Timing of ischemic insult alters fetal growth trajectory, maternal angiogenic balance, and markers of renal oxidative stress in the pregnant rat

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 303, Issue 6, 2012, Pages

  Banek, Christopher T ^a   Bauer, Ashley J ^a   Gingery, Anne ^a   Gilbert, Jeffrey S ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Angiogenic balance; Hypertension; Intrauterine growth restriction; Preeclampsia

Indexed keywords

8 ISOPROSTANE; FMS RELATED TYROSINE KINASE 1; MALONALDEHYDE; PROTEIN TYROSINE KINASE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG; VASCULOTROPIN; BIOLOGICAL MARKER; TROLOX C; VASCULOTROPIN RECEPTOR 1;

ABDOMINAL AORTA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PRESSURE; ARTERY RESISTANCE; ARTICLE; BLOOD PRESSURE; CELL ASSAY; CONTROLLED STUDY; ENDOTHELIUM; ENZYME BLOOD LEVEL; FEMALE; FETUS; FETUS GROWTH; FETUS WEIGHT; HYPERTENSION; INTRAUTERINE GROWTH RETARDATION; NONHUMAN; OXIDATIVE STRESS; PLACENTA INSUFFICIENCY; PLACENTA PERFUSION; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; RAT; UTERUS BLOOD FLOW; ANGIOGENESIS; ANIMAL; BLOOD; FETUS DEVELOPMENT; ISCHEMIA; KIDNEY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; UTERUS; VASCULARIZATION; DISEASE SEVERITY; GESTATION PERIOD; MEAN ARTERIAL PRESSURE; PLACENTA WEIGHT; PROTEIN BLOOD LEVEL;

ANIMALS; BIOLOGICAL MARKERS; BLOOD PRESSURE; FEMALE; FETAL DEVELOPMENT; ISCHEMIA; KIDNEY; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; UTERUS;

EID: 84866388606     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00250.2012     Document Type: Article

References (47)

1. Agarwal I, Karumanchi SA. Preeclampsia and the anti-angiogenic state. Pregnancy Hypertens 1: 17-21, 2011.
2. Akolekar R, Syngelaki A, Sarquis R, Zvanca M, Nicolaides KH. Prediction of early, intermediate and late pre-eclampsia from maternal factors, biophysical and biochemical markers at 11-13 weeks. Prenat Diagn 31: 66-74, 2011.
3. Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, Granger JP. Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension 37: 1191-1195, 2001.
4. Alexander BT, Llinas MT, Kruckeberg WC, Granger JP. L-arginine attenuates hypertension in pregnant rats with reduced uterine perfusion pressure. Hypertension 43: 832-836, 2004.
5. Banek CT, Gilbert JS. Approaching the threshold for predicting preeclampsia: monitoring angiogenic balance during pregnancy. Hypertension 58: 774-775, 2011.
6. Barr M Jr., Brent RL. The relation of the uterine vasculature to fetal growth and the intrauterine position effect in rats. Teratology 3: 251-260, 1970.
7. Bdolah Y, Lam C, Rajakumar A, Shivalingappa V, Mutter W, Sachs BP, Lim KH, Bdolah-Abram T, Epstein FH, Karumanchi SA. Twin pregnancy and the risk of preeclampsia: bigger placenta or relative ischemia? Am J Obstet Gynecol 198: 428, 2008.
8. Bridges JP, Gilbert JS, Colson D, Gilbert SA, Dukes MP, Ryan MJ, Granger JP. Oxidative stress contributes to soluble Fms-like tyrosine kinase-1 induced vascular dysfunction in pregnant rats. Am J Hypertens 22: 564-568, 2009.
9. Bruce NW. Resistance of the rat embryo to ligation of a uterine artery early in gestation. J Reprod Fertil 28: 265-267, 1972.
10. Bruce NW. The distribution of blood flow to the reproductive organs of rats near term. Reproduction 46: 359-362, 1976.
11. Buelke-Sam J, Holson JF, Nelson CJ. Blood flow during pregnancy in the rat: II. Dynamics of and litter variability in uterine flow. Teratology 26: 279-288, 1982.
12. Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS. Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 30: Suppl 43-48, 2009.
13. Caughey AB, Sundaram V, Kaimal AJ, Cheng YW, Gienger A, Little SE, Lee JF, Wong L, Shaffer BL, Tran SH, Padula A, McDonald KM, Long EF, Owens DK, Bravata DM. Maternal and neonatal outcomes of elective induction of labor. Evid Rep Technol Assess 176: 1-257, 2009.
14. Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS. Association of maternal endothelial dysfunction with preeclampsia. JAMA 285: 1607-1612, 2001.
15. Chappell LC, Seed PT, CStat Kelly FJ, Briley A, Hunt BJ, Charnock-Jones DS, Mallet A, Poston L. Vitamin C and E supplementation in women at risk of preeclampsia is associated with changes in indices of oxidative stress and placental function. Am J Obstet Gynecol 187: 777-784, 2002.
16. Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 195: 201-207, 2006.
17. Eder DJ, McDonald MT. A role for brain angiotensin II in experimental pregnancy-induced hypertension in laboratory rats. Clin Exp Hypertens Pregnancy B6: 431-451, 1987.
18. Espinoza J, Romero R, Nien JK, Gomez R, Kusanovic JP, Goncalves LF, Medina L, Edwin S, Hassan S, Carstens M, Gonzalez R. Identification of patients at risk for early onset and/or severe preeclampsia with the use of uterine artery Doppler velocimetry and placental growth factor. Am J Obstet Gynecol 196: 326-313, 2007.
19. Gilbert JS, Bauer AJ, Gingery A, Banek CT, Chasson S. Circulating and utero-placental adaptations to chronic placental ischemia in the rat. Placenta 33: 100-105, 2012.
20. Gilbert JS, Dukes M, LaMarca BB, Cockrell K, Babcock SA, Granger JP. Effects of reduced uterine perfusion pressure on blood pressure and metabolic factors in pregnant rats. Am J Hypertens 20: 686-691, 2007.
21. 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 50: 1142-1147, 2007.
22. Gilbert JS, Nijland MJ. Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol 295: R1941-R1952, 2008.
23. 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 placental ischemia-induced hypertension. Hypertension 55: 380-385, 2009.
24. Gilbert M, Leturque A. Fetal weight and its relationship to placental blood flow and placental weight in experimental intrauterine growth retardation in the rat. J Dev Physiol 4: 237-246, 1982.
25. Hasegawa J, Sekizawa A, Farina A, Nakamura M, Matsuoka R, Ichizuka K, Okai T. Location of the placenta or the umbilical cord insertion site in the lowest uterine segment is associated with low maternal blood pressure. BJOG 118: 1464-1469, 2011.
26. Heltemes A, Gingery A, Soldner ELB, Bozadjieva N, Jahr K, Johnson B, 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) 235: 892-899, 2010.
27. Hoffmann DS, Weydert CJ, Lazartigues E, Kutschke WJ, Kienzle MF, Leach JE, Sharma JA, Sharma RV, Davisson RL. Chronic tempol prevents hypertension, proteinuria, and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertension 51: 1058-1065, 2008.
28. Ishibashi O, Ohkuchi A, Ali MM, Kurashina R, Luo SS, Ishikawa T, Takizawa T, Hirashima C, Takahashi K, Migita M, Ishikawa G, Yoneyama K, Asakura H, Izumi A, Matsubara S, Takeshita T, Takizawa T. Hydroxysteroid (17-β) dehydrogenase 1 is dysregulated by Mir-210 and Mir-518c that are aberrantly expressed in preeclamptic placentas: a novel marker for predicting preeclampsia. Hypertension 59: 265-273, 2012.
29. Karumanchi SA, Bdolah Y. Hypoxia and sFlt-1 in preeclampsia: the "chicken-and-egg" question. Endocrinology 145: 4835-4837, 2004.
30. Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Edwin SS, Gomez R, Yeo L, Conde-Agudelo A, Hassan SS. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia. J Matern Fetal Neonatal Med 22: 1021-1038, 2009.
31. LaMarca B, Parrish M, Ray LF, Murphy SR, Roberts L, Glover P, Wallukat G, Wenzel K, Cockrell K, Martin JN Jr, Ryan MJ, Dechend R. Hypertension in response to autoantibodies to the angiotensin II type I receptor (AT1-AA) in pregnant rats: role of endothelin-1. Hypertension 54: 905-909, 2009.
32. LaMarca BD, Ryan MJ, Gilbert JS, Murphy SR, Granger JP. Inflammatory cytokines in the pathophysiology of hypertension during preeclampsia. Curr Hypertens Rep 9: 480-485, 2007.
33. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683, 2004.
34. Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res 57: 1R-7R, 2005.
35. Murji A, Proctor LK, Paterson AD, Chitayat D, Weksberg R, Kingdom J. Male sex bias in placental dysfunction. Am J Med Genet 158A: 779-783, 2012.
36. Parrish MR, Ryan MJ, Glover P, Brewer J, Ray L, Dechend R, Martin JN Jr., LaMarca BB. Angiotensin II type 1 autoantibody induced hypertension during pregnancy is associated with renal endothelial dysfunction. Gend Med 8: 184-188, 2011.
37. Roberts JM, Gammill HS. Preeclampsia: Recent Insights. Hypertension 46: 1243-1249, 2005.
38. Roberts JM, Pearson G, Cutler J, Lindheimer M. Summary of the NHLBI Working Group on Research on Hypertension During Pregnancy. Hypertension 41: 437-445, 2003.
39. Schlembach D, Wallner W, Sengenberger R, Stiegler E, Mortl M, Beckmann MW, Lang U. Angiogenic growth factor levels in maternal and fetal blood: correlation with Doppler ultrasound parameters in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 29: 407-413, 2007.
40. 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 21: 1152-1156, 2008.
41. Shibata E, Rajakumar A, Powers RW, Larkin RW, Gilmour C, Bodnar LM, Crombleholme WR, Ness RB, Roberts JM, Hubel CA. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab 90: 4895-4903, 2005.
42. Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet 365: 785-799, 2005.
43. Sikov MR, Thomas JM. Prenatal growth of the rat. Growth 34: 1-14, 1970.
44. Tjoa ML, Levine RJ, Karumanchi SA. Angiogenic factors and preeclampsia. Front Biosci 12: 2395-2402, 2007.
45. Valensise H, Vasapollo B, Gagliardi G, Novelli GP. Early and late preeclampsia: two different maternal hemodynamic states in the latent phase of the disease. Hypertension 52: 873-880, 2008.
46. Wathen KA, Tuutti E, Stenman UH, Alfthan H, Halmesmaki E, Finne P, Ylikorkala O, Vuorela P. Maternal serum-soluble vascular endothelial growth factor receptor-1 in early pregnancy ending in preeclampsia or intrauterine growth retardation. J Clin Endocrinol Metab 91: 180-184, 2006.
47. Wigglesworth JS. Experimental growth retardation in the foetal rat. J Pathol Bacteriol 88: 1-13, 1964.