Sex differences in the developmental programming of hypertension

Acta Physiologica

Volumn 210, Issue 2, 2014, Pages 307-316

  Ojeda, N B ^a,b   Intapad, S ^a   Alexander, B T ^a,b  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

Blood pressure; Endothelin; Oxidative stress; Renal nerves; Renin angiotensin system; Sex hormones

Indexed keywords

ENDOTHELIN; SEX HORMONE;

ADRENERGIC SYSTEM; BLOOD PRESSURE; BLOOD PRESSURE REGULATION; CARDIOVASCULAR RISK; DISEASE PREDISPOSITION; HUMAN; HYPERTENSION; NEPHRON; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; REGULATORY MECHANISM; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SEX DIFFERENCE; ANIMAL; EMBRYOLOGY; FEMALE; FETUS DEVELOPMENT; MALE; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; FEMALE; FETAL DEVELOPMENT; HUMANS; HYPERTENSION; MALE; SEX CHARACTERISTICS;

EID: 84892399569     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12206     Document Type: Review

References (75)

1. Alexander, B.T. 2003. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41, 457-462.
2. Alexander, B.T., Rinewalt, A.N., Cockrell, K.L., Massey, M.B., Bennett, W.A. & Granger, J.P. 2001. Endothelin type a receptor blockade attenuates the hypertension in response to chronic reductions in uterine perfusion pressure. Hypertension 37, 485-489.
3. Alexander, B.T., Hendon, A.E., Ferril, G. & Dwyer, T.M. 2005. Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension 45, 754-758.
4. Andersson, S.W., Lapidus, L., Niklasson, A., Hallberg, L., Bengtsson, C. & Hulthen, L. 2000. Blood pressure and hypertension in middle-aged women in relation to weight and length at birth: a follow-up study. J Hypertens 18, 1753-1761.
5. Barker, D.J. & Osmond, C. 1988. Low birth weight and hypertension. BMJ 297, 134-135.
6. Barker, D.J., Osmond, C., Golding, J., Kuh, D. & Wadsworth, M.E. 1989. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298, 564-567.
7. Basioti, M., Giapros, V., Kostoula, A., Cholevas, V. & Andronikou, S. 2009. Growth restriction at birth and kidney function during childhood. Am J Kidney Dis 54, 850-858.
8. Baum, M. 2010. Role of the kidney in the prenatal and early postnatal programming of hypertension. Am J Physiol Renal Physiol 298, F235-F247.
9. Bourque, S.L., Gragasin, F.S., Quon, A.L., Mansour, Y., Morton, J.S. & Davidge, S.T. 2013. Prenatal hypoxia causes long-term alterations in vascular endothelin-1 function in aged male, but not female, offspring. Hypertension 62, 753-758.
10. Brenner, B.M., Garcia, D.L. & Anderson, S. 1988. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1, 335-347.
11. Cerda, S. & Weitzman, S.A. 1997. Influence of oxygen radical injury on DNA methylation. Mutat Res 386, 141-152.
12. Chen, Y.F., Naftilan, A.J. & Oparil, S. 1992. Androgen-dependent angiotensinogen and renin messenger RNA expression in hypertensive rats. Hypertension 19, 456-463.
13. Chiavaroli, V., Giannini, C., D'Adamo, E., de Giorgis, T., Chiarelli, F. & Mohn, A. 2009. Insulin resistance and oxidative stress in children born small and large for gestational age. Pediatrics 124, 695-702.
14. Curhan, G.C., Chertow, G.M., Willett, W.C., Spiegelman, D., Colditz, G.A., Manson, J.E., Speizer, F.E. & Stampfer, M.J. 1996a. Birth weight and adult hypertension and obesity in women. Circulation 94, 1310-1315.
15. Curhan, G.C., Willett, W.C., Rimm, E.B., Spiegelman, D., Ascherio, A.L. & Stampfer, M.J. 1996b. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 94, 3246-3250.
16. David, F.L., Carvalho, M.H., Cobra, A.L., Nigro, D., Fortes, Z.B., Reboucas, N.A. & Tostes, R.C. 2001. Ovarian hormones modulate endothelin-1 vascular reactivity and mRNA expression in DOCA-salt hypertensive rats. Hypertension 38, 692-696.
17. Dennery, P.A. 2010. Oxidative stress in development: nature or nurture? Free Radic Biol Med 49, 1147-1151.
18. Fischer, M., Baessler, A. & Schunkert, H. 2002. Renin angiotensin system and gender differences in the cardiovascular system. Cardiovasc Res 53, 672-677.
19. Forsdahl, A. 1977. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prev Soc Med 31, 91-95.
20. Franco Mdo, C., Dantas, A.P., Akamine, E.H., Kawamoto, E.M., Fortes, Z.B., Scavone, C., Tostes, R.C., Carvalho, M.H. & Nigro, D. 2002. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. J Cardiovasc Pharmacol 40, 501-509.
21. Franco, M.C., Casarini, D.E., Carneiro-Ramos, M.S., Sawaya, A.L., Barreto-Chaves, M.L. & Sesso, R. 2008. Circulating renin-angiotensin system and catecholamines in childhood: is there a role for birthweight? Clin Sci (Lond) 114, 375-380.
22. Fyhrquist, F. & Saijonmaa, O. 2008. Renin-angiotensin system revisited. J Intern Med 264, 224-236.
23. Gamborg, M., Byberg, L., Rasmussen, F., Andersen, P.K., Baker, J.L., Bengtsson, C., Canoy, D., Droyvold, W., Eriksson, J.G., Forsen, T. et al. 2007. Birth weight and systolic blood pressure in adolescence and adulthood: meta-regression analysis of sex- and age-specific results from 20 Nordic studies. Am J Epidemiol 166, 634-645.
24. Gauster, M., Desoye, G., Totsch, M. & Hiden, U. 2012. The placenta and gestational diabetes mellitus. Curr Diab Rep 12, 16-23.
25. Gilbert, J.S., Ford, S.P., Lang, A.L., Pahl, L.R., Drumhiller, M.C., Babcock, S.A., Nathanielsz, P.W. & Nijland, M.J. 2007. Nutrient restriction impairs nephrogenesis in a gender-specific manner in the ovine fetus. Pediatr Res 61, 42-47.
26. Grigore, D., Ojeda, N.B., Robertson, E.B., Dawson, A.S., Huffman, C.A., Bourassa, E.A., Speth, R.C., Brosnihan, K.B. & Alexander, B.T. 2007. Placental insufficiency results in temporal alterations in the renin angiotensin system in male hypertensive growth restricted offspring. Am J Physiol Regul Integr Comp Physiol 293, R804-R811.
27. Guyton, A.C., Coleman, T.G., Cowley, A.V. Jr, Scheel, K.W., Manning, R.D. Jr & Norman, R.A. Jr 1972. Arterial pressure regulation. Overriding dominance of the kidneys in long-term regulation and in hypertension. Am J Med 52, 584-594.
28. Hallan, S., Euser, A.M., Irgens, L.M., Finken, M.J., Holmen, J. & Dekker, F.W. 2008. Effect of intrauterine growth restriction on kidney function at young adult age: the Nord Trondelag Health (HUNT 2) Study. Am J Kidney Dis 51, 10-20.
29. Hilliard, L.M., Sampson, A.K., Brown, R.D. & Denton, K.M. 2013. The "his and hers" of the renin-angiotensin system. Curr Hypertens Rep 15, 71-79.
30. Hitchler, M.J. & Domann, F.E. 2007. An epigenetic perspective on the free radical theory of development. Free Radic Biol Med 43, 1023-1036.
31. Hotoura, E., Argyropoulou, M., Papadopoulou, F., Giapros, V., Drougia, A., Nikolopoulos, P. & Andronikou, S. 2005. Kidney development in the first year of life in small-for-gestational-age preterm infants. Pediatr Radiol 35, 991-994.
32. Intapad, S., Tull, F.L., Brown, A.D., Dasinger, J.H., Ojeda, N.B., Fahling, J.M. & Alexander, B.T. 2013. Renal denervation abolishes the age-dependent increase in blood pressure in female intrauterine growth-restricted rats at 12 months of age. Hypertension 61, 828-834.
33. Jarvelin, M.R., Sovio, U., King, V., Lauren, L., Xu, B., McCarthy, M.I., Hartikainen, A.L., Laitinen, J., Zitting, P., Rantakallio, P. & Elliott, P. 2004. Early life factors and blood pressure at age 31 years in the 1966 northern Finland birth cohort. Hypertension 44, 838-846.
34. Jones, A., Beda, A., Osmond, C., Godfrey, K.M., Simpson, D.M. & Phillips, D.I. 2008. Sex-specific programming of cardiovascular physiology in children. Eur Heart J 29, 2164-2170.
35. Katkhuda, R., Peterson, E.S., Roghair, R.D., Norris, A.W., Scholz, T.D. & Segar, J.L. 2012. Sex-specific programming of hypertension in offspring of late-gestation diabetic rats. Pediatr Res 72, 352-361.
36. Kittikulsuth, W., Sullivan, J.C. & Pollock, D.M. 2013. ET-1 actions in the kidney: evidence for sex differences. Br J Pharmacol 168, 318-326.
37. Lawlor, D.A., Ebrahim, S. & Davey Smith, G. 2002. Is there a sex difference in the association between birth weight and systolic blood pressure in later life? Findings from a meta-regression analysis. Am J Epidemiol 156, 1100-1104.
38. Loria, A.S., Pollock, D.M. & Pollock, J.S. 2010. Early life stress sensitizes rats to angiotensin II-induced hypertension and vascular inflammation in adult life. Hypertension 55, 494-499.
39. Loria, A.S., Yamamoto, T., Pollock, D.M. & Pollock, J.S. 2013. Early life stress induces renal dysfunction in adult male rats but not female rats. Am J Physiol Regul Integr Comp Physiol 304, R121-R129.
40. Lukaszewski, M.A., Eberle, D., Vieau, D. & Breton, C. 2013. Nutritional manipulations in the perinatal period program adipose tissue in offspring. Am J Physiol Endocrinol Metab 305, E1195-E1207.
41. Manning, J. & Vehaskari, V.M. 2001. Low birth weight-associated adult hypertension in the rat. Pediatr Nephrol 16, 417-422.
42. Mehta, P.K. & Griendling, K.K. 2007. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292, C82-C97.
43. Minghetti, L., Greco, A., Zanardo, V. & Suppiej, A. 2013. Early-life sex-dependent vulnerability to oxidative stress: the natural twining model. J Matern Fetal Neonatal Med 26, 259-262.
44. Mitchell, E.K., Louey, S., Cock, M.L., Harding, R. & Black, M.J. 2004. Nephron endowment and filtration surface area in the kidney after growth restriction of fetal sheep. Pediatr Res 55, 769-773.
45. Montezano, A.C., Callera, G.E., Mota, A.L., Fortes, Z.B., Nigro, D., Carvalho, M.H., Zorn, T.M. & Tostes, R.C. 2005. Endothelin-1 contributes to the sexual differences in renal damage in DOCA-salt rats. Peptides 26, 1454-1462.
46. Moritz, K.M., Mazzuca, M.Q., Siebel, A.L., Mibus, A., Arena, D., Tare, M., Owens, J.A. & Wlodek, M.E. 2009. Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J Physiol 587, 2635-2646.
47. Moritz, K.M., Cuffe, J.S., Wilson, L.B., Dickinson, H., Wlodek, M.E., Simmons, D.G. & Denton, K.M. 2010. Review: sex specific programming: a critical role for the renal renin-angiotensin system. Placenta 31(Suppl), S40-S46.
48. Nathanielsz, P.W. 2006. Animal models that elucidate basic principles of the developmental origins of adult diseases. ILAR J 47, 73-82.
49. Ojeda, N.B., Grigore, D., Robertson, E.B. & Alexander, B.T. 2007a. Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension 50, 679-685.
50. Ojeda, N.B., Grigore, D., Yanes, L.L., Iliescu, R., Robertson, E.B., Zhang, H. & Alexander, B.T. 2007b. Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am J Physiol Regul Integr Comp Physiol 292, R758-R763.
51. Ojeda, N.B., Royals, T.P., Black, J.T., Dasinger, J.H., Johnson, J.M. & Alexander, B.T. 2010. Enhanced sensitivity to acute angiotensin II is testosterone dependent in adult male growth-restricted offspring. Am J Physiol Regul Integr Comp Physiol 298, R1421-R1427.
52. Ojeda, N.B., Intapad, S., Royals, T.P., Black, J.T., Dasinger, J.H., Tull, F.L. & Alexander, B.T. 2011. Hypersensitivity to acute ANG II in female growth-restricted offspring is exacerbated by ovariectomy. Am J Physiol Regul Integr Comp Physiol 301, R1199-R1205.
53. Ojeda, N.B., Hennington, B.S., Williamson, D.T., Hill, M.L., Betson, N.E., Sartori-Valinotti, J.C., Reckelhoff, J.F., Royals, T.P. & Alexander, B.T. 2012. Oxidative stress contributes to sex differences in blood pressure in adult growth-restricted offspring. Hypertension 60, 114-122.
54. Peuchant, E., Brun, J.L., Rigalleau, V., Dubourg, L., Thomas, M.J., Daniel, J.Y., Leng, J.J. & Gin, H. 2004. Oxidative and antioxidative status in pregnant women with either gestational or type 1 diabetes. Clin Biochem 37, 293-298.
55. Reckelhoff, J.F., Zhang, H. & Srivastava, K. 2000. Gender differences in development of hypertension in spontaneously hypertensive rats: role of the renin-angiotensin system. Hypertension 35, 480-483.
56. Richardson, L.J., Hussey, J.M. & Strutz, K.L. 2011. Origins of disparities in cardiovascular disease: birth weight, body mass index, and young adult systolic blood pressure in the national longitudinal study of adolescent health. Ann Epidemiol 21, 598-607.
57. Roberts, J.M. & Lain, K.Y. 2002. Recent Insights into the pathogenesis of pre-eclampsia. Placenta 23, 359-372.
58. Saez, F., Castells, M.T., Zuasti, A., Salazar, F., Reverte, V., Loria, A. & Salazar, F.J. 2007. Sex differences in the renal changes elicited by angiotensin II blockade during the nephrogenic period. Hypertension 49, 1429-1435.
59. Sandberg, K. & Ji, H. 2012. Sex differences in primary hypertension. Biol Sex Differ 3, 7.
60. da Silva, A.A., do Carmo, J.M. & Hall, J.E. 2013. Role of leptin and central nervous system melanocortins in obesity hypertension. Curr Opin Nephrol Hypertens 22, 135-140.
61. Singh, R.R., Denton, K.M., Bertram, J.F., Jefferies, A.J. & Moritz, K.M. 2010. Reduced nephron endowment due to fetal uninephrectomy impairs renal sodium handling in male sheep. Clin Sci (Lond) 118, 669-680.
62. Speed, J.S. & Pollock, D.M. 2013. Endothelin, kidney disease, and hypertension. Hypertension 61, 1142-1145.
63. Stewart, T., Jung, F.F., Manning, J. & Vehaskari, V.M. 2005. Kidney immune cell infiltration and oxidative stress contribute to prenatally programmed hypertension. Kidney Int 68, 2180-2188.
64. Tao, H., Rui, C., Zheng, J., Tang, J., Wu, L., Shi, A., Chen, N., He, R., Wu, C., Li, J. et al. 2013. Angiotensin II-mediated vascular changes in aged offspring rats exposed to perinatal nicotine. Peptides 44, 111-119.
65. Tarry-Adkins, J.L. & Ozanne, S.E. 2011. Mechanisms of early life programming: current knowledge and future directions. Am J Clin Nutr 94, 1765S-1771S.
66. Tufro-McReddie, A., Romano, L.M., Harris, J.M., Ferder, L. & Gomez, R.A. 1995. Angiotensin II regulates nephrogenesis and renal vascular development. Am J Physiol 269, F110-F115.
67. Wlodek, M.E., Westcott, K., Siebel, A.L., Owens, J.A. & Moritz, K.M. 2008. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int 74, 187-195.
68. Woods, L.L. & Rasch, R. 1998. Perinatal ANG II programs adult blood pressure, glomerular number, and renal function in rats. Am J Physiol 275, R1593-R1599.
69. Woods, L.L., Ingelfinger, J.R., Nyengaard, J.R. & Rasch, R. 2001. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 49, 460-467.
70. Woods, L.L., Ingelfinger, J.R. & Rasch, R. 2005. Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol 289, R1131-R1136.
71. Woods, L.L., Morgan, T.K. & Resko, J.A. 2010. Castration fails to prevent prenatally programmed hypertension in male rats. Am J Physiol Regul Integr Comp Physiol 298, R1111-R1116.
72. Xiao, D., Xu, Z., Huang, X., Longo, L.D., Yang, S. & Zhang, L. 2008. Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension 51, 1239-1247.
73. Xiao, D., Huang, X., Yang, S. & Zhang, L. 2011. Antenatal nicotine induces heightened oxidative stress and vascular dysfunction in rat offspring. Br J Pharmacol 164, 1400-1409.
74. Xiao, D., Huang, X., Yang, S. & Zhang, L. 2013. Estrogen normalizes perinatal nicotine-induced hypertensive responses in adult female rat offspring. Hypertension 61, 1246-1254.
75. Zandi-Nejad, K., Luyckx, V.A. & Brenner, B.M. 2006. Adult hypertension and kidney disease: the role of fetal programming. Hypertension 47, 502-508.