Effect of C-type natriuretic peptide on maturation and developmental competence of immature mouse oocytes in vitro
Qiang Wei A B , Chuan Zhou A B , Min Yuan A B , Yuyang Miao A , Xiaoe Zhao A B and Baohua Ma A B C
+ Author Affiliations
- Author Affiliations
A College of Veterinary Medicine, Northwest A&F University, No. 22 Xinong Road, Yangling, Shaanxi, 712100, People’s Republic of China.
B Key Laboratory of Animal Biotechnology, Ministry of Agriculture, No. 22 Xinong Road, Yangling, Shaanxi, 712100, People’s Republic of China.
C Corresponding author. Email: mabh@nwsuaf.edu.cn
*These authors contributed equally to this paper.
Reproduction, Fertility and Development 29(2) 319-324 https://doi.org/10.1071/RD15160
Submitted: 22 April 2015 Accepted: 3 July 2015 Published: 21 August 2015
Abstract
In vitro maturation (IVM) of oocytes is an important assisted reproductive technology for infertility treatment and livestock breeding programs. Because of asynchronous nuclear and cytoplasmic maturation, the developmental competence of oocytes matured in vitro is compromised. C-Type natriuretic peptide (CNP), which has been proved to be an inhibitor of oocyte maturation, provides a new alternative to optimise synchronisation of nuclear and cytoplasmic maturation and improve developmental capacity of immature oocytes in vitro. To investigate the effect of temporary meiotic arrest mediated by CNP on maturation and subsequent development of immature oocytes, immature mouse oocytes from small antral follicles were temporarily arrested in meiosis by CNP (0, 5, 10 and 50 nM) for 24 h and then matured for 16 h. CNP treatment significantly increased the oocyte maturation rate from less than half to above 80%. After IVF, temporary meiotic arrest mediated by 10 and 50 nM CNP significantly improved fertilisation and blastocyst rate of oocytes matured in vitro up to approximately 55% and 30% respectively. Moreover, this positive effect of CNP was attributed, in part, to an increase in the number of mature oocytes with aligned chromosomes and a normal spindle. The present findings indicate the potential to use CNP to improve the efficiency of oocyte IVM.
Additional keywords: blastocyst, cumulus–oocyte complexes, in vitro fertilisation, meiosis, spindle.
References
Albuz, F. K., Sasseville, M., Lane, M., Armstrong, D. T., Thompson, J. G., and Gilchrist, R. B. (2010). Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 25, 2999–3011.| Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbotlKnsg%3D%3D&md5=31e1b4d3e80de984cb6923382dabd13eCAS | 20870682PubMed |
Duncan, F. E., Moss, S. B., and Williams, C. J. (2006). Knockdown of the cAMP dependent protein kinase (PKA) Type I alpha regulatory subunit in mouse oocytes disrupts meiotic arrest and results in meiotic spindle defects. Dev. Dyn. 235, 2961–2968.
| Knockdown of the cAMP dependent protein kinase (PKA) Type I alpha regulatory subunit in mouse oocytes disrupts meiotic arrest and results in meiotic spindle defects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12mt7vI&md5=6c19d5d0bbd864237cbdf2f5f0bb7d5cCAS | 16937372PubMed |
Egbert, J. R., Shuhaibar, L. C., Edmund, A. B., Van Helden, D. A., Robinson, J. W., Uliasz, T. F., Baena, V., Geerts, A., Wunder, F., Potter, L. R., and Jaffe, L. A. (2014). Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes. Development 141, 3594–3604.
| Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVWltrzF&md5=74b61e76b5fc16992f50d1766ac4db39CAS | 25183874PubMed |
Eppig, J. J., Schultz, R. M., O’Brien, M., and Chesnel, F. (1994). Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol. 164, 1–9.
| Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3pvFSjtA%3D%3D&md5=9fe69aee2fd22d00cf74ec0c4a70cb45CAS | 8026614PubMed |
Franciosi, F., Coticchio, G., Lodde, V., Tessaro, I., Modina, S. C., Fadini, R., Dal Canto, M., Renzini, M. M., Albertini, D. F., and Luciano, A. M. (2014). Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol. Reprod. 91, 61.
| Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes.Crossref | GoogleScholarGoogle Scholar | 25078681PubMed |
Gharibi, S. h., Hajian, M., Ostadhosseini, S., Hosseini, S. M., Forouzanfar, M., and Nasr-Esfahani, M. H. (2013). Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology 80, 302–312.
| Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnslequ7g%3D&md5=5c0937fd48845da62db48b7823dfa7a9CAS | 23683693PubMed |
Gilchrist, R. B. (2011). Recent insights into oocyte–follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev. 23, 23–31.
| Recent insights into oocyte–follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 21366977PubMed |
Giritharan, G., Talbi, S., Donjacour, A., Di Sebastiano, F., Dobson, A. T., and Rinaudo, P. F. (2007). Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction 134, 63–72.
| Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFGis74%3D&md5=f2976153fb2a48a279b1604aafcb4ad0CAS | 17641089PubMed |
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 |
Hodges, C. A., Ilagan, A., Jennings, D., Keri, R., Nilson, J., and Hunt, P. A. (2002). Experimental evidence that changes in oocyte growth influence meiotic chromosome segregation. Hum. Reprod. 17, 1171–1180.
| Experimental evidence that changes in oocyte growth influence meiotic chromosome segregation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383ktlWruw%3D%3D&md5=4034ec65d688d40605d028a8f4717098CAS | 11980735PubMed |
Jurema, M. W., and Nogueira, D. (2006). In vitro maturation of human oocytes for assisted reproduction. Fertil. Steril. 86, 1277–1291.
| In vitro maturation of human oocytes for assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 16996508PubMed |
Kastrop, P. M. M., Bevers, M. M., Desetree, O. H. J., and Kruip, T. A. M. (1991). Protein synthesis and phosphorylation patterns of bovine oocytes matured in vivo. Mol. Reprod. Dev. 29, 271–275.
| Protein synthesis and phosphorylation patterns of bovine oocytes matured in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvV2ru78%3D&md5=3caa6b2b9c662204ce085eeff9b3d1f3CAS |
Kawamura, K., Cheng, Y., Kawamura, N., Takae, S., Okada, A., Kawagoe, Y., Mulders, S., Terada, Y., and Hsueh, A. J. (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 |
Kiyosu, C., Tsuji, T., Yamada, K., Kajita, S., and Kunieda, T. (2012). CNP/NPR2 signaling is essential for oocyte meiotic arrest and cumulus oophorus formation during follicular development in the mouse ovary. Reproduction 144, 187–193.
| CNP/NPR2 signaling is essential for oocyte meiotic arrest and cumulus oophorus formation during follicular development in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Klu7fL&md5=b740255ed6e41a160281402ba38ccb9aCAS | 22696190PubMed |
Liu, L., Kong, N., Xia, G., and Zhang, M. (2013). Molecular control of oocyte meiotic arrest and resumption. Reprod. Fertil. Dev. 25, 463–471.
| 1:CAS:528:DC%2BC3sXjslejtr0%3D&md5=ffe99be56f24fc192bc0a62a6ca7d177CAS | 23217677PubMed |
Lodde, V., Modina, S., Galbusera, C., Franciosi, F., and Luciano, A. M. (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74, 740–749.
| Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVGrt7c%3D&md5=acd192f5161cd87e0a825da63f5d0791CAS | 17075796PubMed |
Luciano, A. M., Modina, S., Vassena, R., Milanesi, E., Lauria, A., and Gandolfi, F. (2004). Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol. Reprod. 70, 465–472.
| Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsl2juw%3D%3D&md5=0c0400c8cf76f5100912d4412ae400ebCAS | 14568913PubMed |
Nogueira, D., and Vanhoutte, L. (2009). Use of phosphodiesterase type 3 inhibitor to improve IVM outcome: experimental set up matters. Fertil. Steril. 91, e3.
| Use of phosphodiesterase type 3 inhibitor to improve IVM outcome: experimental set up matters.Crossref | GoogleScholarGoogle Scholar | 19342017PubMed |
Nogueira, D., Cortvrindt, R., De Matos, D. G., Vanhoutte, L., and Smitz, J. (2003). Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol. Reprod. 69, 2045–2052.
| Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCnsbg%3D&md5=787e4a4d863ff130b1231ccc0ed35354CAS | 12930710PubMed |
Nogueira, D., Ron-El, R., Friedler, S., Schachter, M., Raziel, A., Cortvrindt, R., and Smitz, J. (2006). Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol. Reprod. 74, 177–184.
| Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCjsrfO&md5=5c191452c502950dd4f7f7f8d3ec1806CAS | 16207840PubMed |
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 |
Rose, R. D., Gilchrist, R. B., Kelly, J. M., Thompson, J. G., and Sutton-McDowall, M. L. (2013). Regulation of sheep oocyte maturation using cAMP modulators. Theriogenology 79, 142–148.
| Regulation of sheep oocyte maturation using cAMP modulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsF2ru7vI&md5=372c669a837758589e9146d7a1d66f4bCAS | 23102843PubMed |
Sanfins, A., Lee, G. Y., Plancha, C. E., Overstrom, E. W., and Albertini, D. F. (2003). Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes. Biol. Reprod. 69, 2059–2067.
| Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCnsbY%3D&md5=2976474c9697e6afb806c15ba4d42b24CAS | 12930715PubMed |
Sanfins, A., Plancha, C. E., Overstrom, E. W., and Albertini, D. F. (2004). Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: insights into the relationship between nuclear and cytoplasmic quality. Hum. Reprod. 19, 2889–2899.
| Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: insights into the relationship between nuclear and cytoplasmic quality.Crossref | GoogleScholarGoogle Scholar | 15388682PubMed |
Schatten, H., and Sun, Q. Y. (2011). Centrosome dynamics during mammalian oocyte maturation with a focus on meiotic spindle formation. Mol. Reprod. Dev. 78, 757–768.
| Centrosome dynamics during mammalian oocyte maturation with a focus on meiotic spindle formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7rJ&md5=b1541544a1af6b6d0f03bdc34beae411CAS | 21887720PubMed |
Sirard, M. A., Florman, H. M., Leibfried-Rutledge, M. L., Barnes, F. L., Sims, M. L., and First, N. L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.
| Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlsFWitLo%3D&md5=13d51a1a5b7fc82497d8c866ea576366CAS | 2775818PubMed |
Trounson, A., Anderiesz, C., and Jones, G. (2001). Maturation of human oocytes in vitro and their developmental competence. Reproduction 121, 51–75.
| Maturation of human oocytes in vitro and their developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslakuw%3D%3D&md5=dde7e6da624b5a33862dba224fd1a91fCAS | 11226029PubMed |
Vanhoutte, L., De Sutter, P., Nogueira, D., Gerris, J., Dhont, M., and Van der Elst, J. (2007). Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor. Hum. Reprod. 22, 1239–1246.
| Nuclear and cytoplasmic maturation of in vitro matured human oocytes after temporary nuclear arrest by phosphodiesterase 3-inhibitor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntlWmsrs%3D&md5=5155387beeafe68358264f08b9f8d438CAS | 17303631PubMed |
Vanhoutte, L., Nogueira, D., Gerris, J., Dhont, M., and De Sutter, P. (2008). Effect of temporary nuclear arrest by phosphodiesterase 3-inhibitor on morphological and functional aspects of in vitro matured mouse oocytes. Mol. Reprod. Dev. 75, 1021–1030.
| Effect of temporary nuclear arrest by phosphodiesterase 3-inhibitor on morphological and functional aspects of in vitro matured mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsVWjtrY%3D&md5=6ee3423c58bebeb876e19c76964106eaCAS | 18163445PubMed |
Vanhoutte, L., Nogueira, D., Dumortier, F., and De Sutter, P. (2009). Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor. Hum. Reprod. 24, 1946–1959.
| Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVartLg%3D&md5=c55e1d527e859c71a53f818d98a4304cCAS | 19395363PubMed |
Walls, M., Junk, S., Ryan, J. P., and Hart, R. (2012). IVF versus ICSI for the fertilization of in-vitro matured human oocytes. Reprod. Biomed. Online 25, 603–607.
| IVF versus ICSI for the fertilization of in-vitro matured human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s%2FkvFOlsA%3D%3D&md5=555b1dae7189cc3f40d6e616b474c188CAS | 23063820PubMed |
Zeng, H. T., Ren, Z., Guzman, L., Wang, X., Sutton-McDowall, M. L., Ritter, L. J., De Vos, M., Smitz, J., Thompson, J. G., and Gilchrist, R. B. (2013). Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum. Reprod. 28, 1536–1545.
| Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotlOgtLg%3D&md5=d7c81fd3aca94f690bcd5e5a83a42e39CAS | 23559189PubMed |
Zeng, H. T., Richani, D., Sutton-McDowall, M. L., Ren, Z., Smitz, J. E., Stokes, Y., Gilchrist, R. B., and Thompson, J. G. (2014). Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol. Reprod. 91, 47.
| Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 24966394PubMed |
Zhang, M., Su, Y. Q., Sugiura, K., Xia, G., and Eppig, J. J. (2010). Granulosa cell ligand CNP and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330, 366–369.
| Granulosa cell ligand CNP 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 |
Zhong, Y., Lin, J., Liu, X., Hou, J., Zhang, Y., and Zhao, X. (2015). C-Type natriuretic peptide maintains domestic cat oocytes in meiotic arrest. Reprod. Fertil. Dev. , .
| C-Type natriuretic peptide maintains domestic cat oocytes in meiotic arrest.Crossref | GoogleScholarGoogle Scholar | 25873238PubMed |
