. Plasma glutathione peroxidase in healthy young adults: influence of gender and physical activity. Clin Biochem. 2003;36:345-351.
42. Godin N, Liu F, Lau GJ, Brezniceanu ML, Chenier I, Filep JG, Ingelfinger JR, Zhang SL, Chan JS. Catalase overexpression prevents hypertension and tubular apoptosis in angiotensinogen transgenic mice. Kidney Int. 2010;77:1086-1097.
43. Campese VM, Ye S, Zhong H, Yanamadala V, Ye Z, Chiu J. Reactive oxygen species stimulate central and peripheral sympathetic nervous system activity. Am J Physiol Heart Circ Physiol. 2004;287:H695-H703.
44. Xu H, Fink GD, Galligan JJ. Tempol lowers blood pressure and sympathetic nerve activity but not vascular O2-in DOCA-salt rats. Hypertension. 2004;43:329-334.
45. Wei SG, Zhang ZH, Yu Y, Felder RB. Systemically administered tempol reduces neuronal activity in paraventricular nucleus of hypothalamus and rostral ventrolateral medulla in rats. J Hypertens. 2009;27:543-550.
46. Shokoji T, Nishiyama A, Fujisawa Y, Hitomi H, Kiyomoto H, Takahashi N, Kimura S, Kohno M, Abe Y. Renal sympathetic nerve responses to tempol in spontaneously hypertensive rats. Hypertension. 2003;41:266-273.
47. Roson MI, Della Penna SL, Cao G, Gorzalczany S, Pandolfo M, Toblli JE, Fernandez BE. Different protective actions of losartan and tempol on the renal inflammatory response to acute sodium overload. J Cell Physiol. 2010;224:41-48.
48. Pinaud F, Loufrani L, Toutain B, Lambert D, Vandekerckhove L, Henrion D, Baufreton C. In vitro protection of vascular function from oxidative stress and inflammation by pulsatility in resistance arteries. J Thorac Cardiovasc Surg. 2011;142:1254-1262.
49. Grigore D, Ojeda N, La Marca BB, Alexander BT. Inflammatory cytokines are elevated in intrauterine growth restricted offspring in response to placental insufficiency[abstract]. FASEB J. 2008;22:923-A6.