Evidence that angiotensin-(1-7) is an intermediate of gonadotrophin-induced oocyte maturation in the rat preovulatory follicle

Experimental Physiology

Volumn 97, Issue 5, 2012, Pages 642-650

  Honorato Sampaio, Kinulpe ^a   Pereira, Virginia M ^a   Santos, Robson A S ^a   Reis, Adelina M ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7]; CHORIONIC GONADOTROPIN; ESTRADIOL; LUTEINIZING HORMONE; MESSENGER RNA; PROGESTERONE; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GERMINAL VESICLE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MEIOSIS; NONHUMAN; OOCYTE; OOCYTE MATURATION; OVARY FOLLICLE; RAT; REAL TIME POLYMERASE CHAIN REACTION;

EID: 84860320527     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2011.061960     Document Type: Article

References (49)

1. Billig H, Furuta I & Hsueh AJ (1993). Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133, 2204-2212.
2. Botelho LM, Block CH, Khosla MC & Santos RA (1994). Plasma angiotensin(1-7) immunoreactivity is increased by salt load, water deprivation, and hemorrhage. Peptides 15, 723-729.
3. Brosnihan KB, Neves LA, Joyner J, Averill DB, Chappell MC, Sarao R, Penninger J & Ferrario CM (2003). Enhanced renal immunocytochemical expression of ANG-(1-7) and ACE2 during pregnancy. Hypertension 42, 749-753.
4. Costa AP, Fagundes-Moura CR, Pereira VM, Silva LF, Vieira MA, Santos RA & Dos Reis AM (2003). Angiotensin-(1-7): a novel peptide in the ovary. Endocrinology 144, 1942-1948.
5. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE & Acton S (2000). A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87, E1-E9.
6. Edson MA, Nagaraja AK & Matzuk MM (2009). The mammalian ovary from genesis to revelation. Endocr Rev 30, 624-712.
7. 2. Endocrinology 99, 452-458.
8. Fortune JE & Armstrong DT (1977). Androgen production by theca and granulosa isolated from proestrous rat follicles. Endocrinology 100, 1341-1347.
9. Fraga-Silva RA, Costa-Fraga FP, De Sousa FB, Alenina N, Bader M, Sinisterra RD & Santos RA (2011). An orally active formulation of angiotensin-(1-7) produces an antithrombotic effect. Clinics (Sao Paulo) 66, 837-841.
10. Franke TF, Kaplan DR & Cantley LC (1997). PI3K: downstream AKTion blocks apoptosis. Cell 88, 435-437.
11. Gall L, Boulesteix C, Ruffini S & Germain G (2005). EGF-induced EGF-receptor and MAP kinase phosphorylation in goat cumulus cells during in vitro maturation. Mol Reprod Dev 71, 489-494.
12. 1 and Mas receptors. Am J Physiol Heart Circ Physiol 293, H1154-H1163.
13. Giometti IC, Bertagnolli AC, Ornes RC, da Costa LF, Carambula SF, Reis AM, de Oliveira JF, Emanuelli IP & Goncalves PB (2005). Angiotensin II reverses the inhibitory action produced by theca cells on bovine oocyte nuclear maturation. Theriogenology 63, 1014-1025.
14. Glorioso N, Atlas SA, Laragh JH, Jewelewicz R & Sealey JE (1986). Prorenin in high concentrations in human ovarian follicular fluid. Science 233, 1422-1424.
15. Hoshino Y, Yokoo M, Yoshida N, Sasada H, Matsumoto H & Sato E (2004). Phosphatidylinositol 3-kinase and Akt participate in the FSH-induced meiotic maturation of mouse oocytes. Mol Reprod Dev 69, 77-86.
16. Itskovitz J, Rubattu S, Rosenwaks Z, Liu HC & Sealey JE (1991). Relationship of follicular fluid prorenin to oocyte maturation, steroid levels, and outcome of in vitro fertilization. J Clin Endocrinol Metab 72, 165-171.
17. Johnson AL & Bridgham JT (2002). Caspase-mediated apoptosis in the vertebrate ovary. Reproduction 124, 19-27.
18. Joyner J, Neves LA, Granger JP, Alexander BT, Merrill DC, Chappell MC, Ferrario CM, Davis WP & Brosnihan KB (2007). Temporal-spatial expression of ANG-(1-7) and angiotensin-converting enzyme 2 in the kidney of normal and hypertensive pregnant rats. Am J Physiol Regul Integr Comp Physiol 293, R169-R177.
19. Kalous J, Solc P, Baran V, Kubelka M, Schultz RM & Motlik J (2006). PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol Cell 98, 111-123.
20. Kucharewicz I, Pawlak R, Matys T, Pawlak D & Buczko W (2002). Antithrombotic effect of captopril and losartan is mediated by angiotensin-(1-7). Hypertension40, 774-779.
21. Kuji N, Sueoka K, Miyazaki T, Tanaka M, Oda T, Kobayashi T & Yoshimura Y (1996). Involvement of angiotensin II in the process of gonadotropin-induced ovulation in rabbits. Biol Reprod 55, 984-991.
22. Lehr HA, Mankoff DA, Corwin D, Santeusanio G & Gown AM (1997). Application of Photoshop-based image analysis to quantification of hormone receptor expression in breast cancer. J Histochem Cytochem 45, 1559-1565.
23. Li M, Liang CG, Xiong B, Xu BZ, Lin SL, Hou Y, Chen DY, Schatten H & Sun QY (2008). PI3-kinase and mitogen-activated protein kinase in cumulus cells mediate EGF-induced meiotic resumption of porcine oocyte. Domest Anim Endocrinol 34, 360-371.
24. Li YH, Jiao LH, Liu RH, Chen XL, Wang H & Wang WH (2004). Localization of angiotensin II in pig ovary and its effects on oocyte maturation in vitro. Theriogenology 61, 447-459.
25. Lightman A, Jones CL, MacLusky NJ, Palumbo A, DeCherney AH & Naftolin F (1988). Immunocytochemical localization of angiotensin II immunoreactivity and demonstration of angiotensin II binding in the rat ovary. Am J Obstet Gynecol 159, 526-530.
26. Lightman A, Tarlatzis BC, Rzasa PJ, Culler MD, Caride VJ, Negro-Vilar AF, Lennard D, DeCherney AH & Naftolin F (1987). The ovarian renin-angiotensin system: renin-like activity and angiotensin II/III immunoreactivity in gonadotropin-stimulated and unstimulated human follicular fluid. Am J Obstet Gynecol 156, 808-816.
27. T method. Methods 25, 402-408.
28. Peluso JJ & Pappalardo A (1994). Progesterone and cell-cell adhesion interact to regulate rat granulosa cell apoptosis. Biochem Cell Biol 72, 547-551.
29. Pereira VM, Reis FM, Santos RA, Cassali GD, Santos SH, Honorato-Sampaio K & dos Reis AM (2009). Gonadotropin stimulation increases the expression of angiotensin-(1-7) and MAS receptor in the rat ovary. Reprod Sci 16, 1165-1174.
30. Picciarelli-Lima P, Oliveira AG, Reis AM, Kalapothakis E, Mahecha GA, Hess RA & Oliveira CA (2006). Effects of 3-beta-diol, an androgen metabolite with intrinsic estrogen-like effects, in modulating the aquaporin-9 expression in the rat efferent ductules. Reprod Biol Endocrinol 4, 51.
31. Quirk SM, Cowan RG, Harman RM, Hu CL & Porter DA (2004). Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J Anim Sci 82 E-Suppl, E40-E52.
32. Reis FM, Bouissou DR, Pereira VM, Camargos AF, dos Reis AM & Santos RA (2011). Angiotensin-(1-7), its receptor Mas, and the angiotensin-converting enzyme type 2 are expressed in the human ovary. Fertil Steril 95, 176-181.
33. Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL & Touyz RM (2007). Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49, 185-192.
34. Santos RA, Ferreira AJ & Simoes ESAC (2008). Recent advances in the angiotensin-converting enzyme 2-angiotensin(1-7)-Mas axis. Exp Physiol 93, 519-527.
35. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R & Walther T (2003). Angiotensin (1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci U S A 100, 8258-8263.
36. Sealey JE, Atlas SA, Glorioso N, Manapat H & Laragh JH (1985). Cyclical secretion of prorenin during the menstrual cycle: synchronization with luteinizing hormone and progesterone. Proc Natl Acad Sci U S A 82, 8705-8709.
37. Shimada M & Terada T (2001). Phosphatidylinositol 3-kinase in cumulus cells and oocytes is responsible for activation of oocyte mitogen-activated protein kinase during meiotic progression beyond the meiosis I stage in pigs. Biol Reprod 64, 1106-1114.
38. Stefanello JR, Barreta MH, Porciuncula PM, Arruda JN, Oliveira JF, Oliveira MA & Goncalves PB (2006). Effect of angiotensin II with follicle cells and insulin-like growth factor-I or insulin on bovine oocyte maturation and embryo development. Theriogenology 66, 2068-2076.
39. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G & Turner AJ (2000). A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J BiolChem 275, 33238-33243.
40. Tonellotto Dos Santos J, Ferreira R, Gasperin BG, Siqueira LC, de Oliveira JF, Santos RA, Reis AM & Goncalves PB (2011). 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, doi:.
41. Vaz-Silva J, Carneiro MM, Ferreira MC, Pinheiro SV, Silva DA, Silva-Filho AL, Witz CA, Reis AM, Santos RA & Reis FM (2009). The vasoactive peptide angiotensin-(1-7), its receptor Mas and the angiotensin-converting enzyme type 2 are expressed in the human endometrium. Reprod Sci 16, 247-256.
42. Viana GE, Pereira VM, Honorato-Sampaio K, Oliveira CA, Santos RA & Reis AM (2011). Angiotensin-(1-7) induces ovulation and steroidogenesis in perfused rabbit ovaries. Exp Physiol 96, 957-965.
43. Yoshimura Y (1997). The ovarian renin-angiotensin system in reproductive physiology. Front Neuroendocrinol 18, 247-291.
44. Yoshimura Y, Karube M, Aoki H, Oda T, Koyama N, Nagai A, Akimoto Y, Hirano H & Nakamura Y (1996). Angiotensin II induces ovulation and oocyte maturation in rabbit ovaries via the AT2 receptor subtype. Endocrinology 137, 1204-1211.
45. Yoshimura Y, Karube M, Koyama N, Shiokawa S, Nanno T & Nakamura Y (1992). Angiotensin II directly induces follicle rupture and oocyte maturation in the rabbit. FEBS Lett 307, 305-308.
46. Yoshimura Y, Karube M, Oda T, Koyama N, Shiokawa S, Akiba M, Yoshinaga A & Nakamura Y (1993). Locally produced angiotensin II induces ovulation by stimulating prostaglandin production in in vitro perfused rabbit ovaries. Endocrinology 133, 1609-1616.
47. Yoshimura Y, Koyama N, Karube M, Oda T, Akiba M, Yoshinaga A, Shiokawa S, Jinno M & Nakamura Y (1994). Gonadotropin stimulates ovarian renin-angiotensin system in the rabbit. J Clin Invest 93, 180-187.
48. Yuan JS, Reed A, Chen F & Stewart CN Jr (2006). Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.
49. Zhang M, Ouyang H & Xia G (2009). The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol Hum Reprod 15, 399-409.