Uterine artery dysfunction in pregnant ACE2 knockout mice is associated with placental hypoxia and reduced umbilical blood flow velocity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 1, 2015, Pages E84-E94

  Yamaleyeva, Liliya M ^a   Pulgar, Victor M ^a   Lindsey, Sarah H ^b   Yamane, Larissa ^a   Varagic, Jasmina ^a   McGee, Carolynne ^a   DaSilva, Mauro ^a   Bonfa, Paula Lopes ^a   Gurley, Susan B ^c   Brosnihan, K Bridget ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin II; Fetal growth restriction; Hypoxia; Vascular reactivity; Vasoconstriction

Indexed keywords

ANGIOTENSIN II; CREATININE; HYPOXIA INDUCIBLE FACTOR 2ALPHA; PHENYLEPHRINE; PIMONIDAZOLE; ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY DISEASE; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL REACTIVITY; CELL INVASION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; EC50; FEMALE; FETUS; FETUS GROWTH; FETUS WEIGHT; HEART WEIGHT; HYPOXEMIA; IMMUNOHISTOCHEMISTRY; KIDNEY MASS; KNOCKOUT MOUSE; MOUSE; NEWBORN; NONHUMAN; PEAK SYSTOLIC VELOCITY; PHENOTYPE; PLACENTA CIRCULATION; PLACENTA INSUFFICIENCY; PLACENTA WEIGHT; PREGNANCY; PRIORITY JOURNAL; PROTEIN URINE LEVEL; SYSTOLIC BLOOD PRESSURE; TROPHOBLAST; UMBILICAL CORD BLOOD FLOW; UTERINE ARTERY; WILD TYPE; ANIMAL; ANOXIA; C57BL MOUSE; GENETICS; INTRAUTERINE GROWTH RETARDATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA; UMBILICAL CORD; VASCULARIZATION;

ANIMALS; ANOXIA; BLOOD FLOW VELOCITY; FEMALE; FETAL GROWTH RETARDATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDYL-DIPEPTIDASE A; PLACENTA; PLACENTAL CIRCULATION; PREGNANCY; UMBILICAL CORD; UTERINE ARTERY;

EID: 84935487323     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00596.2014     Document Type: Article

References (66)

1. 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, 2000.
2. Benjamin N, Rymer J, Todd SD, Thom M, Ritter JM. Sensitivity to angiotensin II of forearm resistance vessels in pregnancy. Br J Clin Pharmacol 32: 523–525, 1991.
3. Bharadwaj MS, Strawn WB, Groban L, Yamaleyeva LM, Chappell MC, Horta C, Atkins K, Firmes L, Gurley SB, Brosnihan KB. Angiotensin-converting enzyme 2 deficiency is associated with impaired gestational weight gain and fetal growth restriction. Hypertension 58: 852–858, 2011.
4. Burrell JH, Lumbers ER. Angiotensin receptor subtypes in the uterine artery during ovine pregnancy. Eur J Pharmacol 330: 257–267, 1997.
5. Chen K, Merrill DC, Rose JC. The importance of angiotensin II subtype receptors for blood pressure control during mouse pregnancy. Reprod Sci 14: 694–704, 2007.
6. Chinnathambi V, Blesson CS, Vincent KL, Saade GR, Hankins GD, Yallampalli C, Sathishkumar K. Elevated testosterone levels during rat pregnancy cause hypersensitivity to angiotensin II and attenuation of endothelium-dependent vasodilation in uterine arteries. Hypertension 64: 405–414, 2014.
7. Chung E, Yeung F, Leinwand LA. Calcineurin activity is required for cardiac remodelling in pregnancy. Cardiovasc Res 100: 402–410, 2013.
8. Cohen-Tannoudji J, Mhaouty S, Elwardy-Merezak J, Lecrivain JL, Robin MT, Legrand C, Maltier JP. Regulation of myometrial Gi2, Gi3, and Gq expression during pregnancy. Effects of progesterone and estra-diol Biol Reprod 53: 55–64, 1995.
9. 10. Cooke CL, Davidge ST. Endothelial-dependent vasodilation is reduced in mesenteric arteries from superoxide dismutase knockout mice. Cardiovasc Res 60: 635–642, 2003.
10. Croy BA, Yamada AT, DeMayo FJ, Adamson SL, eds. The Guide to Investigation of Mouse Pregnancy (1st Ed.). Elsevier, 2014.
11. Elvert G, Kappel A, Heidenreich R, Englmeier U, Lanz S, Acker T, Rauter M, Plate K, Sieweke M, Breier G, Flamme I. Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha) and Ets-1 in the transcriptional activation of vascular endothelial growth factor recep-tor-2 (Flk-1). J Biol Chem 278: 7520–7530, 2003.
12. Everett TR, Lees CC. Beyond the placental bed: placental and systemic determinants of the uterine artery Doppler waveform. Placenta 33: 893–901, 2012.
13. Ferrario CM, Trask AJ, Jessup JA. Advances in the biochemical and functional roles of angiotensin converting enzyme 2 and angiotensin-(1–7) in the regulation of cardiovascular function. Am J Physiol Heart Circ Physiol 289: H2281–H2290, 2005.
14. Fonseca BM, Correia-da-Silva G, and Teixeira NA. The rat as an animal model for fetoplacental development: a reappraisal of the post-implantation period. Reprod Biol 12: 97–118, 2012.
15. Gant NF, Daley GL, Chand S, Whalley PJ, MacDonald PC. A study of angiotensin II pressor response throughout primigravid pregnancy. J Clin Invest 52: 2682–2689, 1973.
16. Gant NF, Whalley PJ, Everett RB, Worley RJ, MacDonald PC. Control of vascular reactivity in pregnancy. Am J Kid Dis 9: 303–307, 1987.
17. Gebb J, Dar P. Colour Doppler ultrasound of spiral artery blood flow in the prediction of pre-eclampsia and intrauterine growth restriction. Best Pract Res Clin Obstet Gynaecol 25: 355–366, 2011.
18. Genbacev O, Krtolica A, Kaelin W, Fisher SJ. Human cytotrophoblast expression of the von Hippel-Lindau protein is downregulated during uterine invasion in situ and upregulated by hypoxia in vitro. Dev Biol 233: 526–536, 2001.
19. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hy-poxic gene regulation. Mol Cell Biol 23: 9361–9374, 2003.
20. Hutter D, Kingdom J, Jaeggi E. Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: a review. Int J Pediatr 2010: 2010.
21. Ibrahim HS, Froemming GR, Omar E, Singh HJ. ACE2 activation by xanthenone prevents leptin-induced increases in blood pressure and pro-teinuria during pregnancy in Sprague-Dawley rats. Reprod Toxicol 49C: 155–161, 2014.
22. Khalil RA, Granger JP. Vascular mechanisms of increased arterial pressure in preeclampsia: lessons from animal models. Am J Physiol Regul Integr Comp Physiol 283: R29–R45, 2002.
23. Kostrzewska A, Laudanski T, Batra S. Effect of calcium and calmod-ulin antagonists on contractile responses of the human uterine artery. Br J Pharmacol 94: 1037–1042, 1988.
24. Kuba K, Imai Y, Rao S, Gao H, Guo F, Guan B, Huan Y, Yang P, Zhang Y, Deng W, Bao L, Zhang B, Liu G, Wang Z, Chappell M, Liu Y, Zheng D, Leibbrandt A, Wada T, Slutsky AS, Liu D, Qin C, Jiang C, Penninger JM. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat Med 11: 875–879, 2005.
25. Kulandavelu S, Whiteley KJ, Bainbridge SA, Qu D, Adamson SL. Endothelial NO synthase augments fetoplacental blood flow, placental vascularization, and fetal growth in mice. Hypertension 61: 259–266, 2013.
26. Kusinski LC, Stanley JL, Dilworth MR, Hirt CJ, Andersson IJ, Renshall LJ, Baker BC, Baker PN, Sibley CP, Wareing M, Glazier JD. eNOS knockout mouse as a model of fetal growth restriction with an impaired uterine artery function and placental transport phenotype. Am J Physiol Regul Integr Comp Physiol 303: R86–R93, 2012.
27. Levy A, Yagil Y, Bursztyn M, Barkalifa R, Scharf S, Yagil C. ACE2 expression and activity are enhanced during pregnancy. Am J Physiol Regul Integr Comp Physiol 295: R1953–R1961, 2008.
28. Lindsey SH, da Silva AS, Silva MS, Chappell MC. Reduced vasorelax-ation to estradiol and G-1 in aged female and adult male rats is associated with GPR30 downregulation. Am J Physiol Endocrinol Metab 305: E113–E118, 2013.
29. Lindsey SH, Yamaleyeva LM, Brosnihan KB, Gallagher PE, Chappell MC. Estrogen receptor GPR30 reduces oxidative stress and proteinuria in the salt-sensitive female mRen2. Lewis rat. Hypertension 58: 665–671, 2011.
30. Mayer C, Joseph KS. Fetal growth: a review of terms, concepts and issues relevant to obstetrics. Ultrasound Obstet Gynecol 41: 136–145, 2013.
31. McCormick MC. The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med 312: 82–90, 1985.
32. McMullen JR, Gibson KJ, Lumbers ER, Burrell JH. Selective down-regulation of AT2 receptors in uterine arteries from pregnant ewes given 24-h intravenous infusions of angiotensin II. Regul Pept 99: 119–129, 2001.
33. McMullen JR, Gibson KJ, Lumbers ER, Burrell JH, Wu J. Interactions between AT1 and AT2 receptors in uterine arteries from pregnant ewes. Eur J Pharmacol 378: 195–202, 1999.
34. Mhaouty-Kodja S, Houdeau E, Legrand C. Regulation of myometrial phospholipase C system and uterine contraction by beta-adrenergic receptors in midpregnant rat. Biol Reprod 70: 570–576, 2004.
35. Mirabito KM, Hilliard LM, Wei Z, Tikellis C, Widdop RE, Vinh A, Denton KM. Role of inflammation and the angiotensin type 2 receptor in the regulation of arterial pressure during pregnancy in mice. Hypertension 2014.
36. Mishra N, Nugent WH, Mahavadi S, Walsh SW. Mechanisms of enhanced vascular reactivity in preeclampsia. Hypertension 58: 867–873, 2011.
37. Mu J, Adamson SL. Developmental changes in hemodynamics of uterine artery, utero- and umbilicoplacental, and vitelline circulations in mouse throughout gestation. Am J Physiol Heart Circ Physiol 291: H1421–H1428, 2006.
38. Mulvany MJ, Halpern W. Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41: 19–26, 1977.
39. Neves LAA, Stovall K, Joyner J, Valdes G, Gallagher PE, Ferrario CM, Merrill DC, Brosnihan KB. ACE2 and Ang-(1–7) in the uterus during early and late gestation. Am J Physiol Regul Integr Comp Physiol 294: R151–R161, 2008.
40. Neves LAA, Williams AF, Averill DB, Ferrario CM, Walkup MP, Brosnihan KB. Pregnancy enhances the angiotensin (Ang)-(1–7) vasodilator response in mesenteric arteries and increases the renal concentration and urinary excretion of Ang-(1–7). Endocrinology 14: 3338–3343, 2003.
41. Nguyen DH, Zhou T, Shu J, Mao JH. Quantifying chromogen intensity in immunohistochemis-try via reciprocal intensity. Cancer InCytes 2(1), e. 2013.
42. Ni Y, Meyer M, Osol G. Gestation increases nitric oxide-mediated vasodilation in rat uterine arteries. Am J Obstet Gynecol 176: 856–864, 1997.
43. Osol G, Cipolla M. Pregnancy-induced changes in the three-dimensional mechanical properties of pressurized rat uteroplacental (radial) arteries. Am J Obstet Gynecol 168: 268–274, 1993.
44. Osol G, Mandala M. Maternal uterine vascular remodeling during pregnancy. Physiology (Bethesda) 24: 58–71, 2009.
45. Pastore MB, Jobe SO, Ramadoss J, Magness RR. Estrogen receptor-alpha and estrogen receptor-beta in the uterine vascular endothelium during pregnancy: functional implications for regulating uterine blood flow. Semin Reprod Med 30: 46–61, 2012.
46. Patel VB, Zhong JC, Fan D, Basu R, Morton JS, Parajuli N, Mc-Murtry MS, Davidge ST, Kassiri Z, Oudit GY. Angiotensin-converting enzyme 2 is a critical determinant of angiotensin II-induced loss of vascular smooth muscle cells and adverse vascular remodeling. Hypertension 64: 157–164, 2014.
47. Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4: 397–413, 1983.
48. Pisaneschi S, Strigini FA, Sanchez AM, Begliuomini S, Casarosa E, Ripoli A, Ghirri P, Boldrini A, Fink B, Genazzani AR, Coceani F, Simoncini T. Compensatory feto-placental upregulation of the nitric oxide system during fetal growth restriction. PLoS One 7: e45294, 2012.
49. Pulgar VM, Yamaleyeva LM, Varagic J, McGee CM, Bader M, Dechend R, Howlett AC, Brosnihan KB. Increased angiotensin II contraction of the uterine artery at early gestation in a transgenic model of hypertensive pregnancy is reduced by inhibition of endocannabinoid hydrolysis. Hypertension 64: 619–625, 2014.
50. Pulgar VM, Yamashiro H, Rose JC, Moore LG. Role of the AT2 receptor in modulating the angiotensin II contractile response of the uterine artery at mid-gestation. J Renin Angiotensin Aldosterone Syst 12: 176–183, 2011.
51. Raleigh JA, Chou SC, Arteel GE, Horsman MR. Comparisons among pimonidazole binding, oxygen electrode measurements, and radiation response in C3H mouse tumors. Radiat Res 151: 580–589, 1999.
52. Rentzsch B, Todiras M, Iliescu R, Popova E, Campos LA, Oliveira ML, Baltatu OC, Santos RA, Bader M. Transgenic angiotensin-convert-ing enzyme 2 overexpression in vessels of SHRSP rats reduces blood pressure and improves endothelial function. Hypertension 52: 967–973, 2008.
53. Sriramula S, Cardinale JP, Lazartigues E, Francis J. ACE2 overex-pression in the paraventricular nucleus attenuates angiotensin II-induced hypertension. Cardiovasc Res 92: 401–408, 2011.
54. Tallant EA, Ferrario CM, Gallagher PE. Angiotensin-(1–7) inhibits growth of cardiac myocytes through activation of the mas receptor. Am J Physiol Heart Circ Physiol 289: H1560–H1566, 2005.
55. Thomas MC, Pickering RJ, Tsorotes D, Koitka A, Sheehy K, Bernardi S, Toffoli B, Nguyen-Huu TP, Head GA, Fu Y, Chin-Dusting J, Cooper ME, Tikellis C. Genetic Ace2 deficiency accentuates vascular inflammation and atherosclerosis in the ApoE knockout mouse. Circ Res 107: 888–897, 2010.
56. Valdes G, Neves LA, Anton L, Corthorn J, Chacon C, Germain AM, Merrill DC, Ferrario CM, Sarao R, Penninger J, Brosnihan KB. Distribution of angiotensin-(1–7) and ACE2 in human placentas of normal and pathological pregnancies. Placenta 27: 200–207, 2006.
57. Vandenbosche RC, Kirchner JT. Intrauterine growth retardation. Am Fam Physician 58: 1384, 1998.
58. Walters PE, Gaspari TA, Widdop RE. Angiotensin-(1–7) acts as a vasodepressor agent via angiotensin II type 2 receptors in conscious rats. Hypertension 45: 960–966, 2005.
59. Wareing M, Crocker IP, Warren AY, Taggart MJ, Baker PN. Characterization of small arteries isolated from the human placental chorionic plate. Placenta 23: 400–409, 2002.
60. Wareing M, Greenwood SL, Baker PN. Reactivity of human placental chorionic plate vessels is modified by level of oxygenation: differences between arteries and veins. Placenta 27: 42–48, 2006.
61. Wareing M, Myers JE, O’Hara M, Baker PN. Sildenafil citrate (Viagra) enhances vasodilatation in fetal growth restriction. J Clin Endocrinol Metab 90: 2550–2555, 2005.
62. Yamaleyeva LM, Gilliam-Davis S, Almeida I, Brosnihan KB, Lindsey SH, Chappell MC. Differential regulation of circulating and renal ACE2 and ACE in hypertensive mRen2. Lewis rats with early-onset diabetes. Am J Physiol Renal Physiol 302: F1374–F1384, 2012.
63. Yamaleyeva LM, Lindsey SH, Varagic J, Zhang LL, Gallagher PE, Chen AF, Chappell MC. Amelioration of renal injury and oxidative stress by the nNOS inhibitor L-VNIO in the salt-sensitive mRen2. Lewis congenic rat. J Cardiovasc Pharmacol 59: 529–538, 2012.
64. Yamaleyeva LM, Merrill DC, Ebert TJ, Smith TL, Mertz HL, Bros-nihan KB. Hemodynamic responses to angiotensin-(1–7) in women in their third trimester of pregnancy. Hypertens Pregnancy 1–14, 2014.
65. Yin FC, Spurgeon HA, Rakusan K, Weisfeldt ML, Lakatta EG. Use of tibial length to quantify cardiac hypertrophy: application in the aging rat. Am J Physiol Heart Circ Physiol 243: H941–H947, 1982.
66. Zhang H, Xiao D, Longo LD, Zhang L. Regulation of alpha1-adreno-ceptor-mediated contractions of uterine arteries by PKC: effect of pregnancy. Am J Physiol Heart Circ Physiol 291: H2282–H2289, 2006.