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

Comparative analysis of granulosa cell gene expression in association with oocyte competence in FSH-stimulated Holstein cows

David A. Landry A , Chloé Fortin A , Anne-Marie Bellefleur B , 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, 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 - https://doi.org/10.1071/RD16459
Submitted: 16 November 2016  Accepted: 9 March 2017   Published online: 19 April 2017

Abstract

Ovarian stimulation with exogenous FSH followed by FSH withdrawal or ‘coasting’ is an effective means of increasing the number of oocytes obtainable for the in vitro production of cattle embryos. However, the quality of the oocytes thus obtained varies considerably from one cow to the next. The aim of the present study was to gain a better understanding of the follicular conditions associated with low oocyte developmental competence. Granulosa cells from 94 Holstein cows in a commercial embryo production facility were collected following ovarian stimulation and coasting. Microarray analysis showed 120 genes expressed with a differential of at least 1.5 when comparing donors of mostly competent with donors of mostly incompetent oocytes. Using ingenuity pathway analysis, we revealed the main biological functions and potential upstream regulators that distinguish donors of mostly incompetent oocytes. These are involved in cell proliferation, apoptosis, lipid metabolism, retinol availability and insulin signalling. In summary, we demonstrated that differences in follicle maturity at collection could explain differences in oocyte competence associated with individual animals. We also revealed deficiencies in lipid metabolism and retinol signalling in granulosa cells from donors of mostly incompetent oocytes.

Additional keywords: follicle, superovulation.


References

Adams, G. P., Matteri, R. L., Kastelic, J. P., Ko, J. C., and Ginther, O. J. (1992). Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers. J. Reprod. Fertil. 94, 177–188.
Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers.CrossRef | 1:CAS:528:DyaK38Xhs1Kltr4%3D&md5=6dc038a7abfbfeaa4d53923e7627b706CAS | open url image1

Ali, A., Lange, A., Gilles, M., and Glatzel, P. S. (2001). Morphological and functional characteristics of the dominant follicle and corpus luteum in cattle and their influence on ovarian function. Theriogenology 56, 569–576.
Morphological and functional characteristics of the dominant follicle and corpus luteum in cattle and their influence on ovarian function.CrossRef | 1:CAS:528:DC%2BD3MXntlahsbw%3D&md5=e4bc60b4c65d44750067ce7c44c6e1dcCAS | open url image1

Anahory, T., Dechaud, H., Bennes, R., Marin, P., Lamb, N. J., and Laoudj, D. (2002). Identification of new proteins in follicular fluid of mature human follicles. Electrophoresis 23, 1197–1202.
Identification of new proteins in follicular fluid of mature human follicles.CrossRef | 1:CAS:528:DC%2BD38Xjs12qsLk%3D&md5=e8f73d97d1f20f518378b814b57984feCAS | open url image1

Balasubramanian, K., Lavoie, H. A., Garmey, J. C., Stocco, D. M., and Veldhuis, J. D. (1997). Regulation of porcine granulosa cell steroidogenic acute regulatory protein (StAR) by insulin-like growth factor I: synergism with follicle-stimulating hormone or protein kinase A agonist. Endocrinology 138, 433–439.
| 1:CAS:528:DyaK2sXjslWk&md5=25d82219bfd3068ebf42fe9313c50a08CAS | open url image1

Beale, E. G., Harvey, B. J., and Forest, C. (2007). PCK1 and PCK2 as candidate diabetes and obesity genes. Cell Biochem. Biophys. 48, 89–95.
PCK1 and PCK2 as candidate diabetes and obesity genes.CrossRef | 1:CAS:528:DC%2BD2sXosV2gtro%3D&md5=2ffff69d3028d9b00ef7591568c498c7CAS | open url image1

Blondin, P., Bousquet, D., Twagiramungu, H., Barnes, F., and Sirard, M.-A. (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38–43.
Manipulation of follicular development to produce developmentally competent bovine oocytes.CrossRef | 1:CAS:528:DC%2BD38Xht1ylsA%3D%3D&md5=4c7a1417ade1ec0d4805f7ca5479b1f5CAS | open url image1

Bragulla, H. H., and Homberger, D. G. (2009). Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J. Anat. 214, 516–559.
Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia.CrossRef | 1:CAS:528:DC%2BD1MXlvVajt7c%3D&md5=4a7db09f3920c1b1d15ec198e68b4df2CAS | open url image1

Brown, J. A., Eberhardt, D. M., Schrick, F. N., Roberts, M. P., and Godkin, J. D. (2003). Expression of retinol-binding protein and cellular retinol-binding protein in the bovine ovary. Mol. Reprod. Dev. 64, 261–269.
Expression of retinol-binding protein and cellular retinol-binding protein in the bovine ovary.CrossRef | 1:CAS:528:DC%2BD3sXos1Whsg%3D%3D&md5=1190b444aa1fe0fa8856baaa37866faeCAS | open url image1

Bunel, A., Nivet, A. L., Blondin, P., Vigneault, C., Richard, F. J., and Sirard, M. A. (2014). Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes. Reprod. Fertil. Dev. 26, 855–865.
Cumulus cell gene expression associated with pre-ovulatory acquisition of developmental competence in bovine oocytes.CrossRef | 1:CAS:528:DC%2BC2cXhtFynsbjO&md5=de66edf7a1151c1e074160717a81668dCAS | open url image1

Bunel, A., Jorssen, E. P., Merckx, E., Leroy, J. L., Bols, P. E., and Sirard, M. A. (2015). Individual bovine in vitro embryo production and cumulus cell transcriptomic analysis to distinguish cumulus–oocyte complexes with high or low developmental potential. Theriogenology 83, 228–237.
Individual bovine in vitro embryo production and cumulus cell transcriptomic analysis to distinguish cumulus–oocyte complexes with high or low developmental potential.CrossRef | 1:CAS:528:DC%2BC2cXhs1ymu7bE&md5=3bd94955456a48170e2dcef74f54a41fCAS | open url image1

Campbell, B. K., Onions, V., Kendall, N. R., Guo, L., and Scaramuzzi, R. J. (2010). The effect of monosaccharide sugars and pyruvate on the differentiation and metabolism of sheep granulosa cells in vitro. Reproduction 140, 541–550.
The effect of monosaccharide sugars and pyruvate on the differentiation and metabolism of sheep granulosa cells in vitro.CrossRef | 1:CAS:528:DC%2BC3cXhtlCqurrI&md5=9cebd755adc8ed8afcc6f8ff6367a5f1CAS | open url image1

Cheng, Y., Kim, J., Li, X. X., and Hsueh, A. J. (2015). Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators. PLoS One 10, e0117769.
Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators.CrossRef | open url image1

Chronowska, E. (2014). High-throughput analysis of ovarian granulosa cell transcriptome. BioMed Res. Int. 2014, 213570.
High-throughput analysis of ovarian granulosa cell transcriptome.CrossRef | open url image1

Devoto, L., Christenson, L. K., McAllister, J. M., Makrigiannakis, A., and Strauss, J. F. (1999). Insulin and insulin-like growth factor-I and -II modulate human granulosa-lutein cell steroidogenesis: enhancement of steroidogenic acute regulatory protein (StAR) expression. Mol. Hum. Reprod. 5, 1003–1010.
Insulin and insulin-like growth factor-I and -II modulate human granulosa-lutein cell steroidogenesis: enhancement of steroidogenic acute regulatory protein (StAR) expression.CrossRef | 1:CAS:528:DyaK1MXnvVKhs7Y%3D&md5=d55cf8532bac38acd7afd687d303ea3dCAS | open url image1

Dong, X.-Y., and Tang, S.-Q. (2010). Insulin-induced gene: a new regulator in lipid metabolism. Peptides 31, 2145–2150.
Insulin-induced gene: a new regulator in lipid metabolism.CrossRef | 1:CAS:528:DC%2BC3cXht1OmtLnE&md5=3ab8802e9e814de191252ed6886dfd3fCAS | open url image1

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 | open url image1

El-Hayek, S., and Clarke, H. J. (2016). Control of oocyte growth and development by intercellular communication within the follicular niche. Results Probl. Cell Differ. 58, 191–224.
Control of oocyte growth and development by intercellular communication within the follicular niche.CrossRef | open url image1

Gervais, M., Dugourd, C., Muller, L., Ardidie, C., Canton, B., Loviconi, L., Corvol, P., Chneiweiss, H., and Monnot, C. (2006). Akt down-regulates ERK1/2 nuclear localization and angiotensin II-induced cell proliferation through PEA-15. Mol. Biol. Cell 17, 3940–3951.
Akt down-regulates ERK1/2 nuclear localization and angiotensin II-induced cell proliferation through PEA-15.CrossRef | 1:CAS:528:DC%2BD28Xpt1alu7g%3D&md5=6c50ef849dfb8716eccbe28a612eacf3CAS | open url image1

Ginther, O. J., Knopf, L., and Kastelic, J. P. (1989). Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves. J. Reprod. Fertil. 87, 223–230.
Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves.CrossRef | 1:STN:280:DyaK3c7ls1WrsQ%3D%3D&md5=99941af00e28e0f1c240883091a3dfc7CAS | open url image1

Ginther, O. J., Kot, K., Kulick, L. J., and Wiltbank, M. C. (1997). Emergence and deviation of follicles during the development of follicular waves in cattle. Theriogenology 48, 75–87.
Emergence and deviation of follicles during the development of follicular waves in cattle.CrossRef | 1:STN:280:DC%2BD28zgtVylsg%3D%3D&md5=f54e5968b20cfe351e536e207637568dCAS | open url image1

Girard, A., Dufort, I., Douville, G., and Sirard, M.-A. (2015a). Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle. Reprod. Biol. Endocrinol. 13, 17.
Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle.CrossRef | open url image1

Girard, A., Dufort, I., and Sirard, M.-A. (2015b). The effect of energy balance on the transcriptome of bovine granulosa cells at 60 days postpartum. Theriogenology 84, 1350–1361.e6.
The effect of energy balance on the transcriptome of bovine granulosa cells at 60 days postpartum.CrossRef | 1:CAS:528:DC%2BC2MXht1ygtLrE&md5=ef62a8797a7cae8a62d25cad5646b9b9CAS | open url image1

Goto, M., Iwase, A., Harata, T., Takigawa, S., Suzuki, K., Manabe, S., and Kikkawa, F. (2009). IGF1-induced AKT phosphorylation and cell proliferation are suppressed with the increase in PTEN during luteinization in human granulosa cells. Reproduction 137, 835–842.
IGF1-induced AKT phosphorylation and cell proliferation are suppressed with the increase in PTEN during luteinization in human granulosa cells.CrossRef | 1:CAS:528:DC%2BD1MXovVKgtbg%3D&md5=92d4bbe8040cc421a2613d5e6551ed65CAS | open url image1

Hatzirodos, N., Hummitzsch, K., Irving-Rodgers, H. F., Harland, M. L., Morris, S. E., and Rodgers, R. J. (2014). Transcriptome profiling of granulosa cells from bovine ovarian follicles during atresia. BMC Genomics 15, 40.
Transcriptome profiling of granulosa cells from bovine ovarian follicles during atresia.CrossRef | open url image1

Hu, C.-L., Cowan, R. G., Harman, R. M., and Quirk, S. M. (2004). Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells. Mol. Endocrinol. 18, 326–338.
Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells.CrossRef | 1:CAS:528:DC%2BD2cXhtVChsro%3D&md5=6ebacc973407bd4f9718c38b5c4cb92dCAS | open url image1

Inoki, K., Li, Y., Zhu, T., Wu, J., and Guan, K.-L. (2002). TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4, 648–657.
TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling.CrossRef | 1:CAS:528:DC%2BD38Xms1ahtL4%3D&md5=da35e7cd2fe27f4697a7c90a2257e4b7CAS | open url image1

Ireland, J. J., and Roche, J. F. (1987). Hypothesis regarding development of dominant follicles during a bovine estrous cycle. In ‘Follicular Growth and Ovulation Rate in Farm Animals’. (Eds J. F. Roche and D. O’Callaghan.) pp. 1–18. (Martinus Nijhoff Publishers: The Hague.)

Krämer, A., Green, J., Pollard, J., and Tugendreich, S. (2014). Causal analysis approaches in ingenuity pathway analysis. Bioinformatics 30, 523–530.
Causal analysis approaches in ingenuity pathway analysis.CrossRef | open url image1

Krapivner, S., Popov, S., Chernogubova, E., Hellénius, M.-L., Fisher, R. M., Hamsten, A., and van’t Hooft, F. M. (2008). Insulin-induced gene 2 involvement in human adipocyte metabolism and body weight regulation. J. Clin. Endocrinol. Metab. 93, 1995–2001.
Insulin-induced gene 2 involvement in human adipocyte metabolism and body weight regulation.CrossRef | 1:CAS:528:DC%2BD1cXlvFWgt7s%3D&md5=b0db36412f59edd977b0da0976857506CAS | open url image1

Kwintkiewicz, J., and Giudice, L. C. (2009). The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function. Semin. Reprod. Med. 27, 43–51.
The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function.CrossRef | 1:CAS:528:DC%2BD1MXhvVGntro%3D&md5=d8f7f349c2cbaf98f2d0572f5344f13fCAS | open url image1

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 | 1:CAS:528:DC%2BC28XnslGmur0%3D&md5=d896361de08a68685a8ab351ebf46d4eCAS | open url image1

Laplante, M., and Sabatini, D. M. (2009). mTOR signaling at a glance. J. Cell Sci. 122, 3589–3594.
mTOR signaling at a glance.CrossRef | 1:CAS:528:DC%2BD1MXhsVKitrvP&md5=c63244fb3d082b5a7ba20031c8dec851CAS | open url image1

LaVoie, H. A., Garmey, J. C., Day, R. N., and Veldhuis, J. D. (1999). Concerted regulation of low density lipoprotein receptor gene expression by follicle-stimulating hormone and insulin-like growth factor I in porcine granulosa cells: promoter activation, messenger ribonucleic acid stability, and sterol feedback. Endocrinology 140, 178–186.
| 1:CAS:528:DyaK1MXhtFWmsA%3D%3D&md5=a7511f3ace9d34fdedca2a6da22a3799CAS | open url image1

Liu, Z., Rudd, M. D., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., Fan, H.-Y., Zeleznik, A. J., and Richards, J. S. (2009). FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells. Mol. Endocrinol. 23, 649–661.
FSH and FOXO1 regulate genes in the sterol/steroid and lipid biosynthetic pathways in granulosa cells.CrossRef | 1:CAS:528:DC%2BD1MXlsFCgtrw%3D&md5=f874e9a12fc1d00e8311b50e574a1294CAS | open url image1

Liwak, U., Faye, M. D., and Holcik, M. (2012). Translation control in apoptosis. Exp. Oncol. 34, 218–230.
| 1:CAS:528:DC%2BC38XhvFSiu7vO&md5=4d64ee080f4c21c09080863a1643cd6cCAS | open url image1

Lonergan, P., Fair, T., Forde, N., and Rizos, D. (2016). Embryo development in dairy cattle. Theriogenology 86, 270–277.
Embryo development in dairy cattle.CrossRef | 1:CAS:528:DC%2BC28XnsVWgurk%3D&md5=b732c23e97de8ba6081f85864cf2855eCAS | open url image1

Mack, E. M., Smith, J. E., Kurz, S. G., and Wood, J. R. (2012). cAMP-dependent regulation of ovulatory response genes is amplified by IGF1 due to synergistic effects on Akt phosphorylation and NF-κB transcription factors. Reproduction 144, 595–602.
cAMP-dependent regulation of ovulatory response genes is amplified by IGF1 due to synergistic effects on Akt phosphorylation and NF-κB transcription factors.CrossRef | 1:CAS:528:DC%2BC38XhslClt7rP&md5=b5fdb6630ff59ac5041f5082a70856abCAS | open url image1

Makker, A., Goel, M. M., and Mahdi, A. A. (2014). PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: an update. J. Mol. Endocrinol. 53, R103–R118.
PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: an update.CrossRef | 1:CAS:528:DC%2BC2MXmtFKjuw%3D%3D&md5=f26c5ccaaee1e8f40eaa21c427f1c4e8CAS | open url image1

Mani, A. M., Fenwick, M. A., Cheng, Z., Sharma, M. K., Singh, D., and Wathes, D. C. (2010). IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells. Reproduction 139, 139–151.
IGF1 induces up-regulation of steroidogenic and apoptotic regulatory genes via activation of phosphatidylinositol-dependent kinase/AKT in bovine granulosa cells.CrossRef | 1:CAS:528:DC%2BC3cXovVWmtw%3D%3D&md5=82b49c25aeaff4006b56919008d22d83CAS | open url image1

Martinez, L. O., Najib, S., Perret, B., Cabou, C., and Lichtenstein, L. (2015). Ecto-F1-ATPase/P2Y pathways in metabolic and vascular functions of high density lipoproteins. Atherosclerosis 238, 89–100.
Ecto-F1-ATPase/P2Y pathways in metabolic and vascular functions of high density lipoproteins.CrossRef | 1:CAS:528:DC%2BC2cXitValtLnE&md5=371ddd86af5b3e5ceb91bc5b5276e529CAS | open url image1

Moore, R. K., Otsuka, F., and Shimasaki, S. (2001). Role of ERK1/2 in the differential synthesis of progesterone and estradiol by granulosa cells. Biochem. Biophys. Res. Commun. 289, 796–800.
Role of ERK1/2 in the differential synthesis of progesterone and estradiol by granulosa cells.CrossRef | 1:CAS:528:DC%2BD3MXovVWitbo%3D&md5=0b11e6178260bd223ece6776a282d64bCAS | open url image1

Niewiarowska, J., Brézillon, S., Sacewicz-Hofman, I., Bednarek, R., Maquart, F.-X., Malinowski, M., Wiktorska, M., Wegrowski, Y., and Cierniewski, C. S. (2011). Lumican inhibits angiogenesis by interfering with α2β1 receptor activity and downregulating MMP-14 expression. Thromb. Res. 128, 452–457.
Lumican inhibits angiogenesis by interfering with α2β1 receptor activity and downregulating MMP-14 expression.CrossRef | 1:CAS:528:DC%2BC3MXhtl2ntrjP&md5=aff014471409931d9e5ca1672a9a0962CAS | open url image1

Nikitovic, D., Katonis, P., Tsatsakis, A., Karamanos, N. K., and Tzanakakis, G. N. (2008). Lumican, a small leucine-rich proteoglycan. IUBMB Life 60, 818–823.
Lumican, a small leucine-rich proteoglycan.CrossRef | 1:CAS:528:DC%2BD1cXhsFSnsbnP&md5=ed47b65e7c4453c9a86828143e590f99CAS | open url image1

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 | 1:CAS:528:DC%2BC38Xjs1Kkt70%3D&md5=c7b073398c07d51b7864bd8064c29b87CAS | open url image1

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 | 1:CAS:528:DC%2BC3sXhtVWmsbnJ&md5=a625f4d7250765ef69d7e5ee473994e5CAS | open url image1

Nivet, A. L., Léveillé, M. C., Leader, A., and Sirard, M. A. (2016). Transcriptional characteristics of different sized follicles in relation to embryo transferability: potential role of hepatocyte growth factor signalling. Mol. Hum. Reprod. 22, 475–484.
Transcriptional characteristics of different sized follicles in relation to embryo transferability: potential role of hepatocyte growth factor signalling.CrossRef | 1:STN:280:DC%2BC28bksVWntA%3D%3D&md5=91c5f12c0b02f23552408b088a529825CAS | open url image1

Potter, C. J., Pedraza, L. G., and Xu, T. (2002). Akt regulates growth by directly phosphorylating Tsc2. Nat. Cell Biol. 4, 658–665.
Akt regulates growth by directly phosphorylating Tsc2.CrossRef | 1:CAS:528:DC%2BD38Xms1ahtLw%3D&md5=b08ff59f0b2d485a8d1530bf2dd88735CAS | open url image1

Puttabyatappa, M., Jacot, T. A., Al-Alem, L. F., Rosewell, K. L., Duffy, D. M., Brännström, M., and Curry, T. E. (2014). Ovarian membrane-type matrix metalloproteinases: induction of MMP14 and MMP16 during the periovulatory period in the rat, macaque, and human. Biol. Reprod. 91, 34.
Ovarian membrane-type matrix metalloproteinases: induction of MMP14 and MMP16 during the periovulatory period in the rat, macaque, and human.CrossRef | open url image1

Ramos, J. W., Hughes, P. E., Renshaw, M. W., Schwartz, M. A., Formstecher, E., Chneiweiss, H., and Ginsberg, M. H. (2000). Death effector domain protein PEA-15 potentiates Ras activation of extracellular signal receptor-activated kinase by an adhesion-independent mechanism. Mol. Biol. Cell 11, 2863–2872.
Death effector domain protein PEA-15 potentiates Ras activation of extracellular signal receptor-activated kinase by an adhesion-independent mechanism.CrossRef | 1:CAS:528:DC%2BD3cXmvFSiur0%3D&md5=0d9e2c3d4d8c2f86440dba14fc9e1384CAS | open url image1

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 | 1:CAS:528:DC%2BC3MXhtFGns7vK&md5=d72db057b1d58d5b0976820b6cf2acceCAS | open url image1

Ross, S. A., McCaffery, P. J., Drager, U. C., and De Luca, L. M. (2000). Retinoids in embryonal development. Physiol. Rev. 80, 1021–1054.
| 1:CAS:528:DC%2BD3cXlsFWjsLY%3D&md5=d31bef13312ad722b1c893bc62ae75bfCAS | open url image1

Sakamoto, K., Aragaki, T., Morita, K., Kawachi, H., Kayamori, K., Nakanishi, S., Omura, K., Miki, Y., Okada, N., Katsube, K.-I., Takizawa, T., and Yamaguchi, A. (2011). Down-regulation of keratin 4 and keratin 13 expression in oral squamous cell carcinoma and epithelial dysplasia: a clue for histopathogenesis. Histopathology 58, 531–542.
Down-regulation of keratin 4 and keratin 13 expression in oral squamous cell carcinoma and epithelial dysplasia: a clue for histopathogenesis.CrossRef | open url image1

Schweigert, F. J., and Zucker, H. (1988). Concentrations of vitamin A, beta-carotene and vitamin E in individual bovine follicles of different quality. J. Reprod. Fertil. 82, 575–579.
Concentrations of vitamin A, beta-carotene and vitamin E in individual bovine follicles of different quality.CrossRef | 1:CAS:528:DyaL1cXit1Slur4%3D&md5=de349af90665abed4d78f47bd9df9b77CAS | open url image1

Schweigert, F. J., Gericke, B., Wolfram, W., Kaisers, U., and Dudenhausen, J. W. (2006). Peptide and protein profiles in serum and follicular fluid of women undergoing IVF. Hum. Reprod. 21, 2960–2968.
Peptide and protein profiles in serum and follicular fluid of women undergoing IVF.CrossRef | 1:CAS:528:DC%2BD28XhtVynsrzI&md5=e0ffc52782d3bea6e24c7b27008d9072CAS | open url image1

Shen, W.-J., Azhar, S., and Kraemer, F. B. (2016). Lipid droplets and steroidogenic cells. Exp. Cell Res. 340, 209–214.
Lipid droplets and steroidogenic cells.CrossRef | 1:CAS:528:DC%2BC2MXhvFeqsr7O&md5=7eb9c25e29f21cf1b7d3fd25895684b4CAS | open url image1

Sirard, M. A., Picard, L., Dery, M., Coenen, K., and Blondin, P. (1999). The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes. Theriogenology 51, 699–708.
The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes.CrossRef | 1:CAS:528:DyaK1MXjsFegtbs%3D&md5=6fc953b1e1510f2712e052cd68cd3a76CAS | open url image1

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 | open url image1

Stasiak, M., Boncela, J., Perreau, C., Karamanou, K., Chatron-Colliet, A., Proult, I., Przygodzka, P., Chakravarti, S., Maquart, F.-X., Kowalska, M. A., Wegrowski, Y., and Brézillon, S. (2016). Lumican inhibits SNAIL-induced melanoma cell migration specifically by blocking MMP-14 activity. PLoS One 11, e0150226.
Lumican inhibits SNAIL-induced melanoma cell migration specifically by blocking MMP-14 activity.CrossRef | open url image1

Törmä, H. (2011). Regulation of keratin expression by retinoids. Dermatoendocrinol 3, 136–140.
Regulation of keratin expression by retinoids.CrossRef | open url image1

Trencia, A., Perfetti, A., Cassese, A., Vigliotta, G., Miele, C., Oriente, F., Santopietro, S., Giacco, F., Condorelli, G., Formisano, P., and Beguinot, F. (2003). Protein kinase B/Akt binds and phosphorylates PED/PEA-15, stabilizing its antiapoptotic action. Mol. Cell. Biol. 23, 4511–4521.
Protein kinase B/Akt binds and phosphorylates PED/PEA-15, stabilizing its antiapoptotic action.CrossRef | 1:CAS:528:DC%2BD3sXltVSit74%3D&md5=147244d2346815811cb6b916e3e3447aCAS | open url image1

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 Biol. 3, RESEARCH0034.1.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.CrossRef | open url image1

Veldhuis, J. D., Garmey, J., and Juchter, D. (1988). Follicle-stimulating hormone regulates low density lipoprotein metabolism by swine granulosa cells. Endocrinology 123, 1660–1667.
Follicle-stimulating hormone regulates low density lipoprotein metabolism by swine granulosa cells.CrossRef | 1:CAS:528:DyaL1cXls1ersrw%3D&md5=35e798c26a198e0ed3f2694b2487eccfCAS | open url image1

Vieira, A. V., and Schneider, W. J. (1993). Transport and uptake of retinol during chicken oocyte growth. Biochim. Biophys. Acta 1169, 250–256.
Transport and uptake of retinol during chicken oocyte growth.CrossRef | 1:CAS:528:DyaK3sXlslOrt70%3D&md5=de3781cb559f5f3c89a62f4ca07a67d1CAS | open url image1

Williams, K. E., Fulford, L. A., and Albig, A. R. (2011). Lumican reduces tumor growth via induction of fas-mediated endothelial cell apoptosis. Cancer Microenviron. 4, 115–126.
Lumican reduces tumor growth via induction of fas-mediated endothelial cell apoptosis.CrossRef | 1:CAS:528:DC%2BC38Xit1aqt7c%3D&md5=2ff3d38f32f3cbdcb8fdc59a60736a38CAS | open url image1

Yu, F.-Q., Han, C.-S., Yang, W., Jin, X., Hu, Z.-Y., and Liu, Y.-X. (2005). Role of ERK1/2 in FSH induced PCNA expression and steroidogenesis in granulosa cells. Front. Biosci. 10, 896–904.
Role of ERK1/2 in FSH induced PCNA expression and steroidogenesis in granulosa cells.CrossRef | 1:CAS:528:DC%2BD2MXis1Snur0%3D&md5=d4a718125766801a1ae7dacae7afbdb8CAS | open url image1

Zimin, A. V., Delcher, A. L., Florea, L., Kelley, D. R., Schatz, M. C., Puiu, D., Hanrahan, F., Pertea, G., Van Tassell, C. P., Sonstegard, T. S., Marçais, G., Roberts, M., Subramanian, P., Yorke, J. A., and Salzberg, S. L. (2009). A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 10, R42.
A whole-genome assembly of the domestic cow, Bos taurus.CrossRef | open url image1



Supplementary MaterialSupplementary Material (77 KB) Export Citation

View Altmetrics