Effect of heifer age on the granulosa cell transcriptome after ovarian stimulation
David A. Landry A , Rémi Labrecque B , François-Xavier Grand B , Christian Vigneault B , Patrick Blondin B and Marc-André Sirard A C
+ Author Affiliations
- Author Affiliations
A Centre de recherche en reproduction, développement et santé intergénérationnelle (CRDSI), Département des Sciences Animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, 2325 Rue de l’Université, Québec, G1V0A6, Canada.
B Boviteq Inc., 19320 Rang Grand Saint Francois Ouest, J2T 5H1, Saint-Hyacinthe, Québec, Canada.
C Corresponding author. Email: marc-andre.sirard@fsaa.ulaval.ca
Reproduction, Fertility and Development 30(7) 980-990 https://doi.org/10.1071/RD17225
Submitted: 29 March 2017 Accepted: 17 November 2017 Published: 18 December 2017
Abstract
Genomic selection is accelerating genetic gain in dairy cattle. Decreasing generation time by using younger gamete donors would further accelerate breed improvement programs. Although ovarian stimulation of peripubertal animals is possible and embryos produced in vitro from the resulting oocytes are viable, developmental competence is lower than when sexually mature cows are used. The aim of the present study was to shed light on how oocyte developmental competence is acquired as a heifer ages. Ten peripubertal Bos taurus Holstein heifers underwent ovarian stimulation cycles at the ages of 8, 11 (mean 10.8) and 14 (mean 13.7) months. Collected oocytes were fertilised in vitro with spermatozoa from the same adult male. Each heifer served as its own control. The transcriptomes of granulosa cells recovered with the oocytes were analysed using microarrays. Differential expression of certain genes was measured using polymerase chain reaction. Principal component analysis of microarray data revealed that the younger the animal, the more distinctive the gene expression pattern. Using ingenuity pathway analysis (IPA) and NetworkAnalyst (www.networkanalyst.ca), the main biological functions affected in younger donors were identified. The results suggest that cell differentiation, inflammation and apoptosis signalling are less apparent in peripubertal donors. Such physiological traits have been associated with a lower basal concentration of LH.
Additional keywords: basal LH, dairy cow, embryo transfer, microarray, puberty.
References
Armstrong, D. T., Holm, P., Irvine, B., Petersen, B. A., Stubbings, R. B., McLean, D., Stevens, G., and Seamark, R. F. (1992). Pregnancies and live birth from in vitro fertilization of calf oocytes collected by laparoscopic follicular aspiration. Theriogenology 38, 667–678.| Pregnancies and live birth from in vitro fertilization of calf oocytes collected by laparoscopic follicular aspiration.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvF2gsw%3D%3D&md5=328633e4c1b5d0721338040c6056c183CAS |
Ax, R. L., Armbrust, S., Tappan, R., Gilbert, G., Oyarzo, J. N., Bellin, M. E., Selner, D., and McCauley, T. C. (2005). Superovulation and embryo recovery from peripubertal Holstein heifers. Anim. Reprod. Sci. 85, 71–80.
| Superovulation and embryo recovery from peripubertal Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSntb7F&md5=8b1961b6d094b59b2eae3199cab1895cCAS |
Bennett, J., Baumgarten, S. C., and Stocco, C. (2013). GATA4 and GATA6 silencing in ovarian granulosa cells affects levels of mRNAs involved in steroidogenesis, extracellular structure organization, IGF-I activity, and apoptosis. Endocrinology 154, 4845–4858.
| GATA4 and GATA6 silencing in ovarian granulosa cells affects levels of mRNAs involved in steroidogenesis, extracellular structure organization, IGF-I activity, and apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2itL7F&md5=bea0fa29eab9dad76020e29d855bc355CAS |
Bras, M., Queenan, B., and Susin, S. A. (2005). Programmed cell death via mitochondria: different modes of dying. Biochemistry (Mosc.) 70, 231–239.
| Programmed cell death via mitochondria: different modes of dying.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislamsb4%3D&md5=687ff1c4a01f061932c9ab7d6f5b5358CAS |
Chalhoub, N., and Baker, S. J. (2009). PTEN and the PI3-kinase pathway in cancer. Annu. Rev. Pathol. 4, 127–150.
| PTEN and the PI3-kinase pathway in cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis1aiu78%3D&md5=85d61dfe2b8c0ef59a6fa056363822f6CAS |
Culhane, A. C., Perrière, G., Considine, E. C., Cotter, T. G., and Higgins, D. G. (2002). Between-group analysis of microarray data. Bioinformatics 18, 1600–1608.
| Between-group analysis of microarray data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpslOht7c%3D&md5=898c9edb3f764aa1d5a4833c41b69401CAS |
Dalman, M. R., Deeter, A., Nimishakavi, G., and Duan, Z.-H. (2012). Fold change and P-value cutoffs significantly alter microarray interpretations. BMC Bioinformatics 13, S11.
| Fold change and P-value cutoffs significantly alter microarray interpretations.Crossref | GoogleScholarGoogle Scholar |
Day, M. L., and Nogueira, G. P. (2013). Management of age at puberty in beef heifers to optimize efficiency of beef production. Anim. Front. 3, 6–11.
| Management of age at puberty in beef heifers to optimize efficiency of beef production.Crossref | GoogleScholarGoogle Scholar |
Dias, F. C. F., Khan, M. I. R., Adams, G. P., Sirard, M. A., and Singh, J. (2014). Granulosa cell function and oocyte competence: super-follicles, super-moms and super-stimulation in cattle. Anim. Reprod. Sci. 149, 80–89.
| Granulosa cell function and oocyte competence: super-follicles, super-moms and super-stimulation in cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M%2Fgt1Kitw%3D%3D&md5=ac0213a005d2c0f4e9075964f983b496CAS |
Douville, G., and Sirard, M.-A. (2014). Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles. J. Ovarian Res. 7, 50.
| Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles.Crossref | GoogleScholarGoogle Scholar |
Fajersson, P., Barradas, H. V., Roman-Ponce, H., and Cook, R. M. (1991). The effects of dietary protein on age and weight at the onset of puberty in Brown Swiss and Zebu heifers in the Tropics. Theriogenology 35, 845–855.
| The effects of dietary protein on age and weight at the onset of puberty in Brown Swiss and Zebu heifers in the Tropics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFOitA%3D%3D&md5=4df91af04a2a0af44acdbff017106f88CAS |
Fan, H.-Y., Shimada, M., Liu, Z., Cahill, N., Noma, N., Wu, Y., Gossen, J., and Richards, J. S. (2008). Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation. Development 135, 2127–2137.
| Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVGhs7g%3D&md5=589ca1ce020384ec3ea1556cd7f1f8a5CAS |
Färkkilä, A., Anttonen, M., Pociuviene, J., Leminen, A., Butzow, R., Heikinheimo, M., and Unkila-Kallio, L. (2011). Vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 are highly expressed in ovarian granulosa cell tumors. Eur. J. Endocrinol. 164, 115–122.
| Vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 are highly expressed in ovarian granulosa cell tumors.Crossref | GoogleScholarGoogle Scholar |
Forman, H. J., Maiorino, M., and Ursini, F. (2010). Signaling functions of reactive oxygen species. Biochemistry 49, 835–842.
| Signaling functions of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1OqsQ%3D%3D&md5=51f7e7ba18d06a075f2d97567ad501b6CAS |
Gandolfi, F., Milanesi, E., Pocar, P., Luciano, A. M., Brevini, T. A., Acocella, F., Lauria, A., and Armstrong, D. T. (1998). Comparative analysis of calf and cow oocytes during in vitro maturation. Mol. Reprod. Dev. 49, 168–175.
| Comparative analysis of calf and cow oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1OktQ%3D%3D&md5=7727be103881ae897a166edeb9603efeCAS |
García-Ruiz, A., Cole, J. B., VanRaden, P. M., Wiggans, G. R., Ruiz-López, F. J., and Van Tassell, C. P. (2016). Changes in genetic selection differentials and generation intervals in US Holstein dairy cattle as a result of genomic selection. Proc. Natl Acad. Sci. USA 113, E3995–E4004.
| Changes in genetic selection differentials and generation intervals in US Holstein dairy cattle as a result of genomic selection.Crossref | GoogleScholarGoogle Scholar |
Glister, C., Hatzirodos, N., Hummitzsch, K., Knight, P. G., and Rodgers, R. J. (2014). The global effect of follicle-stimulating hormone and tumour necrosis factor α on gene expression in cultured bovine ovarian granulosa cells. BMC Genomics 15, 72.
| The global effect of follicle-stimulating hormone and tumour necrosis factor α on gene expression in cultured bovine ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Greenaway, J., Connor, K., Pedersen, H. G., Coomber, B. L., LaMarre, J., and Petrik, J. (2004). Vascular endothelial growth factor and its receptor, Flk-1/KDR, are cytoprotective in the extravascular compartment of the ovarian follicle. Endocrinology 145, 2896–2905.
| Vascular endothelial growth factor and its receptor, Flk-1/KDR, are cytoprotective in the extravascular compartment of the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12gu7w%3D&md5=56c4e7a5cc66b38108f201071a20335fCAS |
Guerrero-Netro, H. M., Chorfi, Y., and Price, C. A. (2015). Effects of the mycotoxin deoxynivalenol on steroidogenesis and apoptosis in granulosa cells. Reproduction 149, 555–561.
| Effects of the mycotoxin deoxynivalenol on steroidogenesis and apoptosis in granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFamtb%2FF&md5=117d076223084348dd75292ccea5c743CAS |
Hanukoglu, I. (2006). Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab. Rev. 38, 171–196.
| Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktlWlurc%3D&md5=405a706dc5ef14a38d6e81c69acc8fa1CAS |
Jiang, C.-F., Li, D.-M., Shi, Z.-M., Wang, L., Liu, M.-M., Ge, X., Liu, X., Qian, Y.-C., Wen, Y.-Y., Zhen, L.-L., Lin, J., Liu, L. Z., and Jiang, B. H. (2016). Estrogen regulates miRNA expression: implication of estrogen receptor and miR-124/AKT2 in tumor growth and angiogenesis. Oncotarget 7, 36940–36955.
| Estrogen regulates miRNA expression: implication of estrogen receptor and miR-124/AKT2 in tumor growth and angiogenesis.Crossref | GoogleScholarGoogle Scholar |
Kauffold, J., Am, H. A. H., Bergfeld, U., Weber, W., and Sobiraj, A. (2005). The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter. J. Reprod. Dev. 51, 325–332.
| The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter.Crossref | GoogleScholarGoogle Scholar |
Khatir, H., Lonergan, P., Touzé, J. L., and Mermillod, P. (1998). The characterization of bovine embryos obtained from prepubertal calf oocytes and their viability after non surgical embryo transfer. Theriogenology 50, 1201–1210.
| The characterization of bovine embryos obtained from prepubertal calf oocytes and their viability after non surgical embryo transfer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVKisg%3D%3D&md5=b54e3ec9ae3b3ba1567023b276bd7c97CAS |
Labrecque, R., Vigneault, C., Blondin, P., and Sirard, M.-A. (2014). Gene expression analysis of bovine oocytes at optimal coasting time combined with GnRH antagonist during the no-FSH period. Theriogenology 81, 1092–1100.
| Gene expression analysis of bovine oocytes at optimal coasting time combined with GnRH antagonist during the no-FSH period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsF2gu70%3D&md5=460b3db326358da7b787282eeda35b21CAS |
Landry, D. A., Bellefleur, A.-M., Labrecque, R., Grand, F.-X., Vigneault, C., Blondin, P., and Sirard, M.-A. (2016). Effect of cow age on the in vitro developmental competence of oocytes obtained after FSH stimulation and coasting treatments. Theriogenology 86, 1240–1246.
| Effect of cow age on the in vitro developmental competence of oocytes obtained after FSH stimulation and coasting treatments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnslGmur0%3D&md5=d896361de08a68685a8ab351ebf46d4eCAS |
Lévesque, J. T., and Sirard, M. A. (1994). Proteins in oocytes from calves and adult cows before maturation: relationship with their development capacity. Reprod. Nutr. Dev. 34, 133–139.
| Proteins in oocytes from calves and adult cows before maturation: relationship with their development capacity.Crossref | GoogleScholarGoogle Scholar |
Looney, C. R., Damiani, P., Lindsey, B. R., Long, C. R., Gonseth, C. L., Johnson, D. L., and Duby, R. T. (1995). Use of prepuberal heifers as oocyte donors for IVF: effect of age and gonadotrophin treatment. Theriogenology 43, 269.
| Use of prepuberal heifers as oocyte donors for IVF: effect of age and gonadotrophin treatment.Crossref | GoogleScholarGoogle Scholar |
Machelon, V., and Nome, F. (1999). Cellular distribution and relative amounts of vascular endothelium growth factor mRNA in granulosa cells from human preovulatory follicles. Eur. Cytokine Netw. 10, 393–402.
| 1:CAS:528:DyaK1MXms1ajt7k%3D&md5=a1651a1838f863cf05b6600f932ef845CAS |
Majerus, V., De Roover, R., Etienne, D., Kaidi, S., Massip, A., Dessy, F., and Donnay, I. (1999). Embryo production by ovum pick up in unstimulated calves before and after puberty. Theriogenology 52, 1169–1179.
| Embryo production by ovum pick up in unstimulated calves before and after puberty.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvFaksg%3D%3D&md5=34e19e5c707014ec8f220276c782350cCAS |
Manna, P. R., and Stocco, D. M. (2011). The role of specific mitogen-activated protein kinase signaling cascades in the regulation of steroidogenesis. J. Signal Transduct. 2011, Article 821615.
| The role of specific mitogen-activated protein kinase signaling cascades in the regulation of steroidogenesis.Crossref | GoogleScholarGoogle Scholar |
Morin-Doré, L., Blondin, P., Vigneault, C., Grand, F.-X., Labrecque, R., and Sirard, M.-A. (2017). Transcriptomic evaluation of bovine blastocysts obtained from peri-pubertal oocyte donors. Theriogenology 93, 111–123.
| Transcriptomic evaluation of bovine blastocysts obtained from peri-pubertal oocyte donors.Crossref | GoogleScholarGoogle Scholar |
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, 165–171.
| FSH withdrawal improves developmental competence of oocytes in the bovine model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1Kkt70%3D&md5=c7b073398c07d51b7864bd8064c29b87CAS |
Nivet, A.-L., Vigneault, C., Blondin, P., and Sirard, M.-A. (2013). Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine. Reproduction 145, 555–565.
| Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVWmsbnJ&md5=a625f4d7250765ef69d7e5ee473994e5CAS |
Padua, M. B., Fox, S. C., Jiang, T., Morse, D. A., and Tevosian, S. G. (2014). Simultaneous gene deletion of Gata4 and Gata6 leads to early disruption of follicular development and germ cell loss in the murine ovary. Biol. Reprod. 91, 24.
| Simultaneous gene deletion of Gata4 and Gata6 leads to early disruption of follicular development and germ cell loss in the murine ovary.Crossref | GoogleScholarGoogle Scholar |
Palma, G. A., Tortonese, D. J., and Sinowatz, F. (2001). Developmental capacity in vitro of prepubertal oocytes. Anat. Histol. Embryol. 30, 295–300.
| Developmental capacity in vitro of prepubertal oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnjs1Wmtw%3D%3D&md5=eb414f61d349f0280d3b838cc39df7daCAS |
Park, J.-I., Jeon, H.-J., Jung, N.-K., Jang, Y.-J., Kim, J.-S., Seo, Y.-W., Jeong, M., Chae, H. Z., and Chun, S.-Y. (2012). Periovulatory expression of hydrogen peroxide-induced sulfiredoxin and peroxiredoxin 2 in the rat ovary: gonadotropin regulation and potential modification. Endocrinology 153, 5512–5521.
| Periovulatory expression of hydrogen peroxide-induced sulfiredoxin and peroxiredoxin 2 in the rat ovary: gonadotropin regulation and potential modification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Onsb7N&md5=c02923c5832fda2895b7402908eeb6baCAS |
Pearson, G., Robinson, F., Beers Gibson, T., Xu, B. E., Karandikar, M., Berman, K., and Cobb, M. H. (2001). Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153–183.
| 1:CAS:528:DC%2BD3MXjsFSntL4%3D&md5=0ee4c76b745394075c59fd49892fac4cCAS |
Peter, AT, and Dhanasekaran, N (2003). Apoptosis of granulosa cells: a review on the role of MAPK-signalling modules. Reprod. Domest. Anim. 38, 209–213.
| Apoptosis of granulosa cells: a review on the role of MAPK-signalling modules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvFWlu7w%3D&md5=71e8bfd91b43b1351a5c0a041d520f92CAS |
Presicce, G. A., Jiang, S., Simkin, M., Zhang, L., Looney, C. R., Godke, R. A., and Yang, X. (1997). Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves. Biol. Reprod. 56, 386–392.
| Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXosF2nuw%3D%3D&md5=09c04071322a98d86f8078e65874bf45CAS |
Rastelli, L., Valentino, M. L., Minderman, M. C., Landin, J., Malyankar, U. M., Lescoe, M. K., Kitson, R., Brunson, K., Souan, L., Forenza, S., Goldfarb, R. H., and Rabbani, S. A. (2011). A KDR-binding peptide (ST100,059) can block angiogenesis, melanoma tumor growth and metastasis in vitro and in vivo. Int. J. Oncol. 39, 401–408.
| 1:CAS:528:DC%2BC3MXpvVegsb8%3D&md5=65c1a368b7cc86698581f8eb7730b0e8CAS |
Revel, F., Mermillod, P., Peynot, N., Renard, J. P., and Heyman, Y. (1995). Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows. J. Reprod. Fertil. 103, 115–120.
| Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3it1CqsA%3D%3D&md5=b13a4198c197dc559031925c20cac92cCAS |
Richards, J. S., Russell, D. L., Ochsner, S., and Espey, L. L. (2002). Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu. Rev. Physiol. 64, 69–92.
| Ovulation: new dimensions and new regulators of the inflammatory-like response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFGms7Y%3D&md5=9606b94c474fb4684bfb696d9f0ee644CAS |
Robert, C., Nieminen, J., Dufort, I., Gagné, D., Grant, J. R., Cagnone, G., Plourde, D., Nivet, A.-L., Fournier, É., Paquet, É., Blazejczyk, M., Rigault, P., Juge, N., and Sirard, M. A. (2011). Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays. Mol. Reprod. Dev. 78, 651–664.
| Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGns7vK&md5=d72db057b1d58d5b0976820b6cf2acceCAS |
Rodriguez, R. E., and Wise, M. E. (1989). Ontogeny of pulsatile secretion of gonadotropin-releasing hormone in the bull calf during infantile and pubertal development. Endocrinology 124, 248–256.
| Ontogeny of pulsatile secretion of gonadotropin-releasing hormone in the bull calf during infantile and pubertal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXovV2lug%3D%3D&md5=77fe02ea045022021e4dc0f8681919fcCAS |
Ryan, K. E., Casey, S. M., Canty, M. J., Crowe, M. A., Martin, F., and Evans, A. C. O. (2007). Akt and Erk signal transduction pathways are early markers of differentiation in dominant and subordinate ovarian follicles in cattle. Reproduction 133, 617–626.
| Akt and Erk signal transduction pathways are early markers of differentiation in dominant and subordinate ovarian follicles in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1ygurk%3D&md5=cfcef655d87ba5b20812b3af0a092c99CAS |
Sakumoto, R., Shibaya, M., and Okuda, K. (2003). Tumor necrosis factor-alpha (TNF alpha) inhibits progesterone and estradiol-17beta production from cultured granulosa cells: presence of TNFalpha receptors in bovine granulosa and theca cells. J. Reprod. Dev. 49, 441–449.
| Tumor necrosis factor-alpha (TNF alpha) inhibits progesterone and estradiol-17beta production from cultured granulosa cells: presence of TNFalpha receptors in bovine granulosa and theca cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFaiu78%3D&md5=a98d1b3cac042bed8e478a01b3538267CAS |
Salamone, D. F., Damiani, P., Fissore, R. A., Robl, J. M., and Duby, R. T. (2001). Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised. Biol. Reprod. 64, 1761–1768.
| Biochemical and developmental evidence that ooplasmic maturation of prepubertal bovine oocytes is compromised.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgt7g%3D&md5=9462655bee146c21835868cd2d9aaf1eCAS |
Shkolnik, K., Tadmor, A., Ben-Dor, S., Nevo, N., Galiani, D., and Dekel, N. (2011). Reactive oxygen species are indispensable in ovulation. Proc. Natl Acad. Sci. USA 108, 1462–1467.
| Reactive oxygen species are indispensable in ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Smt74%3D&md5=b273709c687b4a768d8e06c1976d079dCAS |
Siemeister, G., Schirner, M., Reusch, P., Barleon, B., Marmé, D., and Martiny-Baron, G. (1998). An antagonistic vascular endothelial growth factor (VEGF) variant inhibits VEGF-stimulated receptor autophosphorylation and proliferation of human endothelial cells. Proc. Natl Acad. Sci. USA 95, 4625–4629.
| An antagonistic vascular endothelial growth factor (VEGF) variant inhibits VEGF-stimulated receptor autophosphorylation and proliferation of human endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXis1Ogsbw%3D&md5=8449226a1fb8d9804a2fbb0667f233e8CAS |
Simón, C., Frances, A., Piquette, G., and Polan, M. L. (1994). Immunohistochemical localization of the interleukin-1 system in the mouse ovary during follicular growth, ovulation, and luteinization. Biol. Reprod. 50, 449–457.
| Immunohistochemical localization of the interleukin-1 system in the mouse ovary during follicular growth, ovulation, and luteinization.Crossref | GoogleScholarGoogle Scholar |
Sirard, M.-A. (2016). Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle. Theriogenology 86, 54–61.
| Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmslKru7k%3D&md5=44e0efa88517a6d7e15fb810521584ebCAS |
Sirard, M.-A., Richard, F., Blondin, P., and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
| Contribution of the oocyte to embryo quality.Crossref | GoogleScholarGoogle Scholar |
Son, D.-S., and Roby, K. F. (2006). Interleukin-1alpha-induced chemokines in mouse granulosa cells: impact on keratinocyte chemoattractant chemokine, a CXC subfamily. Mol. Endocrinol. 20, 2999–3013.
| Interleukin-1alpha-induced chemokines in mouse granulosa cells: impact on keratinocyte chemoattractant chemokine, a CXC subfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFymsbzN&md5=0985cfb6075132f54d99938ee675836bCAS |
Spicer, L. J. (1998). Tumor necrosis factor-alpha (TNF-alpha) inhibits steroidogenesis of bovine ovarian granulosa and thecal cells in vitro. Involvement of TNF-alpha receptors. Endocrine 8, 109–115.
| Tumor necrosis factor-alpha (TNF-alpha) inhibits steroidogenesis of bovine ovarian granulosa and thecal cells in vitro. Involvement of TNF-alpha receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkt1Oju7w%3D&md5=db886645c22f7b1d80b336abe09424a4CAS |
Uma, J., Muraly, P., Verma-Kumar, S., and Medhamurthy, R. (2003). Determination of onset of apoptosis in granulosa cells of the preovulatory follicles in the bonnet monkey (Macaca radiata): correlation with mitogen-activated protein kinase activities. Biol. Reprod. 69, 1379–1387.
| Determination of onset of apoptosis in granulosa cells of the preovulatory follicles in the bonnet monkey (Macaca radiata): correlation with mitogen-activated protein kinase activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2nsbg%3D&md5=a2595e7689893110b0e835b3b7d18640CAS |
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034.1.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |
Wang, L.-Q., Liu, J.-C., Chen, C.-L., Cheng, S.-F., Sun, X.-F., Zhao, Y., Yin, S., Hou, Z.-M., Pan, B., Ding, C., Shen, W., and Zhang, X. F. (2016). Regulation of primordial follicle recruitment by cross-talk between the Notch and phosphatase and tensin homologue (PTEN)/AKT pathways. Reprod. Fertil. Dev. 28, 700–712.
| Regulation of primordial follicle recruitment by cross-talk between the Notch and phosphatase and tensin homologue (PTEN)/AKT pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmsFOlsb0%3D&md5=e6c9385de54487785fcd4d5a1528444fCAS |
Xia, J., Gill, E. E., and Hancock, R. E. W. (2015). NetworkAnalyst for statistical, visual and network-based meta-analysis of gene expression data. Nat. Protoc. 10, 823–844.
| NetworkAnalyst for statistical, visual and network-based meta-analysis of gene expression data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnvFSquro%3D&md5=fddfc0f1cbf9f7b30c6bcbbfcea996eaCAS |
