Angiotensin 1-7 and its analogue decrease blood pressure but aggravate renal damage in preeclamptic mice
Preeclampsia (PE) is a multisystem disease that affects the health of both the pregnant women and the fetus during pregnancy. Agonistic autoantibodies to the angiotensin II type I receptor (AT1-AA) play a significant role in the pathogenesis of PE. This study aimed to determine the effects of Angiot...
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| Published in | Experimental Animals Vol. 71; no. 4; pp. 519 - 528 |
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| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
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Japanese Association for Laboratory Animal Science
01.01.2022
Japan Science and Technology Agency |
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| Abstract | Preeclampsia (PE) is a multisystem disease that affects the health of both the pregnant women and the fetus during pregnancy. Agonistic autoantibodies to the angiotensin II type I receptor (AT1-AA) play a significant role in the pathogenesis of PE. This study aimed to determine the effects of Angiotensin 1-7 (Ang 1-7) and its analogue AVE0991 on AT1-AA-induced PE model. Pregnant mice were divided into five groups: the normal pregnant group, AT1-AA-induced preeclampsia group, and AT1-AA-induced preeclampsia group treated with Losartan, Ang 1-7, and AVE0991, respectively. AT1-AA-induced PE model was established on gestational day 13 by tail intravenous injection of purified AT1-AA polyclonal antibody from serum of guinea pigs. Blood urea nitrogen (BUN), urine albumin and urinary creatinine were measured on day 18 of pregnancy. The systolic blood pressure (SBP) was measured from gestational day 13 to day 18. Renal structure changes were observed via light and electron microscopy. Compared with the normal pregnant group (NP group), AT1-AA-induced preeclampsia group (PE group) exhibited elevated blood pressure and proteinuria, consistent with the characteristics of PE. Ang 1-7 or AVE0991 treatment decreased blood pressure without showing renoprotective effects. The findings indicated that Ang 1-7 and its analogue reduced blood pressure but aggravated renal damage in AT1-AA-induced PE mice. |
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| AbstractList | Preeclampsia (PE) is a multisystem disease that affects the health of both the pregnant women and the fetus during pregnancy. Agonistic autoantibodies to the angiotensin II type I receptor (AT1-AA) play a significant role in the pathogenesis of PE. This study aimed to determine the effects of Angiotensin 1-7 (Ang 1-7) and its analogue AVE0991 on AT1-AA-induced PE model. Pregnant mice were divided into five groups: the normal pregnant group, AT1-AA-induced preeclampsia group, and AT1-AA-induced preeclampsia group treated with Losartan, Ang 1-7, and AVE0991, respectively. AT1-AA-induced PE model was established on gestational day 13 by tail intravenous injection of purified AT1-AA polyclonal antibody from serum of guinea pigs. Blood urea nitrogen (BUN), urine albumin and urinary creatinine were measured on day 18 of pregnancy. The systolic blood pressure (SBP) was measured from gestational day 13 to day 18. Renal structure changes were observed via light and electron microscopy. Compared with the normal pregnant group (NP group), AT1-AA-induced preeclampsia group (PE group) exhibited elevated blood pressure and proteinuria, consistent with the characteristics of PE. Ang 1-7 or AVE0991 treatment decreased blood pressure without showing renoprotective effects. The findings indicated that Ang 1-7 and its analogue reduced blood pressure but aggravated renal damage in AT1-AA-induced PE mice. |
| ArticleNumber | 22-0029 |
| Author | Liu, Yuan Yang, Lin Zhai, Ruonan Yu, Ying Tong, Jiahao Niu, Jianying Gu, Yong |
| Author_xml | – sequence: 1 fullname: Liu, Yuan organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China – sequence: 2 fullname: Zhai, Ruonan organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China – sequence: 3 fullname: Tong, Jiahao organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China – sequence: 4 fullname: Yu, Ying organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China – sequence: 5 fullname: Yang, Lin organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China – sequence: 6 fullname: Gu, Yong organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China – sequence: 7 fullname: Niu, Jianying organization: Department of Nephrology, Shanghai Fifth People’s Hospital, Fudan University, 801 Heqing Road, Shanghai 200240, P.R. China |
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| Cites_doi | 10.1590/S0100-879X2007000400018 10.1161/HYPERTENSIONAHA.109.137935 10.3390/ijms20153695 10.1155/2012/256294 10.1371/journal.pone.0005406 10.1210/en.2009-0076 10.1007/s00280-003-0710-0 10.1161/01.HYP.37.4.1191 10.1080/14767050500217244 10.1172/JCI4106 10.1161/HYPERTENSIONAHA.112.191650 10.1080/10641950601147937 10.1161/HYPERTENSIONAHA.110.167569 10.1161/CIRCRESAHA.118.313276 10.1016/j.hipert.2016.06.002 10.2215/CJN.01820212 10.1038/nm.1856 10.1016/S0140-6736(13)60686-8 10.1161/01.HYP.0000256565.20983.d4 10.1016/j.cardiores.2006.09.006 10.1097/HJH.0b013e328304dbff 10.2174/0929866524666170728154459 10.1038/s41598-018-30008-5 10.1016/j.abb.2019.07.006 10.1136/bmj.39335.385301.BE 10.1038/s41598-020-61250-5 10.1152/ajprenal.00410.2003 10.1152/ajpregu.00221.2019 10.1100/tsw.2009.70 10.1016/j.jchromb.2006.07.004 10.3390/ijms21145131 10.1152/ajprenal.00363.2017 10.1097/00004872-200018070-00017 10.1042/CS20120461 10.1016/S1071-5576(02)00259-9 |
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| References | 31. Velázquez-Armenta EY, Han JY, Choi JS, Yang KM, Nava-Ocampo AA. Angiotensin II receptor blockers in pregnancy: a case report and systematic review of the literature. Hypertens Pregnancy. 2007; 26: 51–66. 14. Keidar S, Kaplan M, Gamliel-Lazarovich A. ACE2 of the heart: From angiotensin I to angiotensin (1-7). Cardiovasc Res. 2007; 73: 463–469. 29. Choi HS, Song JH, Kim IJ, Joo SY, Eom GH, Kim I, et al. Histone deacetylase inhibitor, CG200745 attenuates renal fibrosis in obstructive kidney disease. Sci Rep. 2018; 8: 11546. 10. Hubel CA, Wallukat G, Wolf M, Herse F, Rajakumar A, Roberts JM, et al. Agonistic angiotensin II type 1 receptor autoantibodies in postpartum women with a history of preeclampsia. Hypertension. 2007; 49: 612–617. 12. LaMarca B, Wallace K, Herse F, Wallukat G, Martin JN Jr, Weimer A, et al. Hypertension in response to placental ischemia during pregnancy: role of B lymphocytes. Hypertension. 2011; 57: 865–871. 30. Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ. 2007; 335: 974. 9. LaMarca B, Parrish M, Ray LF, Murphy SR, Roberts L, Glover P, et al. Hypertension in response to autoantibodies to the angiotensin II type I receptor (AT1-AA) in pregnant rats: role of endothelin-1. Hypertension. 2009; 54: 905–909. 35. Vishnyakova P, Elchaninov A, Fatkhudinov T, Sukhikh G. Role of the Monocyte-Macrophage System in Normal Pregnancy and Preeclampsia. Int J Mol Sci. 2019; 20: E3695. 34. Ellefson DD, diZerega GS, Espinoza T, Roda N, Maldonado S, Rodgers KE. Synergistic effects of co-administration of angiotensin 1-7 and Neupogen on hematopoietic recovery in mice. Cancer Chemother Pharmacol. 2004; 53: 15–24. 20. de Moraes PL, Kangussu LM, Castro CH, Almeida AP, Santos RAS, Ferreira AJ. Vasodilator Effect of Angiotensin-(1-7) on Vascular Coronary Bed of Rats: Role of Mas, ACE and ACE2. Protein Pept Lett. 2017; 24: 869–875. 2. Rana S, Lemoine E, Granger JP, Karumanchi SA. Preeclampsia: Pathophysiology, Challenges, and Perspectives. Circ Res. 2019; 124: 1094–1112. 28. Chihanga T, Ma Q, Nicholson JD, Ruby HN, Edelmann RE, Devarajan P, et al. NMR spectroscopy and electron microscopy identification of metabolic and ultrastructural changes to the kidney following ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2018; 314: F154–F166. 33. El-Saka MH, Madi NM, Ibrahim RR, Alghazaly GM, Elshwaikh S, El-Bermawy M. The ameliorative effect of angiotensin 1-7 on experimentally induced-preeclampsia in rats: Targeting the role of peroxisome proliferator-activated receptors gamma expression & asymmetric dimethylarginine. Arch Biochem Biophys. 2019; 671: 123–129. 5. Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, et al. Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension. 2001; 37: 1191–1195. 25. Newcombe C, Newcombe AR. Antibody production: polyclonal-derived biotherapeutics. J Chromatogr B Analyt Technol Biomed Life Sci. 2007; 848: 2–7. 1. Souza JP, Gülmezoglu AM, Vogel J, Carroli G, Lumbiganon P, Qureshi Z, et al. Moving beyond essential interventions for reduction of maternal mortality (the WHO Multicountry Survey on Maternal and Newborn Health): a cross-sectional study. Lancet. 2013; 381: 1747–1755. 27. Miller AJ, Bingaman SS, Mehay D, Medina D, Arnold AC. Angiotensin-(1-7) Improves Integrated Cardiometabolic Function in Aged Mice. Int J Mol Sci. 2020; 21: E5131. 16. Passos-Silva DG, Verano-Braga T, Santos RA. Angiotensin-(1-7): beyond the cardio-renal actions. Clin Sci (Lond). 2013; 124: 443–456. 24. Fu ML, Herlitz H, Schulze W, Wallukat G, Micke P, Eftekhari P, et al. Autoantibodies against the angiotensin receptor (AT1) in patients with hypertension. J Hypertens. 2000; 18: 945–953. 15. Anton L, Merrill DC, Neves LA, Diz DI, Corthorn J, Valdes G, et al. The uterine placental bed Renin-Angiotensin system in normal and preeclamptic pregnancy. Endocrinology. 2009; 150: 4316–4325. 3. Alvarez-Alvarez B, Martell-Claros N, Abad-Cardiel M, García-Donaire JA. [Hypertensive disorders during pregnancy: Cardiovascular long-term outcomes]. Hipertens Riesgo Vasc. 2017; 34: 85–92. 22. Stanhewicz AE, Alexander LM. Local angiotensin-(1-7) administration improves microvascular endothelial function in women who have had preeclampsia. Am J Physiol Regul Integr Comp Physiol. 2020; 318: R148–R155. 11. Wallukat G, Homuth V, Fischer T, Lindschau C, Horstkamp B, Jüpner A, et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest. 1999; 103: 945–952. 23. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, et al. Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med. 2008; 14: 855–862. 17. Tikellis C, Thomas MC. Angiotensin-Converting Enzyme 2 (ACE2) Is a Key Modulator of the Renin Angiotensin System in Health and Disease. Int J Pept. 2012; 2012: 256294. 19. Patel VB, Bodiga S, Fan D, Das SK, Wang Z, Wang W, et al. Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1-7 in experimental heart failure in angiotensin-converting enzyme 2-null mice. Hypertension. 2012; 59: 1195–1203. 18. Esteban V, Heringer-Walther S, Sterner-Kock A, de Bruin R, van den Engel S, Wang Y, et al. Angiotensin-(1-7) and the g protein-coupled receptor MAS are key players in renal inflammation. PLoS One. 2009; 4: e5406. 7. Yang X, Wang F, Chang H, Zhang S, Yang L, Wang X, et al. Autoantibody against AT1 receptor from preeclamptic patients induces vasoconstriction through angiotensin receptor activation. J Hypertens. 2008; 26: 1629–1635. 13. Dilauro M, Burns KD. Angiotensin-(1-7) and its effects in the kidney. ScientificWorldJournal. 2009; 9: 522–535. 4. Vikse BE, Irgens LM, Karumanchi SA, Thadhani R, Reisæter AV, Skjærven R. Familial factors in the association between preeclampsia and later ESRD. Clin J Am Soc Nephrol. 2012; 7: 1819–1826. 8. Xia Y, Wen H, Bobst S, Day MC, Kellems RE. Maternal autoantibodies from preeclamptic patients activate angiotensin receptors on human trophoblast cells. J Soc Gynecol Investig. 2003; 10: 82–93. 21. Velloso EP, Vieira R, Cabral AC, Kalapothakis E, Santos RA. Reduced plasma levels of angiotensin-(1-7) and renin activity in preeclamptic patients are associated with the angiotensin I- converting enzyme deletion/deletion genotype. Braz J Med Biol Res. 2007; 40: 583–590. 32. Vendemmia M, Garcia-Méric P, Rizzotti A, Boubred F, Lacroze V, Liprandi A, et al. Fetal and neonatal consequences of antenatal exposure to type 1 angiotensin II receptor-antagonists. J Matern Fetal Neonatal Med. 2005; 18: 137–140. 6. Shah DM. Role of the renin-angiotensin system in the pathogenesis of preeclampsia. Am J Physiol Renal Physiol. 2005; 288: F614–F625. 26. Choi HS, Kim IJ, Kim CS, Ma SK, Scholey JW, Kim SW, et al. Angiotensin-[1-7] attenuates kidney injury in experimental Alport syndrome. Sci Rep. 2020; 10: 4225. 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 34 13 35 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: 16. Passos-Silva DG, Verano-Braga T, Santos RA. Angiotensin-(1-7): beyond the cardio-renal actions. Clin Sci (Lond). 2013; 124: 443–456. – reference: 20. de Moraes PL, Kangussu LM, Castro CH, Almeida AP, Santos RAS, Ferreira AJ. Vasodilator Effect of Angiotensin-(1-7) on Vascular Coronary Bed of Rats: Role of Mas, ACE and ACE2. Protein Pept Lett. 2017; 24: 869–875. – reference: 32. Vendemmia M, Garcia-Méric P, Rizzotti A, Boubred F, Lacroze V, Liprandi A, et al. Fetal and neonatal consequences of antenatal exposure to type 1 angiotensin II receptor-antagonists. J Matern Fetal Neonatal Med. 2005; 18: 137–140. – reference: 33. El-Saka MH, Madi NM, Ibrahim RR, Alghazaly GM, Elshwaikh S, El-Bermawy M. The ameliorative effect of angiotensin 1-7 on experimentally induced-preeclampsia in rats: Targeting the role of peroxisome proliferator-activated receptors gamma expression & asymmetric dimethylarginine. Arch Biochem Biophys. 2019; 671: 123–129. – reference: 14. Keidar S, Kaplan M, Gamliel-Lazarovich A. ACE2 of the heart: From angiotensin I to angiotensin (1-7). Cardiovasc Res. 2007; 73: 463–469. – reference: 1. Souza JP, Gülmezoglu AM, Vogel J, Carroli G, Lumbiganon P, Qureshi Z, et al. Moving beyond essential interventions for reduction of maternal mortality (the WHO Multicountry Survey on Maternal and Newborn Health): a cross-sectional study. Lancet. 2013; 381: 1747–1755. – reference: 30. Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ. 2007; 335: 974. – reference: 4. Vikse BE, Irgens LM, Karumanchi SA, Thadhani R, Reisæter AV, Skjærven R. Familial factors in the association between preeclampsia and later ESRD. Clin J Am Soc Nephrol. 2012; 7: 1819–1826. – reference: 5. Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, et al. Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension. 2001; 37: 1191–1195. – reference: 8. Xia Y, Wen H, Bobst S, Day MC, Kellems RE. Maternal autoantibodies from preeclamptic patients activate angiotensin receptors on human trophoblast cells. J Soc Gynecol Investig. 2003; 10: 82–93. – reference: 17. Tikellis C, Thomas MC. Angiotensin-Converting Enzyme 2 (ACE2) Is a Key Modulator of the Renin Angiotensin System in Health and Disease. Int J Pept. 2012; 2012: 256294. – reference: 29. Choi HS, Song JH, Kim IJ, Joo SY, Eom GH, Kim I, et al. Histone deacetylase inhibitor, CG200745 attenuates renal fibrosis in obstructive kidney disease. Sci Rep. 2018; 8: 11546. – reference: 21. Velloso EP, Vieira R, Cabral AC, Kalapothakis E, Santos RA. Reduced plasma levels of angiotensin-(1-7) and renin activity in preeclamptic patients are associated with the angiotensin I- converting enzyme deletion/deletion genotype. Braz J Med Biol Res. 2007; 40: 583–590. – reference: 12. LaMarca B, Wallace K, Herse F, Wallukat G, Martin JN Jr, Weimer A, et al. Hypertension in response to placental ischemia during pregnancy: role of B lymphocytes. Hypertension. 2011; 57: 865–871. – reference: 31. Velázquez-Armenta EY, Han JY, Choi JS, Yang KM, Nava-Ocampo AA. Angiotensin II receptor blockers in pregnancy: a case report and systematic review of the literature. Hypertens Pregnancy. 2007; 26: 51–66. – reference: 13. Dilauro M, Burns KD. Angiotensin-(1-7) and its effects in the kidney. ScientificWorldJournal. 2009; 9: 522–535. – reference: 6. Shah DM. Role of the renin-angiotensin system in the pathogenesis of preeclampsia. Am J Physiol Renal Physiol. 2005; 288: F614–F625. – reference: 27. Miller AJ, Bingaman SS, Mehay D, Medina D, Arnold AC. Angiotensin-(1-7) Improves Integrated Cardiometabolic Function in Aged Mice. Int J Mol Sci. 2020; 21: E5131. – reference: 23. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, et al. Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med. 2008; 14: 855–862. – reference: 25. Newcombe C, Newcombe AR. Antibody production: polyclonal-derived biotherapeutics. J Chromatogr B Analyt Technol Biomed Life Sci. 2007; 848: 2–7. – reference: 24. Fu ML, Herlitz H, Schulze W, Wallukat G, Micke P, Eftekhari P, et al. Autoantibodies against the angiotensin receptor (AT1) in patients with hypertension. J Hypertens. 2000; 18: 945–953. – reference: 19. Patel VB, Bodiga S, Fan D, Das SK, Wang Z, Wang W, et al. Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1-7 in experimental heart failure in angiotensin-converting enzyme 2-null mice. Hypertension. 2012; 59: 1195–1203. – reference: 10. Hubel CA, Wallukat G, Wolf M, Herse F, Rajakumar A, Roberts JM, et al. Agonistic angiotensin II type 1 receptor autoantibodies in postpartum women with a history of preeclampsia. Hypertension. 2007; 49: 612–617. – reference: 7. Yang X, Wang F, Chang H, Zhang S, Yang L, Wang X, et al. Autoantibody against AT1 receptor from preeclamptic patients induces vasoconstriction through angiotensin receptor activation. J Hypertens. 2008; 26: 1629–1635. – reference: 22. Stanhewicz AE, Alexander LM. Local angiotensin-(1-7) administration improves microvascular endothelial function in women who have had preeclampsia. Am J Physiol Regul Integr Comp Physiol. 2020; 318: R148–R155. – reference: 11. Wallukat G, Homuth V, Fischer T, Lindschau C, Horstkamp B, Jüpner A, et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest. 1999; 103: 945–952. – reference: 26. Choi HS, Kim IJ, Kim CS, Ma SK, Scholey JW, Kim SW, et al. 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| Snippet | Preeclampsia (PE) is a multisystem disease that affects the health of both the pregnant women and the fetus during pregnancy. Agonistic autoantibodies to the... |
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| SubjectTerms | agonistic autoantibodies to the angiotensin II type I receptor Albumins Angiotensin angiotensin 1-7 Angiotensin II animal model Antibodies Autoantibodies Blood pressure Creatinine Damage Electron microscopy Fetuses Guinea pigs Hypertension Intravenous administration Kidneys Pathogenesis Pre-eclampsia Preeclampsia Pregnancy Pregnancy complications Pressure effects Proteinuria renal damage Urea |
| Title | Angiotensin 1-7 and its analogue decrease blood pressure but aggravate renal damage in preeclamptic mice |
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