Exercise training attenuates placental ischemia-induced hypertension and angiogenic imbalance in the rat

Hypertension

Volumn 60, Issue 6, 2012, Pages 1545-1551

  Gilbert, Jeffrey S ^a,b   Banek, Christopher T ^a,b   Bauer, Ashley J ^a   Gingery, Anne ^a,c   Needham, Karen ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF OREGON   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

blood pressure; preeclampsia; pregnancy; vascular endothelial growth factor A

Indexed keywords

PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TROLOX C; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

AMNION FLUID; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; EXERCISE; FEMALE; HEART MUSCLE ISCHEMIA; HYPERTENSION; NONHUMAN; OXIDATIVE STRESS; PLACENTA; PLACENTA PERFUSION; PREGNANCY; PRIORITY JOURNAL; RAT; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BLOOD PRESSURE; EXERCISE THERAPY; FEMALE; HYPERTENSION; ISCHEMIA; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; PLACENTA; PREGNANCY; PROCOLLAGEN-PROLINE DIOXYGENASE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; UTERUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84870243564     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.112.202275     Document Type: Article

References (37)

1. Rana S, Powe CE, Salahuddin S, Verlohren S, Perschel FH, Levine RJ, Lim KH, Wenger JB, Thadhani R, Karumanchi SA. Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia. Circulation. 2012;125:911-919.
2. Raijmakers MT, Dechend R, Poston L. Oxidative stress and preeclampsia: rationale for antioxidant clinical trials. Hypertension. 2004;44:374-380.
3. LaMarca BD, Gilbert J, Granger JP. Recent progress toward the understanding of the pathophysiology of hypertension during preeclampsia. Hypertension. 2008;51:982-988.
4. Granger JP, Alexander BT, Llinas MT, Bennett WA, Khalil RA. Pathophysiology of hypertension during preeclampsia linking placental ischemia with endothelial dysfunction. Hypertension. 2001;38(3 pt 2):718-722.
5. Clapp JF 3rd, Kim H, Burciu B, Schmidt S, Petry K, Lopez B. Continuing regular exercise during pregnancy: effect of exercise volume on fetoplacental growth. Am J Obstet Gynecol. 2002;186:142-147.
6. Weissgerber TL, Davies GA, Roberts JM. Modification of angiogenic factors by regular and acute exercise during pregnancy. J Appl Physiol. 2010;108:1217-1223.
7. Clapp JF 3rd. Long-term outcome after exercising throughout pregnancy: fitness and cardiovascular risk. Am J Obstet Gynecol. 2008;199:489.e1-489.e6.
8. Clapp JF 3rd. Morphometric and neurodevelopmental outcome at age five years of the offspring of women who continued to exercise regularly throughout pregnancy. J Pediatr. 1996;129:856-863.
9. Fidalgo M, Falcão-Tebas F, Bento-Santos A, de Oliveira E, Nogueira-Neto JF, de Moura EG, Lisboa PC, de Castro RM, Leandro CG. Programmed changes in the adult rat offspring caused by maternal protein restriction during gestation and lactation are attenuated by maternal moderate-low physical training. Br J Nutr. 2012 May 1:1-8 [Epub ahead of print] doi:10.1017/ S0007114512001316.
10. Yeo S, Steele NM, Chang MC, Leclaire SM, Ronis DL, Hayashi R. Effect of exercise on blood pressure in pregnant women with a high risk of gestational hypertensive disorders. J Reprod Med. 2000;45:293-298.
11. Falcao S, Bisotto S, Michel C, Lacasse AA, Vaillancourt C, Gutkowska J, Lavoie JL. Exercise training can attenuate preeclampsia-like features in an animal model. J Hypertens. 2010;28:2446-2453.
12. Gilbert JS, Banek CT, Bauer AJ, Gingery A, Dreyer HC. Placental and vascular adaptations to exercise training before and during pregnancy in the rat. Am J Physiol Regul Integr Comp Physiol. 2012;303:R520-R526.
13. Yamashita N, Hoshida S, Otsu K, Asahi M, Kuzuya T, Hori M. Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation. J Exp Med. 1999;189:1699-1706.
14. Atalay M, Oksala NK, Laaksonen DE, Khanna S, Nakao C, Lappalainen J, Roy S, Hänninen O, Sen CK. Exercise training modulates heat shock protein response in diabetic rats. J Appl Physiol. 2004;97:605-611.
15. Siu PM, Bryner RW, Martyn JK, Alway SE. Apoptotic adaptations from exercise training in skeletal and cardiac muscles. FASEB J. 2004;18:1150-1152.
16. Chicco AJ, McCune SA, Emter CA, Sparagna GC, Rees ML, Bolden DA, Marshall KD, Murphy RC, Moore RL. Low-intensity exercise training delays heart failure and improves survival in female hypertensive heart failure rats. Hypertension. 2008;51:1096-1102.
17. Freyssenet D. Energy sensing and regulation of gene expression in skeletal muscle. J Appl Physiol. 2007;102:529-540.
18. ACOG Committee on Obstetric Practice. Committee opinion #267: exercise during pregnancy and the postpartum period. Obstetrics & Gynecology. 2002; 99:171-173.
19. Moraska A, Deak T, Spencer RL, Roth D, Fleshner M. Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol. 2000;279:R1321-R1329.
20. Gilbert JS, Verzwyvelt J, Colson D, Arany M, Karumanchi SA, Granger JP. Recombinant vascular endothelial growth factor 121 infusion lowers blood pressure and improves renal function in rats with placentalischemia-induced hypertension. Hypertension. 2010;55:380-385.
21. Gilbert JS, Bauer AJ, Gingery A, Banek CT, Chasson S. Circulating and utero-placental adaptations to chronic placental ischemia in the rat. Placenta. 2012;33:100-105.
22. Heltemes A, Gingery A, Soldner EL, Bozadjieva N, Jahr KN, Johnson BK, Gilbert JS. Chronic placental ischemia alters amniotic fluid milieu and results in impaired glucose tolerance, insulin resistance and hyperleptinemia in young rats. Exp Biol Med (Maywood). 2010;235:892-899.
23. Gilbert JS, Babcock SA, Granger JP. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension. 2007;50:1142-1147.
24. Sedeek M, Gilbert JS, LaMarca BB, Sholook M, Chandler DL, Wang Y, Granger JP. Role of reactive oxygen species in hypertension produced by reduced uterine perfusion in pregnant rats. Am J Hypertens. 2008;21:1152-1156.
25. Banek CT, Bauer AJ, Gingery A, Gilbert JS. Timing of ischemic insult alters fetal growth trajectory, maternal angiogenic balance and markers of renal oxidative stress in the pregnant rat. Am J Physiol Regul Integr Comp Physiol. 2012;303:R658-R664
26. Myatt L. Placental adaptive responses and fetal programming. J Physiol (Lond). 2006;572(pt 1):25-30.
27. Lam C, Lim KH, Karumanchi SA. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension. 2005;46:1077-1085.
28. Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res. 2005;57(5 pt 2):1R-7R.
29. Venkatesha S, Toporsian M, Lam C, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006;12:642-649.
30. Gilbert JS, Gilbert SA, Arany M, Granger JP. Hypertension produced by placental ischemia in pregnant rats is associated with increased soluble endoglin expression. Hypertension. 2009;53:399-403.
31. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, Pugh CW, Ratcliffe PJ, Gleadle JM. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem. 2004;279:38458-38465.
32. George EM, Cockrell K, Aranay M, Csongradi E, Stec DE, Granger JP. Induction of heme oxygenase 1 attenuates placental ischemia-induced hypertension. Hypertension. 2011;57:941-948.
33. George EM, Cockrell K, Adair TH, Granger JP. Regulation of sFlt-1 and VEGF secretion by adenosine under hypoxic conditions in rat placental villous explants. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1629-R1633.
34. Chinsomboon J, Ruas J, Gupta RK, Thom R, Shoag J, Rowe GC, Sawada N, Raghuram S, Arany Z. The transcriptional coactivator PGC-1α mediates exercise-induced angiogenesis in skeletal muscle. Proc Natl Acad Sci USA. 2009;106:21401-21406.
35. Myatt L. Review: reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta. 2010;31(suppl):S66-S69.
36. Weissgerber TL, Wolfe LA, Davies GA. The role of regular physical activity in preeclampsia prevention. Med Sci Sports Exerc. 2004;36:2024-2031.
37. Kasawara KT, Nascimento SL, Costa ML, Surita FG, E Silva JL. Exercise and physical activity in the prevention of pre-eclampsia: systematic review. Acta Obstet Gynecol Scand. 2012;91:1147-1157.