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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

C-Type natriuretic peptide maintains domestic cat oocytes in meiotic arrest

Yougang Zhong A B , Jiabao Lin B , Xiaoping Liu B , Jian Hou C , Yong Zhang A and Xingxu Zhao A D
+ Author Affiliations
- Author Affiliations

A College of Veterinary Medicine, Gansu Agricultural University, No.1 Yingmen County, Anning District, Lanzhou 730070, P. R. China.

B College of Veterinary Medicine, China Agricultural University, Yuanmingyuan West Road No. 2, Haidian District, Beijing 100193, P. R. China.

C State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, Yuanmingyuan West Road No. 2, Haidian District, Beijing 100193, P. R. China.

D Corresponding author. Email: zhaoxingxu@126.com

Reproduction, Fertility and Development 28(10) 1553-1559 https://doi.org/10.1071/RD14425
Submitted: 5 November 2014  Accepted: 27 February 2015   Published: 15 April 2015

Abstract

Recent studies have shown that C-type natriuretic peptide (CNP; encoded by the natriuretic peptide C (NPPC) gene) plays an essential role in maintaining meiotic arrest of mouse and porcine oocytes. However, whether CNP inhibits feline meiotic resumption is not known. In the present study we used a domestic cat model to explore the role played by CNP in feline oocyte meiotic resumption. We determined mRNA expression of genes encoding CNP and its cognate receptor natriuretic peptide receptor 2 (NPR2) in antral follicles. NPPC mRNA was primarily expressed in mural granulosa cells, whereas NPR2 mRNA was predominantly expressed in cumulus cells. Following in vitro culture for 24 h, 100 nM CNP increased cGMP levels, and maintained meiotic arrest of oocytes associated with cumulus cells. When the duration of in vitro culture increased from 24 h to 36 h, the ability of CNP to maintain meiotic arrest decreased, and this was accompanied by a decrease in the steady state levels of NPR2 mRNA in cumulus cells. In addition, CNP decreased the rate of degeneration of oocytes. These results indicate that CNP is required to maintain meiotic arrest and prevent degeneration in domestic cat oocytes.

Additional keywords: meiosis, natriuretic peptide receptor 2.


References

Ali, A., and Sirard, M. A. (2002). Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation. Biol. Reprod. 66, 901–905.
Effect of the absence or presence of various protein supplements on further development of bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCltLs%3D&md5=ea9f5bc0a8ea59174ce03559d241b944CAS | 11906907PubMed |

Alm, H., Choi, Y. H., Love, L., Heleil, B., Torner, H., and Hinrichs, K. (2008). Holding bovine oocytes in the absence of maturation inhibitors: kinetics of in vitro maturation and effect on blastocyst development after in vitro fertilization. Theriogenology 70, 1024–1029.
Holding bovine oocytes in the absence of maturation inhibitors: kinetics of in vitro maturation and effect on blastocyst development after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFajurjI&md5=f891d661e0a60130aed3d44bee3bf7cdCAS | 18644621PubMed |

Anasti, J. N. (1998). Premature ovarian failure: an update. Fertil. Steril. 70, 1–15.
Premature ovarian failure: an update.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czitFynuw%3D%3D&md5=64c6213070ef33f4df0857ceb911c2bbCAS | 9660412PubMed |

Cho, W. K., Stern, S., and Biggers, J. D. (1974). Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187, 383–386.
Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXktFSit7s%3D&md5=54a18c1f361c91212e757f1e404b4f23CAS | 4362350PubMed |

Dekel, N., and Beers, W. H. (1978). Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins. Proc. Natl Acad. Sci. USA 75, 4369–4373.
Rat oocyte maturation in vitro: relief of cyclic AMP inhibition by gonadotropins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXmtV2ntbg%3D&md5=89f5ad6fb41fa2636aaff01d726c9872CAS | 212746PubMed |

Edwards, R. G. (1965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–351.
Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF287lsVagsg%3D%3D&md5=8f4e859fc27a77c86561604b6e71fe15CAS | 4957259PubMed |

Eppig, J. J. (1989). The participation of cyclic adenosine monophosphate (cAMP) in the regulation of meiotic maturation of oocytes in the laboratory mouse. J. Reprod. Fertil. Suppl. 38, 3–8.
| 1:CAS:528:DyaL1MXlvFaitbs%3D&md5=136f8dfb5185a9a7f43575d324cab408CAS | 2552109PubMed |

Eppig, J. J., and Downs, S. M. (1987). The effect of hypoxanthine on mouse oocyte growth and development in vitro: maintenance of meiotic arrest and gonadotropin-induced oocyte maturation. Dev. Biol. 119, 313–321.
The effect of hypoxanthine on mouse oocyte growth and development in vitro: maintenance of meiotic arrest and gonadotropin-induced oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtFersbY%3D&md5=8b1050378da2e5347696a6deaa6d2255CAS | 3100361PubMed |

Gómez, M. C., Pope, C. E., and Dresser, B. L. (2006). Nuclear transfer in cats and its application. Theriogenology 66, 72–81.
Nuclear transfer in cats and its application.Crossref | GoogleScholarGoogle Scholar | 16620927PubMed |

Hegele-Hartung, C., Kuhnke, J., Lessl, M., Grondahl, C., Ottesen, J., Beier, H. M., Eisner, S., and Eichenlaub-Ritter, U. (1999). Nuclear and cytoplasmic maturation of mouse oocytes after treatment with synthetic meiosis-activating sterol in vitro. Biol. Reprod. 61, 1362–1372.
Nuclear and cytoplasmic maturation of mouse oocytes after treatment with synthetic meiosis-activating sterol in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFertLw%3D&md5=f79b9ae7b88ea05606477aefc1b6ebf8CAS | 10529286PubMed |

Herrick, J. R. (2014). Reversible meiotic arrest in feline oocytes. Reprod. Fertil. Dev. 26, 258–267.
Reversible meiotic arrest in feline oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtFCmtQ%3D%3D&md5=60e59d1091ee04621983c5808b498dfeCAS | 23327827PubMed |

Hinckley, M., Vaccari, S., Horner, K., Chen, R., and Conti, M. (2005). The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev. Biol. 287, 249–261.
The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Ght7fK&md5=d69fae71fae3ea16a63840441c851c73CAS | 16229830PubMed |

Hiradate, Y., Hoshino, Y., Tanemura, K., and Sato, E. (2014). C-Type natriuretic peptide inhibits porcine oocyte meiotic resumption. Zygote 22, 372–377.
C-Type natriuretic peptide inhibits porcine oocyte meiotic resumption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKhsLfF&md5=7792f58c7c138531c786f60051cad544CAS | 23331536PubMed |

Huang, W., Nagano, M., Kang, S. S., Yanagawa, Y., and Takahashi, Y. (2014). Prematurational culture with 3-isobutyl-1-methylxanthine synchronizes meiotic progression of the germinal vesicle stage and improves nuclear maturation and embryonic development in in vitro-grown bovine oocytes. J. Reprod. Dev. 60, 9–13.
Prematurational culture with 3-isobutyl-1-methylxanthine synchronizes meiotic progression of the germinal vesicle stage and improves nuclear maturation and embryonic development in in vitro-grown bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnslKktb0%3D&md5=a6bb84d876a3dbfc72f2ae1f962aecb2CAS | 24212477PubMed |

Kawamura, K., Cheng, Y., Kawamura, N., Takae, S., Okada, A., Kawagoe, Y., Mulders, S., Terada, Y., and Hsueh, A. J. W. (2011). Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes. Hum. Reprod. 26, 3094–3101.
Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGktbrI&md5=88586e0307cb5acef28dac85b9e297e5CAS | 21865234PubMed |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=6db539426b70529f14f65734e4c1d0f6CAS | 11846609PubMed |

Magnusson, C., and Hillensjo, T. (1977). Inhibition of maturation and metabolism in rat oocytes by cyclic AMP. J. Exp. Zool. 201, 139–147.
Inhibition of maturation and metabolism in rat oocytes by cyclic AMP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXls1Wrurw%3D&md5=a6f897bffe875b8b53943093e0ace4aeCAS | 196033PubMed |

McGee, E., Spears, N., Minami, S., Hsu, S. Y., Chun, S. Y., Billig, H., and Hsueh, A. J. (1997). Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′,5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology 138, 2417–2424.
| 1:CAS:528:DyaK2sXjsVeitLc%3D&md5=8e563539ab8b94162c1b8f0a55587d70CAS | 9165031PubMed |

Mehlmann, L. M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–799.
Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt12nsg%3D%3D&md5=61121f4380f8ed09af6ae5eddb9e4d03CAS | 16322539PubMed |

Mehlmann, L. M., Saeki, Y., Tanaka, S., Brennan, T. J., Evsikov, A. V., Pendola, F. L., Knowles, B. B., Eppig, J. J., and Jaffe, L. A. (2004). The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306, 1947–1950.
The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCqtbvE&md5=f2286891d51c88ba9db6de62f7872610CAS | 15591206PubMed |

Norris, R. P., Ratzan, W. J., Freudzon, M., Mehlmann, L. M., Krall, J., Movsesian, M. A., Wang, H., Ke, H., Nikolaev, V. O., and Jaffe, L. A. (2009). Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136, 1869–1878.
Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1aktbw%3D&md5=b04e8786cd9c95e01d7f3724b51bce2cCAS | 19429786PubMed |

Norris, R. P., Freudzon, M., Nikolaev, V. O., and Jaffe, L. A. (2010). Epidermal growth factor receptor kinase activity is required for gap junction closure and for part of the decrease in ovarian follicle cGMP in response to LH. Reproduction 140, 655–662.
Epidermal growth factor receptor kinase activity is required for gap junction closure and for part of the decrease in ovarian follicle cGMP in response to LH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsbfP&md5=48c79f7c8004b7dd06a99181bf95d937CAS | 20826538PubMed |

O’Brien, S. J., Menotti-Raymond, M., Murphy, W. J., and Yuhki, N. (2002). The Feline Genome Project. Annu. Rev. Genet. 36, 657–686.
The Feline Genome Project.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjslertQ%3D%3D&md5=0aad84db431d168d9546db43df9af963CAS | 12359739PubMed |

Pincus, G., and Enzmann, E. V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs. J. Exp. Med. 62, 665–675.
The comparative behavior of mammalian eggs in vivo and in vitro: I. The activation of ovarian eggs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3crjs1agtA%3D%3D&md5=f69e85b92f859503c9c464bd1bd5fd3eCAS | 19870440PubMed |

Pope, C. E. (2000). Embryo technology in conservation efforts for endangered felids. Theriogenology 53, 163–174.
Embryo technology in conservation efforts for endangered felids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFantA%3D%3D&md5=51fbe6996298a77e8626895914666703CAS | 10735071PubMed |

Potter, L. R. (1998). Phosphorylation-dependent regulation of the guanylyl cyclase-linked natriuretic peptide receptor B: dephosphorylation is a mechanism of desensitization. Biochemistry 37, 2422–2429.
Phosphorylation-dependent regulation of the guanylyl cyclase-linked natriuretic peptide receptor B: dephosphorylation is a mechanism of desensitization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotFKmtQ%3D%3D&md5=b8f27987531ad87a5bac0a2d9117b741CAS | 9485390PubMed |

Potter, L. R., Yoder, A. R., Flora, D. R., Antos, L. K., and Dickey, D. M. (2009). Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handb. Exp. Pharmacol. 191, 341–366.
Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlaisb8%3D&md5=d660eb495b4f46cf3083ddedf2ccc126CAS | 19089336PubMed |

Richard, F. J., Tsafriri, A., and Conti, M. (2001). Role of phosphodiesterase type 3A in rat oocyte maturation. Biol. Reprod. 65, 1444–1451.
Role of phosphodiesterase type 3A in rat oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVers7w%3D&md5=d847447d2275c237c388d327df4b96cbCAS | 11673261PubMed |

Robinson, J. W., Zhang, M., Shuhaibar, L. C., Norris, R. P., Geerts, A., Wunder, F., Eppig, J. J., Potter, L. R., and Jaffe, L. A. (2012). Luteinizing hormone reduces the activity of the NPR2 guanylyl cyclase in mouse ovarian follicles, contributing to the cyclic GMP decrease that promotes resumption of meiosis in oocytes. Dev. Biol. 366, 308–316.
Luteinizing hormone reduces the activity of the NPR2 guanylyl cyclase in mouse ovarian follicles, contributing to the cyclic GMP decrease that promotes resumption of meiosis in oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xms12lu7o%3D&md5=57390f6139f0f90cab78e739732453fdCAS | 22546688PubMed |

Ryle, M. (1973). Gonadotropins and ovarian function. Acta Eur. Fertil. 4, 113–122.
| 1:STN:280:DyaE2c7lsVejsg%3D%3D&md5=cbe5d19853144cd5ecd21271ff07d2f3CAS | 4363470PubMed |

Sato, Y., Cheng, Y., Kawamura, K., Takae, S., and Hsueh, A. J. (2012). C-type natriuretic peptide stimulates ovarian follicle development. Mol. Endocrinol. 26, 1158–1166.
C-type natriuretic peptide stimulates ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVegsrzM&md5=1a2026d894bc843046ed9bf5ca9dcafcCAS | 22595960PubMed |

Shitsukawa, K., Andersen, C. B., Richard, F. J., Horner, A. K., Wiersma, A., van Duin, M., and Conti, M. (2001). Cloning and characterization of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte. Biol. Reprod. 65, 188–196.
Cloning and characterization of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWhtbo%3D&md5=cef13a343764d60fc399c1bae57f8518CAS | 11420239PubMed |

Sirard, M. A., and First, N. L. (1988). In vitro inhibition of oocyte nuclear maturation in the bovine. Biol. Reprod. 39, 229–234.
In vitro inhibition of oocyte nuclear maturation in the bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXls1Cgsr0%3D&md5=3a34c5e599d6a8579125d9974882b6ecCAS | 2460146PubMed |

Vaccari, S., Weeks, J. L., Hsieh, M., Menniti, F. S., and Conti, M. (2009). Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol. Reprod. 81, 595–604.
Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu7zE&md5=f91ef08cea4c4919e46c618b975c0139CAS | 19474061PubMed |

Zhang, M., Su, Y. Q., Sugiura, K., Xia, G., and Eppig, J. J. (2010). Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–369.
Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OisL7P&md5=ff45ea07f80955438b79460bedb9c0cfCAS | 20947764PubMed |

Zhang, M., Su, Y. Q., Sugiura, K., Wigglesworth, K., Xia, G., and Eppig, J. J. (2011). Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro. Endocrinology 152, 4377–4385.
Estradiol promotes and maintains cumulus cell expression of natriuretic peptide receptor 2 (NPR2) and meiotic arrest in mouse oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOrtb3J&md5=65a326f536e0716872df17aade969ecdCAS | 21914782PubMed |

Zhang, W., Chen, Q., Yang, Y., Liu, W., Zhang, M., Xia, G., and Wang, C. (2014). Epidermal growth factor-network signaling mediates luteinizing hormone regulation of BNP and CNP and their receptor NPR2 during porcine oocyte meiotic resumption. Mol. Reprod. Dev. 81, 1030–1041.
Epidermal growth factor-network signaling mediates luteinizing hormone regulation of BNP and CNP and their receptor NPR2 during porcine oocyte meiotic resumption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVykt7%2FM&md5=909298102d6fd5c417e89e97d91799ebCAS | 25348585PubMed |

Zhang, W., Yang, Y., Liu, W., Chen, Q., Wang, H., Wang, X., Zhang, Y., Zhang, M., and Xia, G. (2015). Brain natriuretic peptide and C-type natriuretic peptide maintain porcine oocyte meiotic arrest. J. Cell. Physiol. 230, 71–81.
Brain natriuretic peptide and C-type natriuretic peptide maintain porcine oocyte meiotic arrest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1eisb7M&md5=4bae71711e7476d5f928933d6f114b31CAS | 24912131PubMed |