Interaction of SARS-CoV-2 With RAS / ACE2 in the Female Reproductive System
Abstract
Objective: The purpose of this review was to investigate current knowledge of COVID-19 by highlighting its effect on female reproductive tract.
Materials and methods: In this study, all articles related to the effect of SARS, MERS, and CoV-19 viruses on the female reproductive system from 2003 to 2021 were reviewed.
Results: The coronavirus enters the host cell by binding to the enzyme that is most abundant in the host lung. The corona or spike (S) protein of this virus is the main tool for binding to the receptor in the host cell membrane and facility the entrance of CoV into the target cells. This receptor is the Angiotensin-Converting Enzyme-2 (ACE2), but the high expression of this receptor can be a mystery to increase infection in host cells. The overexpression of ACE2 in different tissues has a close connection to the severity of this viral infection. Infection in the female reproductive system requires more attention because it may affect the generation and future progeny by damaged gametes.
Conclusion: The existing evidence proposes that ACE2 is widely expressed in the reproductive tract includes: ovary, uterus, vagina, and placenta.
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5. Yoshimura Y. The Ovarian renin–angiotensin system in reproductive physiology. Front Neuroendocrinol 1997; 18: 247-91.
6. Kobayashi S, Moriya H, Nakabayashi I, Nishiyama J, Fukuda T. Angiotensin II and IGF-I may interact to regulate tubulointerstitial cell kinetics and phenotypic changes in hypertensive rats. Hypertens Res 2002; 25: 257-69.
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36. Guo B, Zhang XM, Li SJ, Tian XC, Wang ST, Li DD, et al. Expression and regulation of Ang-2 in murine ovaries during sexual maturation and development of corpus luteum. Mol Biol (Mosk) 2012; 46: 900-6.
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2. Soubrier F, Alhenc-Gelas F, Hubert C, Allegrini J, John M, Tregear G, et al. Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc Natl Acad Sci USA 1988; 85: 9386-90.
3. Dzau VJ.Angiotensin converting enzyme inhibitors and the cardiovascular system. J Hypertens Suppl 1992; 10: S3–10.
4. Wang W, McKinnie SM, Farhan M, Paul M, McDonald T, McLean B, et al. Angiotensin-Converting Enzyme 2 Metabolizes and Partially Inactivates Pyr-Apelin-13 and Apelin-17: Physiological Effects in the Cardiovascular System. Hypertension 2016; 68: 365–77.
5. Yoshimura Y. The Ovarian renin–angiotensin system in reproductive physiology. Front Neuroendocrinol 1997; 18: 247-91.
6. Kobayashi S, Moriya H, Nakabayashi I, Nishiyama J, Fukuda T. Angiotensin II and IGF-I may interact to regulate tubulointerstitial cell kinetics and phenotypic changes in hypertensive rats. Hypertens Res 2002; 25: 257-69.
7. Li YH, Jiao LH, Liu RH, Chen XL, Wang H, Wang WH. Localization of angiotensin II in pig ovary and its effects on oocyte maturation in vitro. Theriogenology 2004; 61: 447–59.
8. Pereira VM, Reis FM, Santos RA, Cassali GD, Santos SH, Honorato-Sampaio K, et al. Gonadotropin stimulation increases the expression of angiotensin-(1–7) and MAS receptor in the rat ovary. Reprod Sci 2009; 16: 1165–74.
9. Yoshimura T, Ito M, Matsui K, Fujisaki S. Effects of highly purified eicosapentaenoic acid on vascular reactivity to angiotensin II and norepinephrine in pregnant rabbits. Prostaglandins 1986; 32: 179-88.
10. Obermuller N, Gentili M, Gauer S, Gretz N, Weigel M, Geiger H, et al. Immuno-histochemical and mRNA localization of the angiotensin II receptor subtype 2 (AT2) in follicular granulosa cells of the rat ovary. J Histochem Cytochem 2004; 52: 545–8.
11. Ferreira R, Gasperin B, Santos J, Rovani M, Santos RA, Gutierrez K, et al. Angiotensin II profile and mRNA encoding RAS proteins during bovine follicular wave. J Renin Angiotensin Aldosterone Syst 2011; 12: 475-82.
12. de Gooyer TE, Skinner SL, Wlodek ME, Kelly DJ, Wilkinson-Berka JL. Angiotensin II influences ovarian follicle development in the transgenic (mRen-2)27 and Sprague-Dawley rat. J Endocrinol 2004; 180: 311–24.
13. Kotani E, Sugimoto M, Kamata H, Fujii N, Saitoh M, Usuki S, et al. Biological roles of angiotensin II via its type 2 receptor during rat follicle atresia. Am J Physiol 1999; 276: E25–33.
14. Domińska K. Involvement of ACE2/Ang-(1-7)/MAS1 Axis in the Regulation of Ovarian Function in Mammals. Int J Mol Sci 2020, 21: 4572.
15. Hayashi K, Miyamoto A, Berisha B, Kosmann MR, Okuda K, Schams D. Regulation of angiotensin II production and angiotensin receptors in microvascular endothelial cells from bovine corpus luteum. Biol Reprod 2000; 62: 162–7.
16. Pawlikowski M, Melen-Mucha G, Mucha S. The involvement of the renin-angiotensin system in the regulation of cell proliferation in the rat endometrium. Cell Mol Life Sci 1999; 55: 506–10.
17. Herr D, Duncan WC, Hack G, Konrad R, Kreienberg R, Wulff C. Regulated expression of the renin-angiotensin-system in human granulosa lutein cells: angiotensin II increases VEGF expression but its synthesis is reduced by hCG. Arch Gynecol Obstet 2010; 281: 409–16.
18. Li XF, Ahmed A. Dual role of angiotensin II in the human endometrium. Hum Reprod 1996; 11Suppl 2: 95-108.
19. Petit A, Geoffroy P, Belisle S. Expression of angiotensin II type-I receptor and phospholipase
C-linked G alpha q/11 protein in the human placenta. J Soc Gynecol Investig 1996; 3: 316–21.
20. Kalenga MK, DE Gasparo M, DE Hertogh R, Whitebread S, Vankrieken L, Thomas K. Les récepteurs de l'angiotensine II dans le placenta humain sont de type AT1 .[Angiotensin II receptors in the human placenta are type AT1]. Reprod Nutr Dev 1991; 31: 257–67.
21. Bokal EV, Vrtovec HM, Virant Klun I, Verdenik I. Prolonged HCG action affects angiogenic substances and improves follicular maturation, oocyte quality and fertilization competence in patients with polycystic ovarian syndrome. Hum Reprod 2005; 20: 1562–81.
22. Herse F, Dechend R, Harsem NK, Wallukat G, Janke J, Qadri F, et al. Dysregulation of the circulating and tissue-based renin-angiotensin system in preeclampsia. Hypertension 2007; 49: 604–11.
23. Chappell S, Morgan L. Searching for genetic clues to the causes of pre-eclampsia. Clin Sci (Lond) 2006; 110: 443-58.
24. Suganuma T, Ino K, Shibata K, Kajiyama H, Nagasaka T, Mizutani S, et al. Functional expression of the angiotensin II type 1 receptor in human ovarian carcinoma cells and its blockade therapy resulting in suppression of tumor invasion, angiogenesis, and peritoneal dissemination. Clin Cancer Res 2005; 11: 2686–94.
25. Shibata K, Kikkawa F, Mizokami Y, Kajiyama H, Ino K, Nomura S, et al. Possible involvement of adipocyte-derived leucine aminopeptidase via angiotensin II in endometrial carcinoma. Tumour Biol 2005; 26:9–16.
26. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, et al. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 2000; 87: E1–9.
27. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis G, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J of Pathol 2004; 203: 631–7.
28. Paul M, Wagner J, Dzau VJ. Gene expression of the renin-angiotensin system in human tissues. Quantitative analysis by the polymerase chain reaction. J Clin Invest 1993; 91: 2058-64.
29. Vickers C, Hales P, Kaushik V, Dick L, Gavin J, Tang J, Godbout K,Parsons T, Baronas E, Hsieh F,et al. Hydrolysis of biological pepti-des by human angiotensin-converting enzyme-related carboxypep-tidase. J Biol Chem 2002; 277: 14838–43.
30. Iwata M, Cowling RT, Gurantz D, Moore C, Zhang S, Yuan JX, et al. Angiotensin-(1-7) binds to specific receptors on cardiac fibroblasts to initiate anti fibrotic and anti-trophic effects. Am J Physiol Heart Circ Physiol 2005; 289: H2356– 63.
31. Liu C, Lv XH, Li HX, Cao X, Zhang F, Wang L, et al . Angiotensin-(1-7) suppresses oxidative stress and improves glucose uptake via Mas receptor in adipocytes. Acta Diabetol 2012; 49: 291–9.
32. Xu J, Fan J, Wu F, Huang Q, Guo M, Lv Z, et al. The ACE2/Angiotensin-(1–7)/Mas Receptor Axis: Pleiotropic Roles in Cancer. Front Physiol 2017; 8: 276.
33. Honorato-Sampaio K, PereiraVM, Santos RA, Reis AM. Evidence that angiotensin-(1-7) is an intermediate of gonadotrophin-induced oocyte maturation in the rat pre-ovulatory follicle. Exp Physiol 2012; 97: 642-50.
34. Hayashi KG, Acosta TJ, Tetsuka M, Berisha B, Matsui M, Schams D, et al. Involvement of angiopoietin-tie system in bovine follicular development and atresia: messenger RNA expression in theca internal and effect on steroid secretion. Biol Reprod 2003; 69: 2078–84.
35. Stefanello JR, Barreta MH, Porciuncula PM, Arruda JN, Oliveira JF, Oliveira MA, et al. Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 2006; 66: 2068–76.
36. Guo B, Zhang XM, Li SJ, Tian XC, Wang ST, Li DD, et al. Expression and regulation of Ang-2 in murine ovaries during sexual maturation and development of corpus luteum. Mol Biol (Mosk) 2012; 46: 900-6.
37. Sugino N, Suzuki T, Sakata A, Miwa I, Asada H, Taketani T, et al. Angiogenesis in the human corpus luteum: changes in expression of angiopoietins in the corpus luteum throughout the menstrual cycle and in early pregnancy. J Clin Endocrinol Metab 2005; 90: 6141–8.
38. Tonellotto dos Santos J, Ferreira R, Gasperin BG, Siqueira LC, de Oliveira JF, Santos RA, et al. Molecular characterization and regulation of the angiotensin-converting enzyme type 2/angiotensin-
(1-7)/MAS receptor axis during the ovulation process in cattle. J Renin Angiotensin Aldosterone Syst 2012; 13: 91–8.
39. Cavallo IK, Dela Cruz C, Oliveira ML, Del Puerto HL, Dias JA, Lobach VN, et al. Angiotensin-(1-7) in human follicular fluid correlates with oocyte maturation. Hum Reprod 2017; 32: 1318–24.
40. Li XF, Ahmed A. Expression of angiotensin II and its receptor subtypes in endometrial hyperplasia: a possible role in dysfunctional menstruation. Lab Invest 1996; 75: 137–45.
41. Vaz-Silva J, Carneiro MM, Ferreira Mc, Pinheiro SV, Silva DA, Silva- Filho AL, et al. The Vasoactive Peptide Angiotensin-(1–7), it's Receptor Mas and the Angiotensin-converting Enzyme Type 2 are Expressed in the Human Endometrium. Reprod Sci 2009; 16: 247-56.
42. Ghadhanfar E, Alsalem A, Al-Kandari S, Naser J, Babiker F, Al-Bader M. The role of ACE2, angiotensin-(1-7) and Mas1 receptor axis in glucocorticoid-induced intrauterine growth restriction. Reprod Biol Endocrinol 2017; 15: 97.
43. Vaswani K, Chan HW, Verma P, Dekker Nitert M, Peiris HN, Wood-Bradley RJ, et al. The rat placental renin-angiotensin system- a gestational gene expression study. Reprod Biol Endocrinol 2015; 13: 89.
44. Valdes G, Neves LA, Anton L, Corthorn J, Chacon C, Germain AM, et al. Distribution of angiotensin-(1-7) and ACE2 in human placentas of normal and pathological pregnancies. Placenta 2006; 27: 200–7.
45. Hering L, Herse F, Geusens N, Verlohren S, Wenzel K, Staff AC, et al. Effects of circulating and local uteroplacental angiotensin II in rat pregnancy. Hypertension 2010; 56: 311–8.
46. Neves LA, Stovall K, Joyner J, Valdes G, Gallagher PE, Ferrario CM, et al. ACE2 and ANG-(1-7) in the rat uterus during early and late gestation. Am J Physiol Regul Integr Comp Physiol 2008; 294: R151–61.
47. Pringle KG, Tadros MA, Callister RJ, Lumbers ER. The expression and localization of the human placental prorenin/renin-angiotensin system throughout pregnancy: roles in trophoblast invasion and angiogenesis? Placenta 2011; 32: 956–62.
48. Sykes SD, Pringle KG, Zhou A, Dekker GA, Roberts CT, Lumbers ER, et al. Fetal sex and the circulating renin-angiotensin system during early gestation in women who later develop preeclampsia or gestational hypertension. J Hum Hypertens 2014; 28: 133–9.
49. Zeng L, Xia S, Yuan W, Yan K, Xiao F, Shao J, et al. Neonatal early-onset infection with SARS-CoV-2 in 33 neonates born to mothers with COVID-19 in Wuhan, China. a. JAMA Pediatr 2020; 174: 722-5.
50. Dong L, Tian J, He S, Zhu C, Wang J, Liu C, et al. Possible vertical transmission of SARS-CoV-2 from an infected mother to her newborn. JAMA 2020; 323:1846-8.
51. Wong FS, Chow KM, Leung TN, Ng WF, Ng TK, Shek CC, et al . Pregnancy and perinatal outcomes of women with severe acute respiratory syndrome. Am J Obstet Gynecol 2004; 191: 292-7.
52. Wong FS, Chow KM, deSwiet M. Severe acute respiratory syndrome and pregnancy.BJOG 2003; 110: 641-2.
53. Beaudette FR, Hudson CB. Cultivation of the virus of infectious bronchitis. Journal of the American Veterinary Medical Association 1937; 90: 51-60.
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| Files | ||
| Issue | Vol 16, No 1 (March 2022) | |
| Section | Review Articles | |
| DOI | https://doi.org/10.18502/jfrh.v16i1.8588 | |
| Keywords | ||
| Reproduction Gonadal Steroid Hormones Coronavirus Renin-Angiotensin System; Angiotensin-Converting Enzyme 2 | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Zafari Zangeneh F. Interaction of SARS-CoV-2 With RAS / ACE2 in the Female Reproductive System. J Family Reprod Health. 2022;16(1):1-8.
