Abstract

Research Article

Modulation of atrial natriuretic peptide receptors in ovarian folliculogenesis

Sung Zoo Kim*

Published: 24 January, 2022 | Volume 6 - Issue 1 | Pages: 001-007

Specific receptors for atrial natriuretic peptide (ANP) located in intra-ovarian tissues are suggested to be involved in ovarian functions such as oocyte maturation and follicle development. However, the characteristics and modulation of its receptor in relation to ovarian folliculogenesis are not well defined. This study examined the properties of ANP receptors in the ovary using quantitative receptor autoradiography. In the pig ovary, the highest binding sites for 125I-ANP(1-28) were localized in the granulosa cell layer of the follicles as well as cumulus oophorous. The binding sites for 125I-ANP(1-28) on theca layer of the ovarian follicles were mainly localized in the external layer, but none was observed in the internal layer. Specific binding of 125I-ANP(1-28) was not found clearly in atretic follicles. In the corpus luteum, the binding site was not observed. Analysis of the competitive inhibition of the binding of 125I-ANP(1-28) to the granulosa and theca externa layers in various preovulatory follicles by increasing concentrations of unlabeled ANP(1-28)
was consistent with a single high affinity for 125I-ANP(1-28). The maximal binding capacities of 125I-ANP(1-28) in granulosa layer were significantly increased in proportion to the development of ovarian follicles. However, no significant difference of binding capacities of 125I-ANP(1-28) was observed in theca externa layer. The binding affinities of 125I-ANP(1-28) in granulosa and theca externa layers were not different from each other. Especially, the correlation between specific binding of 125I-ANP(1-28) and follicle diameter. A significant correlation was revealed between specific binding of 125I-ANP(1-28) and follicle diameter (R = 0.88, p < 0.0001) in granulosa layer, however, less relationship was detected in theca externa layer (R = 0.50, p < 0.0001). Therefore, these results indicate that the biological ANP receptors exist in granulosa and the theca externa layers of the pig ovary, and suggest that the ANP receptors in granulosa layer may be related to the regulatory function of the ovarian follicullogenesis including oocyte maturation.

Read Full Article HTML DOI: 10.29328/journal.icci.1001019 Cite this Article Read Full Article PDF

Keywords:

Natriuretic peptide receptor; Autoradiography; Granulosa layer; Pig ovary

References

  1. McGee EA, Hsueh AJ. Initial and Cyclic Recruitment of Ovarian Follicles. Endocr Rev. 2000; 21: 200-214. PubMed: https://pubmed.ncbi.nlm.nih.gov/10782364/
  2. Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev. 2012; 58: 44-50. PubMed: https://pubmed.ncbi.nlm.nih.gov/22450284/
  3. Hsueh AJ, Kawamura K, Cheng Y, Fauser BC. Intraovarian control of early folliculogenesis. Endocr Rev. 2015; 36: 1-24. PubMed: https://pubmed.ncbi.nlm.nih.gov/25202833/
  4. Potter LR, Yoder AR, Flora DR, Antos LK, Dickey DM. Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb Exp Pharmacol. 2009; 191: 341-66. PubMed: https://pubmed.ncbi.nlm.nih.gov/19089336/
  5. Nakagawa Y, Nishikimi T, Kuwahara K. Atrial and brain natriuretic peptides: Hormones secreted from the heart. Peptides. 2019; 111: 18-25. PubMed: https://pubmed.ncbi.nlm.nih.gov/29859763/
  6. Vollmar AM, Mytzka C, Arendt RM, Schulz R. Atrial natriuretic peptide in bovine corpus luteum. Endocrinology. 1988; 123: 762-767.
  7. Kim SH, Cho KW, Hwang YH, Oh SH, Seul KH, et al. Ovarian atrial natriuretic peptide during the rat estrous cycle. Life Sci. 1992; 51: 1291-1299. PubMed: https://pubmed.ncbi.nlm.nih.gov/1406049/
  8. Kim SH, Cho KW, Lim SH, Hwang YH, Ryu H, et al. Presence and release of immunoreactive atrial natriuretic peptide in granulosa cells of the pig ovarian follicle. Regul Pept. 1992; 42: 153-162.
  9. Ivanova MD, Gregoraszczuk EL, Augustowska K, Kolodziejczyk J, Mollova MV, et al. Localization of atrial natriuretic peptide in pig granulosa cells isolated from ovarian follicles of various size. Reprod Biol. 2003; 3: 173-181. PubMed: https://pubmed.ncbi.nlm.nih.gov/14666140/
  10. Kim SJ, Shinjo M, Usuki S, Tada M, Miyazaki H, et al. Binding sites for atrial natriuretic peptide in high concentrations in human ovary. Biomed Res. 1987; 8: 415-420.
  11. Pandey KN, Osteen KG, Inagami T. Specific receptor-mediated stimulation of progesterone secretion and cGMP accumulation by rat atrial natriuretic factor in cultured human granulosa-lutein (G-L) cells. Endocrinology. 1987; 121:1195-1197. PubMed: https://pubmed.ncbi.nlm.nih.gov/3040379/
  12. Kim SM, Kim SH, Cho KW, Kim SY, Kim SZ. Expression of C-type natriuretic peptide and its specific guanylyl cyclase-coupled receptor in pig ovarian granulosa cells. Insights Clin Cell Immunol. 2018; 2: 14-25. PubMed: https://www.heighpubs.org/hcci/icci-aid1004.php
  13. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. 2010; 330: 366-369. PubMed: https://pubmed.ncbi.nlm.nih.gov/20947764/
  14. Zhang M, Su YQ, Sugiura K, Wigglesworth K, Xia G, et al. Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology. 2011; 152: 4377-4385. PubMed: https://pubmed.ncbi.nlm.nih.gov/21914782/
  15. Liu L, Kong N, Xia G, Zhang M. Molecular control of oocyte meiotic arrest and resumption. Reprod Fertil Dev. 2013; 25: 463-471. PubMed: https://pubmed.ncbi.nlm.nih.gov/23217677/
  16. Brown J, Chen Q. Regional expression of natriuretic peptide receptors during the formation of arterial neointima in the rabbit. Circ Res. 1995; 77: 906-918. PubMed: https://pubmed.ncbi.nlm.nih.gov/7554144/
  17. Cho KW, Kim SH, Kim CH, Koh GY. Mechanical basis of ANP secretion in beating atria: atrial stroke volume and ECF translocation. Am J Physiol. 1995; 268: R1129-R1136. PubMed: https://pubmed.ncbi.nlm.nih.gov/7771572/
  18. Joseph LJ, Desai KB, Mehta MN, Mathiyarasu R. Measurement of specific activity of radiolabelled antigens by a simple radioimmunoassay technique. Nucl Med Biol. 1988; 15: 589-590. PubMed: https://pubmed.ncbi.nlm.nih.gov/3254882/
  19. Brown J, Zuo Z. Natriuretic peptide receptors in the fetal rat. Am J Physiol. 1995; 269: E261-273. PubMed: https://pubmed.ncbi.nlm.nih.gov/7653646/
  20. Kim SZ, Kim SH, Cho KW. Overlapping distribution of receptors for atrial natriuretic peptide and angiotensin II in the kidney and the adrenal gland of the freshwater turtle, Amyda japonica. Gen Comp Endocrinol. 1997; 108: 119-131. PubMed: https://pubmed.ncbi.nlm.nih.gov/9378266/
  21. Benfenati F, Cimino M, Agnati LF, Fuxe K. Quantitative autoradiography of central neurotransmitter receptors: methodological and statistical aspects with special reference to computer-assisted image analysis. Acta Physiol Scand. 1986; 128: 129-146. PubMed: https://pubmed.ncbi.nlm.nih.gov/3022554/
  22. Munson PJ, Rodbard D. Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem. 1980; 107: 220-239. PubMed: https://pubmed.ncbi.nlm.nih.gov/6254391/
  23. Zhang W, Yang Y, Liu W, Chen Q, Wang H, et al. Brain natriuretic peptide and C-type natriuretic peptide maintain porcine oocyte meiotic arrest. J Cell Physiol. 2015; 230: 71-81. PubMed: https://pubmed.ncbi.nlm.nih.gov/24912131/
  24. Noubani A, Farookhi R, Gutkowska J. B-type natriuretic peptide receptor expression and activity are hormonally regulated in rat ovarian cells. Endocrinology. 2000; 141: 551-559. PubMed: https://pubmed.ncbi.nlm.nih.gov/10650935/
  25. Young JM, McNeilly AS. Theca: the forgotten cell of the ovarian follicle. Reproduction. 2010; 140: 489–504. PubMed: https://pubmed.ncbi.nlm.nih.gov/20628033/
  26. Richards JS, Ren YA, Candelaria N, Adams JE, Rajkovic A. Ovarian Follicular Theca Cell Recruitment, Differentiation, and Impact on Fertility: 2017 Update. Endocr Rev. 2018; 39: 1-20. PubMed: https://pubmed.ncbi.nlm.nih.gov/29028960/
  27. Usuki S, Saitoh T, Saitoh M, Tanaka J, Kawakura Y, et al. Endothelin-renin-angiotensin-atrial natriuretic peptide system in ovaries: an intraovarian ERAANP system. J Cardiovasc Pharmacol. 1993; 22 Suppl 8: S207-210. PubMed: https://pubmed.ncbi.nlm.nih.gov/7509946/
  28. Husain A, Bumpus FM, De Silva P, Speth RC. Localization of angiotensin II receptors in ovarian follicles and the identification of angiotensin II in rat ovaries. Proc Natl Acad Sci U S A. 1987; 84: 2489-2493. PubMed: https://pubmed.ncbi.nlm.nih.gov/3470807/
  29. Speth RC, Bumpus FM, Husain A. Identification of angiotensin II receptors in the rat ovary. Eur J Pharmacol. 1986; 130: 351-352. PubMed: https://pubmed.ncbi.nlm.nih.gov/3792456/
  30. Gonçalves PB, Ferreira R, Gasperin B, Oliveira JF. Role of angiotensin in ovarian follicular development and ovulation in mammals: a review of recent advances. Reproduction. 2012; 143: 11-20. PubMed: https://pubmed.ncbi.nlm.nih.gov/22046052/
  31. Tornell J, Carlsson B, Billig H. Atrial natriuretic peptide inhibits spontaneous rat oocyte maturation. Endocrinology. 1990; 126: 1504-1508. PubMed: https://pubmed.ncbi.nlm.nih.gov/2155102/
  32. Zhang M, Tao Y, Xia G, Xie H, Hong H, et al. Atrial natriuretic peptide negatively regulates follicle-stimulating hormone-induced porcine oocyte maturation and cumulus expansion via cGMP-dependent protein kinase pathway. Theriogenology. 2005; 64: 902-916. PubMed: https://pubmed.ncbi.nlm.nih.gov/16054495/
  33. Zhang M, Tao Y, Zhou B, Xie H, Wang F, et al. Atrial natriuretic peptide inhibits the actions of FSH and forskolin in meiotic maturation of pig oocytes via different signalling pathways. J Mol Endocrinol. 2005; 34: 459-472. PubMed: https://pubmed.ncbi.nlm.nih.gov/15821110/
  34. Brenner BM, Ballermann BJ, Gunning ME, Zeidel ML. Diverse biological actions of atrial natriuretic peptide. Physiol Rev. 1990; 70: 665-699. PubMed: https://pubmed.ncbi.nlm.nih.gov/2141944/
  35. Koller KJ, Lowe DG, Bennett GL, et al. Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science. 1991; 252: 120-123. PubMed: https://pubmed.ncbi.nlm.nih.gov/1672777/
  36. Tremblay J, Desjardins R, Hum D, Gutkowska J, Hamet P. Biochemistry and physiology of the natriuretic peptide receptor guanylyl cyclases. Mol Cell Biochem. 2002; 230: 31-47. PubMed: https://pubmed.ncbi.nlm.nih.gov/11952095/
  37. Schulz S. C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides. 2005; 26: 1024-1034. PubMed: https://pubmed.ncbi.nlm.nih.gov/15911070/
  38. Steegers EA, Hollanders JM, Jongsma HW, Hein PR. Atrial natriuretic peptide and progesterone in ovarian follicular fluid. Gynecol Obstet Invest. 1990; 29: 185-187. PubMed: https://pubmed.ncbi.nlm.nih.gov/2141584/

Figures:

Figure 1

Figure 1

Figure 1

Figure 2

Figure 1

Figure 3

Figure 1

Figure 4

Figure 1

Figure 5

Figure 1

Figure 6

Figure 1

Figure 7

Similar Articles

Recently Viewed

Read More

Most Viewed

Read More