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Morpho-molecular evaluation for developmental competence of oocytes retrieved through transvaginal ovum pick-up from FSH-stimulated Tharparkar donor cows (Bos indicus)

Published online by Cambridge University Press:  29 October 2024

Manoj Donadkar ,
Brijesh Kumar Open the ORCID record for Brijesh Kumar [Opens in a new window] ,
Sanjay Kumar Singh ,
Pradeep Chandra ,
Pradeep Dangi ,
Mohan Gawai ,
Amala Jackson ,
Nancy Jasrotia ,
Shweta Sharma  and
Vikrant Chouhan
...Show all authors
Manoj Donadkar
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Brijesh Kumar*
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Sanjay Kumar Singh
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Pradeep Chandra
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Pradeep Dangi
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Mohan Gawai
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Amala Jackson
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Nancy Jasrotia
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Shweta Sharma
Affiliation:
Division of Physiology and Climatology, ICAR- IVRI, Izatnagar 243122, India
Vikrant Chouhan
Affiliation:
Division of Physiology and Climatology, ICAR- IVRI, Izatnagar 243122, India
M.K. Patra
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
Meraj Haider Khan
Affiliation:
Animal Reproduction Division, ICAR- Indian Veterinary Research Institute (ICAR-IVRI), Izatnagar 243122, India
*
Corresponding author: Brijesh Kumar; Email: [email protected]
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Summary

The study was conducted on indigenous Tharparkar cow (Bos indicus) to evaluate FSH stimulation on follicular attributes, oocyte recovery and morpho-molecular developmental competence parameters concerning oocyte quality. A total of 20 OPU sessions were performed, which included 10 sessions in each FSH stimulated at the dose of 130 µg divided into four sub-doses and non-stimulated. Findings on the size of follicles having ≥6 mm showed a significantly higher, however an opposite trend was observed in the case of smaller sized follicle (<6 mm) between stimulated and non-stimulated respectively. The stimulated cows had a significantly higher number as well as the percentage of oocytes of Grade A, having a diameter ≥120 µm and BCB+VE as compared to the non-stimulated cows. The relative mRNA expression profile of GDF9, BMP15, PCNA and BCL-2 genes was higher and BAX was lower in the FSH-stimulated cow. These results indicated that FSH stimulation before OPU in Bos indicus cows has a significant impact on follicle size, oocyte yield, recovery, and their quality with respect to COC’s, diameter and BCB+VE oocytes. Further, a significant increase in the relative mRNA expression levels of GDF9, BMP15 and PCNA genes in the FSH-stimulated group suggests that FSH plays a key role in modulating the expression of these important candidate genes and thus influencing oocyte quality. The higher mRNA expression of BCL-2 genes and concomitantly lower expression of BAX gene in FSH Stimulated cows indicates the protective role of these genes and preventing programmed cell death and thus promoting cell survival, quality and embryo development.

Keywords

BCB stainingcandidate genesFSH stimulatedoocyte developmental competencetransvaginal oocyte retrieval
Type
Research Article
Information
Zygote , Volume 32 , Issue 5 , October 2024 , pp. 376 - 385
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Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Aguila, L., Treulen, F., Therrien, J., Felmer, R., Valdivia, M. and Smith, L. C. (2020) Oocyte selection for in vitro embryo production in bovine species: noninvasive approaches for new challenges of oocyte competence. Animals 10(12), 2196.CrossRefGoogle ScholarPubMed
Alm, H., Torner, H., Lohrke, B., Viergutz, T., Ghoneim, I. M. and Kanitz, W. (2005) Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology 63(8), 2194–2205.CrossRefGoogle ScholarPubMed
Alves, G. P., Cordeiro, F. B., de Lima, C. B., Annes, K., Dos Santos, É. C., Ispada, J. and Milazzotto, M. P. (2019) Follicular environment as a predictive tool for embryo development and kinetics in cattle. Reproduction, Fertility and Development 31(3), 451–461.CrossRefGoogle ScholarPubMed
Bagg, M. A., Nottle, M. B., Armstrong, D. T. and Grupen, C. G. (2007) Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reproduction, Fertility and Development 19(7), 797–803.CrossRefGoogle ScholarPubMed
Bessa, I. R., Nishimura, R. C., Franco, M. M. and Dode, M. A. N. (2013) Transcription profile of candidate genes for the acquisition of competence during oocyte growth in cattle. Reproduction in Domestic Animals 48(5), 781–789.CrossRefGoogle ScholarPubMed
Bessa, I. R., Nishimura, R. C., Franco, M. M. and Dode, M. A. N. (2013). Transcription profile of candidate genes for the acquisition of competence during oocyte growth in cattle. Reproduction in Domestic Animals, 48(5), 781–789.CrossRefGoogle ScholarPubMed
Bhardwaj, R., Ansari, M. M., Pandey, S., Parmar, M. S., Chandra, V., Kumar, G. S. and Sharma, G. T. (2016) GREM1, EGFR, and HAS2; the oocyte competence markers for improved buffalo embryo production in vitro. Theriogenology 86(8), 2004–2011.CrossRefGoogle ScholarPubMed
Bhojwani, S., Alm, H., Torner, H., Kanitz, W. and Poehland, R. (2007) Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear transfer. Theriogenology 67(2), 341–345.CrossRefGoogle ScholarPubMed
Boldura, O. M., Nica, N., Milovanov, C., Popescu, S., Marc Zarcula, S., Bonca, G. and Tulcan, C. (2016). BCL2 and bax gene expression in cumulus-oocytes complexes in cow, 153-158.Google Scholar
Bols, P. E. J., Vanholder, T., Leroy, J. L. M. R., Aerts, J. M. J. and Van Soom, A. (2003) 218 Ultrasound-guided transvaginal injection of a low dose of FSH-LH into the bovine ovary as an alternative way to stimulate follicular growth: Preliminary results. Reproduction, Fertility and Development 16(2), 230–231.CrossRefGoogle Scholar
Caixeta, E. S., Ripamonte, P., Franco, M. M., Junior, J. B. and Dode, M. A. N. (2009) Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. Reproduction, Fertility and Development 1(5), 655–664.CrossRefGoogle Scholar
Castaneda, C. A., Kaye, P., Pantaleon, M., Phillips, N., Norman, S., Fry, R. and Michael, J. D. (2013) Lipid content, active mitochondria and brilliant cresyl blue staining in bovine oocytes. Theriogenology 79(3), 417–422.CrossRefGoogle ScholarPubMed
Cavalieri, F. L. B., Morotti, F., Seneda, M. M., Colombo, A. H. B., Andreazzi, M. A., Emanuelli, I. P. and Rigolon, L. P. (2018) Improvement of bovine in vitro embryo production by ovarian follicular wave synchronization prior to ovum pick-up. Theriogenology 117, 57–60.CrossRefGoogle ScholarPubMed
Chaubal, S. A., Ferre, L. B., Molina, J. A., Faber, D. C., Bols, P. E. J., Rezamand, P. and Yang, X. (2007) Hormonal treatments for increasing the oocyte and embryo production in an OPU–IVP system. Theriogenology 67(4), 719–728.CrossRefGoogle Scholar
Chu, T., Dufort, I. and Sirard, M. A. (2012) Effect of ovarian stimulation on oocyte gene expression in cattle. Theriogenology 77(9), 1928–1938.CrossRefGoogle ScholarPubMed
De Bem, T. H. C., Adona, P. R., Bressan, F. F., Mesquita, L. G., Chiaratti, M. R., Meirelles, F. V. and Leal, C. L. V. (2014) The influence of morphology, follicle size and Bcl-2 and bax transcripts on the developmental competence of bovine Oocytes. Reproduction in Domestic Animals 49(4), 576–583.CrossRefGoogle ScholarPubMed
de Moraes, M.E.B., Adona, P.R., Guemra, S., De Bem, T.H.C. and dos Santos Miranda, M. (2019) Effect of single dose follicle stimulating hormone on follicular aspiration, in vitro fertilization and pregnancy rate. Brazilian Journal of Veterinary Research and Animal Science 56(3), 156894–156894.CrossRefGoogle Scholar
Demetrio, D. G. B., Hasler, J. F., Oliveira, M., Demetrio, C. G. B., Fonseca, J. C. and Santos, R. M. (2021) 145 Comparison of single to multiple injections of follicle-stimulating hormone before ovum pickup in Holstein heifers: Oocyte recovery and embryo production. Reproduction Fertility and Development 33(2), 180–181.CrossRefGoogle Scholar
Fair, T. (2018) Molecular and endocrine determinants of oocyte competence. Animal Reproduction 10(3), 277–282.Google Scholar
Fair, T., Hyttel, P. and Greve, T. (1995) Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Molecular Reproduction and Development 42(4), 437–442.CrossRefGoogle ScholarPubMed
Fry, R. C. (2020) Gonadotropin priming before OPU: what are the benefits in cows and calves?. Theriogenology 150, 236–240.CrossRefGoogle ScholarPubMed
Gilchrist, R. B., Ritter, L. J., Cranfield, M., Jeffery, L. A., Amato, F., Scott, S. J. and Ritvos, O. (2004) Immunoneutralization of growth differentiation factor 9 reveals it partially accounts for mouse oocyte mitogenic activity. Biology of reproduction 71(3), 732–739.CrossRefGoogle ScholarPubMed
Gode, F., Gulekli, B., Dogan, E., Korhan, P., Dogan, S., Bige, O. and Atabey, N. (2011) Influence of follicular fluid GDF9 and BMP15 on embryo quality. Fertility and Sterility 95(7), 2274–2278.CrossRefGoogle ScholarPubMed
Hadimani, M. R., Khillare, K. P., Amle, M. B., Meshram, M. D., Rangnekar, M. N., Mali, A. B. and Nimbalkar, V. G. (2022) Transvaginal ultrasound guided ovum-pick up in cows. The Pharma Innovation 11(3), 756–758.Google Scholar
Harkal, S. B., Pawshe, C. H., Ingawale, M. V., Deshmukh, S. G., Ambalkar, M. B. and Kale, S. D. (2019) Effect of frequency of follicular aspiration on recovery of oocytes and follicular development. Journal of Entomology and Zoology Studies 7 (6), 568–571.Google Scholar
Hayden, C. B., Sala, R. V., Absalón-Medina, V. A., Motta, J. C., Pereira, D., Moreno, J. F. and García-Guerra, A. (2022) Synchronization of follicle wave emergence before ovarian superstimulation with FSH and ovum pick-up improves in vitro embryo production in pregnant heifers. Theriogenology 188, 71–78.CrossRefGoogle ScholarPubMed
Hussein, T. S., Thompson, J. G. and Gilchrist, R. B. (2006) Oocyte-secreted factors enhance oocyte developmental competence. Developmental biology 296(2), 514–521.CrossRefGoogle ScholarPubMed
Kang, S. S., Kim, U. H., Lee, S. D., Lee, M. S., Han, M. H. and Cho, S. R. (2019) Recovery efficiency of cumulus oocyte complexes (COCs) according to collection frequency for Ovum Pick-up (OPU) method in Hanwoo cow. Journal of Animal Reproduction and Biotechnology 34(4), 300–304.CrossRefGoogle Scholar
Khurchabilig, A., Sato, A., Ashibe, S., Hara, A., Fukumori, R. and Nagao, Y. (2020) Expression levels of FSHR, IGF1R, CYP11al and HSD3β in cumulus cells can predict in vitro developmental competence of bovine oocytes. Zygote 28(5), 425–431.CrossRefGoogle Scholar
Krishna, N. V., Rao, M. M., Veerabramhaiah, K., Kumar, R. S., Srikanth, N. R. and Yasaswini, D. (2023) Effect of FSH stimulation prior to ovum pick-up on follicular dynamics, oocyte competence, and in vitro embryo production in Ongole cows (Bos indicus). Journal of Animal and Feed Sciences 32(4), 354–362.CrossRefGoogle Scholar
Kussano, N. R., Leme, L. O., Guimarães, A. L. S., Franco, M. M. and Dode, M. A. N. (2016) Molecular markers for oocyte competence in bovine cumulus cells. Theriogenology 85(6), 1167–1176.CrossRefGoogle ScholarPubMed
Landeo, L., Zuñiga, M., Gastelu, T., Artica, M., Ruiz, J., Silva, M. and Ratto, M. H. (2022) Oocyte Quality, In Vitro Fertilization and Embryo Development of Alpaca Oocytes Collected by Ultrasound-Guided Follicular Aspiration or from Slaughterhouse Ovaries. Animals 12(9), 1102.CrossRefGoogle ScholarPubMed
Li, F., Chen, X., Pi, W., Liu, C. and Shi, Z. (2007) Collection of Oocytes Through Transvaginal Ovum Pick-up for In Vitro Embryo Production in Nanyang Yellow Cattle. Reproduction in Domestic Animals 42(6), 666–670.CrossRefGoogle ScholarPubMed
Manik, R. S., Singla, S. K. and Palta, P. (2003) Collection of oocytes through transvaginal ultrasound-guided aspiration of follicles in an Indian breed of cattle. Animal Reproduction Science 76(3-4), 155–161.CrossRefGoogle Scholar
Manjunatha, B. M., Gupta, P. S. P., Devaraj, M., Ravindra, J. P. and Nandi, S. (2007) Selection of developmentally competent buffalo oocytes by brilliant cresyl blue staining before IVM. Theriogenology 68(9), 1299–1304.CrossRefGoogle ScholarPubMed
Matoba, S., Bender, K., Fahey, A. G., Mamo, S., Brennan, L., Lonergan, P. and Fair, T. (2014) Predictive value of bovine follicular components as markers of oocyte developmental potential. Reproduction, Fertility and Development 26(2), 337–345.CrossRefGoogle ScholarPubMed
Melo, E. O., Cordeiro, D. M., Pellegrino, R., Wei, Z., Daye, Z. J., Nishimura, R. C. and Dode, M. A. N. (2017) Identification of molecular markers for oocyte competence in bovine cumulus cells. Animal Genetics 48(1), 19–29.CrossRefGoogle ScholarPubMed
Nivet, A. L., Bunel, A., Labrecque, R., Belanger, J., Vigneault, C., Blondin, P. and Sirard, M. A. (2012) FSH withdrawal improves developmental competence of oocytes in the bovine model. Reproduction 143(2), 165.CrossRefGoogle ScholarPubMed
Nogueira, B. G. R., de Souza, L. F. A., Puelker, R. Z., Giometti, I. C., Firetti, S. M. G., Dias, T. S. D. S. B. and Castilho, C. (2021) Factors affecting the in vitro production of bovine embryos in a commercial program. Research, Society and Development 10(2), e16110212264–e16110212264.CrossRefGoogle Scholar
Oktay, K., Schenken, R. S. and Nelson, J. F. (1995) Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biology of reproduction 53(2), 295–301.CrossRefGoogle ScholarPubMed
Oliveira, L. H., Sanches, C. P., Seddon, A. S., Veras, M. B., Lima, F. A., Monteiro, P. L. Jr and Sartori, R. (2016) Follicle superstimulation before ovum pick-up for in vitro embryo production in Holstein cows. Journal of Dairy Science 99(11), 9307–9312.CrossRefGoogle ScholarPubMed
Ongaratto, F. L., Cedeño, A. V., Rodriguez-Villamil, P., Tríbulo, A. and Bó, G. A. (2020) Effect of FSH treatment on cumulus oocyte complex recovery by ovum pick up and in vitro embryo production in beef donor cows. Animal Reproduction Science 214, 106274.CrossRefGoogle ScholarPubMed
Opiela, J., Kątska-Książkiewicz, L., Lipiński, D., Słomski, R., Bzowska, M. and Ryńska, B. (2008) Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis-related genes Bcl-2 and Bax, and developmental competence following IVP in cattle. Theriogenology 69(5), 546–555.CrossRefGoogle ScholarPubMed
Orozco-Lucero, E. and Sirard, M. A. (2018) Molecular markers of fertility in cattle oocytes and embryos: progress and challenges. Animal Reproduction 11(3), 183–194.Google Scholar
Otoi, T., Yamamoto, K., Koyama, N., Tachikawa, S. and Suzuki, T. (1997) Bovine oocyte diameter in relation to developmental competence. Theriogenology 48(5), 769–774.CrossRefGoogle ScholarPubMed
Patil, S. P., Hadiya, K. K., Layek, S. S., Gorani, S., Raj, S., Karuppanasamy, K. and Gupta, R. O. (2022) Ovum Pick-Up and In Vitro Embryo Production from Stimulated Vs Non-Stimulated Buffaloes. Indian Journal of Biotechnology 18(1), 95–100.Google Scholar
Pfeffer, P. L., Sisco, B., Donnison, M., Somers, J. and Smith, C. (2007) Isolation of genes associated with developmental competency of bovine oocytes. Theriogenology 68: S84–S90.CrossRefGoogle ScholarPubMed
Qi, M., Yao, Y., Ma, H., Wang, J., Zhao, X., Liu, L. and Sun, F. (2013) Transvaginal ultrasound-guided ovum pick-up (OPU) in cattle. Journal of Biomimetics, Biomaterials and Biomedical Engineering 18(2), 1000118.Google Scholar
Rajput, S. K., Lee, K., Zhenhua, G., Di, L., Folger, J. K. and Smith, G. W. (2014) Embryotropic actions of follistatin: paracrine and autocrine mediators of oocyte competence and embryo developmental progression. Reproduction, Fertility and Development 26(1), 37–47.CrossRefGoogle Scholar
Robker, R.L. and Richards, J.S. (1998) Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27KIP1. Molecular Endocrinology 12, 924–940.CrossRefGoogle ScholarPubMed
Ruvolo, G., Fattouh, R. R., Bosco, L., Brucculeri, A. M. and Cittadini, E. (2013) New molecular markers for the evaluation of gamete quality. Journal of Assisted Reproduction and Genetics 30, 207–212.CrossRefGoogle ScholarPubMed
Saini, N., Singh, M. K., Shah, S. M., Singh, K. P., Kaushik, R., Manik, R. S. and Chauhan, M. S. (2015) Developmental competence of different quality bovine oocytes retrieved through ovum pick-up following in vitro maturation and fertilization. Animal 9(12), 1979–1985.CrossRefGoogle ScholarPubMed
Sendag, S., Cetin, Y., Alan, M., Hadeler, K. G. and Niemann, H. (2008) Effects of eCG and FSH on ovarian response, recovery rate and number and quality of oocytes obtained by ovum pick-up in Holstein cows. Animal Reproduction Science 106(1-2), 208–214.CrossRefGoogle ScholarPubMed
Silva-Santos, K. C., Santos, G. M. G., Koetz Júnior, C., Morotti, F., Siloto, L. S., Marcantonio, T. N. and Seneda, M. M. (2014) Antral follicle populations and embryo production–in vitro and in vivo–of Bos indicus–taurus donors from weaning to yearling ages. Reproduction in Domestic Animals 49(2), 228–232.CrossRefGoogle ScholarPubMed
Sirait, B., Wiweko, B., Jusuf, A. A., Iftitah, D. and Muharam, R. (2021) Oocyte competence biomarkers associated with oocyte maturation: a review. Frontiers in Cell and Developmental Biology 9: 710292.CrossRefGoogle ScholarPubMed
Sodhi, M., Mukesh, M., Kishore, A., Mishra, B.P., Kataria, R.S. and Joshi, B.K. (2013) Novel polymorphisms in UTR and coding region of inducible heat shock protein 70.1 gene in tropically adapted Indian zebu cattle (Bos indicus) and riverine buffalo (Bubalus bubalis). Gene 527(2), 606–615.CrossRefGoogle ScholarPubMed
Su, Y. Q., Sugiura, K., Li, Q., Wigglesworth, K., Matzuk, M. M. and Eppig, J. J. (2010) Mouse oocytes enable LH-induced maturation of the cumulus-oocyte complex via promoting EGF receptor-dependent signaling. Journal of Molecular Endocrinology’s 24(6), 1230–1239.CrossRefGoogle ScholarPubMed
Sugimura, S., Kobayashi, N., Okae, H., Yamanouchi, T., Matsuda, H., Kojima, T. and Gilchrist, R. B. (2017) Transcriptomic signature of the follicular somatic compartment surrounding an oocyte with high developmental competence. Scientific Reports 7(1), 6815.CrossRefGoogle ScholarPubMed
Viana, J. H. M., Palhao, M. P., Siqueira, L. G. B., Fonseca, J. F. D. and Camargo, L. D. A. (2010) Ovarian follicular dynamics, follicle deviation, and oocyte yield in Gyr breed (Bos indicus) cows undergoing repeated ovum pick-up. Theriogenology 73(7), 966–972.CrossRefGoogle ScholarPubMed
Vieira, L. M., Rodrigues, C. A., Netto, A. C., Guerreiro, B. M., Silveira, C. R. A., Freitas, B. G., and Baruselli, P. S. (2016). Efficacy of a single intramuscular injection of porcine FSH in hyaluronan prior to ovum pick-up in Holstein cattle. Theriogenology, 85(5), 877–886.CrossRefGoogle ScholarPubMed
Vieira, L. M., Rodrigues, C. A., Netto, A. C., Guerreiro, B. M., Silveira, C. R. A., Moreira, R. J. C. and Baruselli, P. S. (2014) Superstimulation prior to the ovum pick-up to improve in vitro embryo production in lactating and non-lactating Holstein cows. Theriogenology 82(2), 318–324.CrossRefGoogle Scholar
Wang, Q. and Sun, Q. Y. (2006) Evaluation of oocyte quality: morphological, cellular and molecular predictors. Reproduction, Fertility and Development 19(1), 1–12.CrossRefGoogle Scholar
Wood, R. D. and Shivji, M. K. (1997) Which DNA polymerases are used for DNA-repair in eukaryotes. Carcinogenesis 18(4), 605–610.CrossRefGoogle ScholarPubMed
Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J. and Wang, X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275(5303), 1129–1132.CrossRefGoogle ScholarPubMed
Yang, Y., Kanno, C., Huang, W., Kang, S. S., Yanagawa, Y. and Nagano, M. (2016) Effect of bone morphogenetic protein-4 on in vitro growth, steroidogenesis and subsequent developmental competence of the oocyte-granulosa cell complex derived from bovine early antral follicles. Reproductive Biology and Endocrinology 14(1), 1–8.CrossRefGoogle ScholarPubMed
Yoshino, O., McMahon, H. E., Sharma, S. and Shimasaki, S. (2006) A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. The Proceedings of the National Academy of Sciences 103(28), 10678–10683.CrossRefGoogle Scholar