Microarray analysis of mRNA from cumulus cells following in vivo or in vitro maturation of mouse cumulus–oocyte complexes
Karen L. Kind A B , Kelly M. Banwell A , Kathryn M. Gebhardt A , Anne Macpherson A , Ashley Gauld A , Darryl L. Russell A and Jeremy G. Thompson A C
+ Author Affiliations
- Author Affiliations
A Research Centre for Reproductive Health, The Robinson Institute, School of Paediatrics and Reproductive Health, The University of Adelaide, Adelaide, SA 5005, Australia.
B School of Animal and Veterinary Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
C Corresponding author. Email: jeremy.thompson@adelaide.edu.au
Reproduction, Fertility and Development 25(2) 426-438 https://doi.org/10.1071/RD11305
Submitted: 6 September 2011 Accepted: 3 April 2012 Published: 15 May 2012
Abstract
The IVM of mammalian cumulus–oocyte complexes (COCs) yields reduced oocyte developmental competence compared with oocytes matured in vivo. Altered cumulus cell function during IVM is implicated as one cause for this difference. We have conducted a microarray analysis of cumulus cell mRNA following IVM or in vivo maturation (IVV). Mouse COCs were sourced from ovaries of 21-day-old CBAB6F1 mice 46 h after equine chorionic gonadotrophin (5 IU, i.p.) or from oviducts following treatment with 5 IU eCG (61 h) and 5 IU human chorionic gonadotrophin (13 h). IVM was performed in α-Minimal Essential Medium with 50 mIU FSH for 17 h. Three independent RNA samples were assessed using the Affymetrix Gene Chip Mouse Genome 430 2.0 array (Affymetrix, Santa Clara, CA, USA). In total, 1593 genes were differentially expressed, with 811 genes upregulated and 782 genes downregulated in IVM compared with IVV cumulus cells; selected genes were validated by real-time reverse transcription–polymerase chain reaction (RT-PCR). Surprisingly, haemoglobin α (Hba-a1) was highly expressed in IVV relative to IVM cumulus cells, which was verified by both RT-PCR and western blot analysis. Because haemoglobin regulates O2 and/or nitric oxide availability, we postulate that it may contribute to regulation of these gases during the ovulatory period in vivo. These data will provide a useful resource to determine differences in cumulus cell function that are possibly linked to oocyte competence.
Additional keywords: Affymetrix, gene expression, haemoglobin.
References
Albertini, D. F., Combelles, C. M., Benecchi, E., and Carabatsos, M. J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–653.| Cellular basis for paracrine regulation of ovarian follicle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVaisbY%3D&md5=6588619d433d88d23008f4966f22d18cCAS | 11427152PubMed |
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=775857df084a210ac27b7fc3608019c8CAS | 20870682PubMed |
Assou, S., Haouzi, D., Mahmoud, K., Aouacheria, A., Guillemin, Y., Pantesco, V., Reme, T., Dechaud, H., De Vos, J., and Hamamah, S. (2008). A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol. Hum. Reprod. 14, 711–719.
| A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gtw%3D%3D&md5=d8d791860dc98b74cfa88dcad1f1d307CAS | 19028806PubMed |
Banwell, K. M., Lane, M., Russell, D. L., Kind, K. L., and Thompson, J. G. (2007). Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum. Reprod. 22, 2768–2775.
| Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2srlsFKhsA%3D%3D&md5=2ec88ac460411e44d90cabbb0bd390a9CAS | 17725990PubMed |
Barrett, S. L., and Albertini, D. F. (2010). Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J. Assist. Reprod. Genet. 27, 29–39.
| Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence.Crossref | GoogleScholarGoogle Scholar | 20039198PubMed |
Beattie, J., Allan, G. J., Lochrie, J. D., and Flint, D. J. (2006). Insulin-like growth factor-binding protein-5 (IGFBP-5): a critical member of the IGF axis. Biochem. J. 395, 1–19.
| Insulin-like growth factor-binding protein-5 (IGFBP-5): a critical member of the IGF axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitlSgu78%3D&md5=e70f1b028829ad8671444052458a5319CAS | 16526944PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1ylsA%3D%3D&md5=64d62e92116101b74458d5ba5881991aCAS | 11751261PubMed |
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=a7b3d941b2d4571e1bf03cdd05e3fd69CAS | 942051PubMed |
Bu, S., Xia, G., Tao, Y., Lei, L., and Zhou, B. (2003). Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol. Cell. Endocrinol. 207, 21–30.
| Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVyns7s%3D&md5=da2aa357fde0c40c78755e4c110a9339CAS | 12972180PubMed |
Cetica, P., Pintos, L., Dalvit, G., and Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 124, 675–681.
| Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1KksA%3D%3D&md5=6b95b807c0908810b258257554508a83CAS | 12417006PubMed |
Cillo, F., Brevini, T. A., Antonini, S., Paffoni, A., Ragni, G., and Gandolfi, F. (2007). Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 134, 645–650.
| Association between human oocyte developmental competence and expression levels of some cumulus genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCisw%3D%3D&md5=d7589aadbc95b2feb2c3877cc4d80e6dCAS | 17965254PubMed |
Combelles, C. M., Cekleniak, N. A., Racowsky, C., and Albertini, D. F. (2002). Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum. Reprod. 17, 1006–1016.
| Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387pt1eisw%3D%3D&md5=278db51fdc8826d6d7b58082ac3ab6e7CAS | 11925398PubMed |
Crosier, A. E., Farin, P. W., Dykstra, M. J., Alexander, J. E., and Farin, C. E. (2001). Ultrastructural morphometry of bovine blastocysts produced in vivo or in vitro. Biol. Reprod. 64, 1375–1385.
| Ultrastructural morphometry of bovine blastocysts produced in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqsrw%3D&md5=3f0a1e95597d3649a115b81acb0d7121CAS | 11319141PubMed |
Curnow, E. C., Ryan, J., Saunders, D., and Hayes, E. S. (2008). Bovine in vitro oocyte maturation as a model for manipulation of the gamma-glutamyl cycle and intraoocyte glutathione. Reprod. Fertil. Dev. 20, 579–588.
| Bovine in vitro oocyte maturation as a model for manipulation of the gamma-glutamyl cycle and intraoocyte glutathione.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFansr0%3D&md5=f1d1ed8b6e3a5dfb546c2e50fc195189CAS | 18577355PubMed |
Dassen, H., Kamps, R., Punyadeera, C., Dijcks, F., de Goeij, A., Ederveen, A., Dunselman, G., and Groothuis, P. (2008). Haemoglobin expression in human endometrium. Hum. Reprod. 23, 635–641.
| Haemoglobin expression in human endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVOhsb4%3D&md5=466a793936ba1dc2930598bbb1be2997CAS | 18216035PubMed |
Diaz, F. J., Wigglesworth, K., and Eppig, J. J. (2007). Oocytes determine cumulus cell lineage in mouse ovarian follicles. J. Cell Sci. 120, 1330–1340.
| Oocytes determine cumulus cell lineage in mouse ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFSjtLw%3D&md5=b37f926df59e6d0908cd5ab73b352b82CAS | 17389684PubMed |
Downs, S. M., Humpherson, P. G., and Leese, H. J. (2002). Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol. Reprod. Dev. 62, 113–123.
| Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVChu7s%3D&md5=41879e42e7ca949d2c55dd0c1cced185CAS | 11933168PubMed |
Dunning, K. R., Lane, M., Brown, H. M., Yeo, C., Robker, R. L., and Russell, D. L. (2007). Altered composition of the cumulus–oocyte complex matrix during in vitro maturation of oocytes. Hum. Reprod. 22, 2842–2850.
| Altered composition of the cumulus–oocyte complex matrix during in vitro maturation of oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Shu7fO&md5=e7740f745297f7edced5d431ebad5d4dCAS | 17872911PubMed |
Dunning, K. R., Cashman, K., Russell, D. L., Thompson, J. G., Norman, R. J., and Robker, R. L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–918.
| Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFahurfN&md5=1f81538ef37347d8d384bad37e91dea3CAS | 20686180PubMed |
Durlinger, A. L., Kramer, P., Karels, B., de Jong, F. H., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (1999). Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 140, 5789–5796.
| Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12htLc%3D&md5=fad477025104e2fde0306bfd5645d6d9CAS | 10579345PubMed |
Durlinger, A. L., Gruijters, M. J., Kramer, P., Karels, B., Kumar, T. R., Matzuk, M. M., Rose, U. M., de Jong, F. H., Uilenbroek, J. T., Grootegoed, J. A., and Themmen, A. P. (2001). Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 142, 4891–4899.
| Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslGqu78%3D&md5=3f7d22d5857084c480c7fc8fc0469ab2CAS | 11606457PubMed |
Ebner, T., Yaman, C., Moser, M., Sommergruber, M., Feichtinger, O., and Tews, G. (2000). Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection. Hum. Reprod. 15, 427–430.
| Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7it1eqsQ%3D%3D&md5=fcabb5a824be2f8e7549b19f390b1bd9CAS | 10655316PubMed |
Eppig, J. J., and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod. 41, 268–276.
| Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FivVGhsA%3D%3D&md5=aff6b47849a8170f44680dc0ebb1d6c1CAS | 2508774PubMed |
Eppig, J. J., Wigglesworth, K., and Pendola, F. L. (2002). The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc. Natl Acad. Sci. USA 99, 2890–2894.
| The mammalian oocyte orchestrates the rate of ovarian follicular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Crtb0%3D&md5=d0aa779268da0c8b3c92336019dcacb4CAS | 11867735PubMed |
Eppig, J. J., Pendola, F. L., Wigglesworth, K., and Pendola, J. K. (2005). Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol. Reprod. 73, 351–357.
| Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yqsLk%3D&md5=a086f727922227317bb6d26480181b48CAS | 15843493PubMed |
Feuerstein, P., Cadoret, V., Dalbies-Tran, R., Guerif, F., Bidault, R., and Royere, D. (2007). Gene expression in human cumulus cells: one approach to oocyte competence. Hum. Reprod. 22, 3069–3077.
| Gene expression in human cumulus cells: one approach to oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKltLjP&md5=3721f4bf6cc94948dfb5c534124c8e41CAS | 17951581PubMed |
Fischer, B., Kunzel, W., Kleinstein, J., and Gips, H. (1992). Oxygen tension in follicular fluid falls with follicle maturation. Eur. J. Obstet. Gynecol. Reprod. Biol. 43, 39–43.
| Oxygen tension in follicular fluid falls with follicle maturation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387ks1Klsw%3D%3D&md5=f5cbc50dffe5102a40cf2b09ef8c4ef0CAS | 1737607PubMed |
Fortune, J. E., Rivera, G. M., and Yang, M. Y. (2004). Follicular development: the role of the follicular microenvironment in selection of the dominant follicle. Anim. Reprod. Sci. 82–83, 109–126.
| Follicular development: the role of the follicular microenvironment in selection of the dominant follicle.Crossref | GoogleScholarGoogle Scholar | 15271447PubMed |
Garlanda, C., Bottazzi, B., Bastone, A., and Mantovani, A. (2005). Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu. Rev. Immunol. 23, 337–366.
| Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFOjurw%3D&md5=a6640ae6c8f363b9597f2d6d5ef506fbCAS | 15771574PubMed |
Gebhardt, K.M., Feil, D.K., Dunning, K.R., Lane, M., and Russell, D.L. (2011). Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer. Fertil. Steril. 96, 47–52.e2.
| Human cumulus cell gene expression as a biomarker of pregnancy outcome after single embryo transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosFWgsbY%3D&md5=1d45f9539a74c68bf888acbd2f834cb9CAS | 21575950PubMed |
Gelman, J. S., Sironi, J., Castro, L. M., Ferro, E. S., and Fricker, L. D. (2010). Hemopressins and other hemoglobin-derived peptides in mouse brain: comparison between brain, blood, and heart peptidome and regulation in Cpefat/fat mice. J. Neurochem. 113, 871–880.
| Hemopressins and other hemoglobin-derived peptides in mouse brain: comparison between brain, blood, and heart peptidome and regulation in Cpefat/fat mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvFShs7Y%3D&md5=70ff439c27bfad13a50d4a65cda56737CAS | 20202081PubMed |
Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
| Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVKmurY%3D&md5=ea2826a49264b29c9302c4d90b63358cCAS | 18175787PubMed |
Grek, C. L., Newton, D. A., Spyropoulos, D. D., and Baatz, J. E. (2011). Hypoxia up-regulates expression of hemoglobin in alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 44, 439–447.
| Hypoxia up-regulates expression of hemoglobin in alveolar epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1Kjsrk%3D&md5=5ccd699be9eb510502af8e7ac9037628CAS | 20508070PubMed |
Hamel, M., Dufort, I., Robert, C., Gravel, C., Leveille, M. C., Leader, A., and Sirard, M. A. (2008). Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum. Reprod. 23, 1118–1127.
| Identification of differentially expressed markers in human follicular cells associated with competent oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1agsrc%3D&md5=1bbba0b5c6e9f3b53c3c053c92ef730eCAS | 18310048PubMed |
Hamel, M., Dufort, I., Robert, C., Leveille, M. C., Leader, A., and Sirard, M. A. (2010). Genomic assessment of follicular marker genes as pregnancy predictors for human IVF. Mol. Hum. Reprod. 16, 87–96.
| Genomic assessment of follicular marker genes as pregnancy predictors for human IVF.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlCisA%3D%3D&md5=35a0f0e71d02fe0992fff5da1ba2083eCAS | 19778949PubMed |
Harris, S. E., Gopichandran, N., Picton, H. M., Leese, H. J., and Orsi, N. M. (2005). Nutrient concentrations in murine follicular fluid and the female reproductive tract. Theriogenology 64, 992–1006.
| Nutrient concentrations in murine follicular fluid and the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVGjsbw%3D&md5=2308de1d60050d36de2a97c47e11b5caCAS | 16054501PubMed |
Harris, S. E., Adriaens, I., Leese, H. J., Gosden, R. G., and Picton, H. M. (2007). Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro. Reproduction 134, 415–424.
| Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKnur3O&md5=1392501645423d87a88589bf0484668cCAS | 17709560PubMed |
Hasegawa, J., Yanaihara, A., Iwasaki, S., Otsuka, Y., Negishi, M., Akahane, T., and Okai, T. (2005). Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality. Hum. Reprod. 20, 2194–2200.
| Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1Gnurw%3D&md5=dac78795d35a24fd33e496bb9c750a5eCAS | 15802315PubMed |
Hasegawa, J., Yanaihara, A., Iwasaki, S., Mitsukawa, K., Negishi, M., and Okai, T. (2007). Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI. J. Assist. Reprod. Genet. 24, 463–466.
| Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI.Crossref | GoogleScholarGoogle Scholar | 17846881PubMed |
Hernandez-Gonzalez, I., Gonzalez-Robayna, I., Shimada, M., Wayne, C. M., Ochsner, S. A., White, L., and Richards, J. S. (2006). Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process? Mol. Endocrinol. 20, 1300–1321.
| Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlSrsLY%3D&md5=702b67fb3bcd6b5809497f92596a22b1CAS | 16455817PubMed |
Higaki, S., Fujii, H., Nagano, M., Katagiri, S., and Takahashi, Y. (2010). Measurement of pO2 in cultured mouse oocytes using electron paramagnetic resonance oximetry. Biomed. Res. 31, 165–168.
| Measurement of pO2 in cultured mouse oocytes using electron paramagnetic resonance oximetry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtVWmtbo%3D&md5=abe4853cee1e95c61c447b287841fe5bCAS | 20460746PubMed |
Hussein, T. S., Froiland, D. A., Amato, F., Thompson, J. G., and Gilchrist, R. B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257–5268.
| Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWru7rK&md5=6914b264c48e5b19522b919f17ee06f4CAS | 16263764PubMed |
Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–521.
| Oocyte-secreted factors enhance oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2gsb4%3D&md5=0f9b6f0fe43b776d7f08409072e0f775CAS | 16854407PubMed |
Jones, G. M., Cram, D. S., Song, B., Magli, M. C., Gianaroli, L., Lacham-Kaplan, O., Findlay, J. K., Jenkin, G., and Trounson, A. O. (2008). Gene expression profiling of human oocytes following in vivo or in vitro maturation. Hum. Reprod. 23, 1138–1144.
| Gene expression profiling of human oocytes following in vivo or in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1agsrw%3D&md5=145ec18d7c9848e32d548c5f6833874fCAS | 18346995PubMed |
Jones, J. I., Gockerman, A., Busby, W. H., Camacho-Hubner, C., and Clemmons, D. R. (1993). Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I. J. Cell Biol. 121, 679–687.
| Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitVKjtro%3D&md5=c0743dc0500874a7a9daeade9715965eCAS | 7683690PubMed |
Krumenacker, J. S., Hanafy, K. A., and Murad, F. (2004). Regulation of nitric oxide and soluble guanylyl cyclase. Brain Res. Bull. 62, 505–515.
| Regulation of nitric oxide and soluble guanylyl cyclase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVOksr0%3D&md5=f400910f18f371a264def2a7eaef3744CAS | 15036565PubMed |
Leibfried-Rutledge, M. L., Critser, E. S., Eyestone, W. H., Northey, D. L., and First, N. L. (1987). Development potential of bovine oocytes matured in vitro or in vivo. Biol. Reprod. 36, 376–383.
| Development potential of bovine oocytes matured in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3hsVemsQ%3D%3D&md5=476775ffaf338598958b7dec88f44ca1CAS | 3580458PubMed |
Liu, Y. J., Xu, Y., and Yu, Q. (2006). Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro- and antimetastatic activity, respectively. Oncogene 25, 2452–2467.
| Full-length ADAMTS-1 and the ADAMTS-1 fragments display pro- and antimetastatic activity, respectively.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1ansr8%3D&md5=a9fad041df59d89b641c64be365b62feCAS | 16314835PubMed |
Liu, Z., de Matos, D. G., Fan, H. Y., Shimada, M., Palmer, S., and Richards, J. S. (2009). Interleukin-6: an autocrine regulator of the mouse cumulus cell–oocyte complex expansion process. Endocrinology 150, 3360–3368.
| Interleukin-6: an autocrine regulator of the mouse cumulus cell–oocyte complex expansion process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotlCrsbg%3D&md5=8ad023c6c35ddcc27f0f72d416809311CAS | 19299453PubMed |
Luque, A., Carpizo, D. R., and Iruela-Arispe, M. L. (2003). ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J. Biol. Chem. 278, 23 656–23 665.
| ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslygt7g%3D&md5=22b09cdb5af0e73d6718ce0826b3e279CAS |
Matzuk, M. M., Burns, K. H., Viveiros, M. M., and Eppig, J. J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–2180.
| Intercellular communication in the mammalian ovary: oocytes carry the conversation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFGhsbw%3D&md5=9d9649c54282d35c7e19823e070620adCAS | 12077402PubMed |
McKenzie, L. J., Pangas, S. A., Carson, S. A., Kovanci, E., Cisneros, P., Buster, J. E., Amato, P., and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–2874.
| Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crotVyisA%3D%3D&md5=4c220a7324f72551a6aa60a07142b155CAS | 15471935PubMed |
Nakamura, Y., Yamagata, Y., Sugino, N., Takayama, H., and Kato, H. (2002). Nitric oxide inhibits oocyte meiotic maturation. Biol. Reprod. 67, 1588–1592.
| Nitric oxide inhibits oocyte meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot1KjsLg%3D&md5=07bebaaf0298ec1ac5b635971bda6de4CAS | 12390892PubMed |
Nicholas, B., Alberio, R., Fouladi-Nashta, A. A., and Webb, R. (2005). Relationship between low-molecular-weight insulin-like growth factor-binding proteins, caspase-3 activity, and oocyte quality. Biol. Reprod. 72, 796–804.
| Relationship between low-molecular-weight insulin-like growth factor-binding proteins, caspase-3 activity, and oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis12hsrs%3D&md5=2fe548fbea3ca11d5b09084b1437deafCAS | 15564596PubMed |
Onoda, N., Li, D., Mickey, G., Erickson, G., and Shimasaki, S. (1995). Gonadotropin-releasing hormone overcomes follicle-stimulating hormone’s inhibition of insulin-like growth factor-5 synthesis and promotion of its degradation in rat granulosa cells. Mol. Cell. Endocrinol. 110, 17–25.
| Gonadotropin-releasing hormone overcomes follicle-stimulating hormone’s inhibition of insulin-like growth factor-5 synthesis and promotion of its degradation in rat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvVWju78%3D&md5=1e2c253a2b98113d98799b65ae3407cbCAS | 7545620PubMed |
Psarros, M., Heber, S., Sick, M., Thoppae, G., Harshman, K., and Sick, B. (2005). RACE: remote analysis computation for gene expression data. Nucleic Acids Res. 33, W638–W643.
| RACE: remote analysis computation for gene expression data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslyqur0%3D&md5=3e82e31b9a56f38050a1f674fadb7fe9CAS | 15980552PubMed |
Redding, G. P., Bronlund, J. E., and Hart, A. L. (2007). Mathematical modelling of oxygen transport-limited follicle growth. Reproduction 133, 1095–1106.
| Mathematical modelling of oxygen transport-limited follicle growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGnu7c%3D&md5=92aa013886794f97362647bfcc7aa53aCAS | 17636164PubMed |
Redding, G. P., Bronlund, J. E., and Hart, A. L. (2008). Theoretical investigation into the dissolved oxygen levels in follicular fluid of the developing human follicle using mathematical modelling. Reprod. Fertil. Dev. 20, 408–417.
| Theoretical investigation into the dissolved oxygen levels in follicular fluid of the developing human follicle using mathematical modelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVKksL0%3D&md5=0378d45fa191dfc6d955798fd6dff22fCAS | 18402761PubMed |
Richter, F., Meurers, B. H., Zhu, C., Medvedeva, V. P., and Chesselet, M. F. (2009). Neurons express hemoglobin alpha- and beta-chains in rat and human brains. J. Comp. Neurol. 515, 538–547.
| Neurons express hemoglobin alpha- and beta-chains in rat and human brains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1yjtLs%3D&md5=18b579ab5b5772bd3efb1077a949b76cCAS | 19479992PubMed |
Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
| Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=7e1cd9cffb7fc878404e93f2e0a29d94CAS | 11803560PubMed |
Russell, D. L., Doyle, K. M., Ochsner, S. A., Sandy, J. D., and Richards, J. S. (2003). Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J. Biol. Chem. 278, 42 330–42 339.
| Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1amu74%3D&md5=e5dbef77fd84ac9257e5af7de6670972CAS |
Salustri, A., Garlanda, C., Hirsch, E., De Acetis, M., Maccagno, A., Bottazzi, B., Doni, A., Bastone, A., Mantovani, G., Beck Peccoz, P., Salvatori, G., Mahoney, D. J., Day, A. J., Siracusa, G., Romani, L., and Mantovani, A. (2004). PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131, 1577–1586.
| PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKltbc%3D&md5=d242775fe0356e38e3d0fad2873bff22CAS | 14998931PubMed |
Sela-Abramovich, S., Galiani, D., Nevo, N., and Dekel, N. (2008). Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action. Biol. Reprod. 78, 1111–1118.
| Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVWktbk%3D&md5=7c6213fd4359114b80b7e4f4da4f5d81CAS | 18337515PubMed |
Shimada, M., Yanai, Y., Okazaki, T., Yamashita, Y., Sriraman, V., Wilson, M. C., and Richards, J. S. (2007). Synaptosomal-associated protein 25 gene expression is hormonally regulated during ovulation and is involved in cytokine/chemokine exocytosis from granulosa cells. Mol. Endocrinol. 21, 2487–2502.
| Synaptosomal-associated protein 25 gene expression is hormonally regulated during ovulation and is involved in cytokine/chemokine exocytosis from granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGhu7bF&md5=92601d43d6f8fc19a911b0f5efe4f9deCAS | 17595323PubMed |
Shimasaki, S., Zachow, R. J., Li, D., Kim, H., Iemura, S., Ueno, N., Sampath, K., Chang, R. J., and Erickson, G. F. (1999). A functional bone morphogenetic protein system in the ovary. Proc. Natl Acad. Sci. USA 96, 7282–7287.
| A functional bone morphogenetic protein system in the ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVOruro%3D&md5=e211efcf87ee2a55a17f0b53788f1ee6CAS | 10377406PubMed |
Smyth, G.K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiment. Stat. Appl. Genet. Mol. Biol. 3, 1–25.
| Linear models and empirical Bayes methods for assessing differential expression in microarray experiment.Crossref | GoogleScholarGoogle Scholar |
Suga, A., Hikasa, H., and Taira, M. (2006). Xenopus ADAMTS1 negatively modulates FGF signaling independent of its metalloprotease activity. Dev. Biol. 295, 26–39.
| Xenopus ADAMTS1 negatively modulates FGF signaling independent of its metalloprotease activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVarsLw%3D&md5=196b64030a2d2beb513748c458f9a4c3CAS | 16690049PubMed |
Sugiura, K., Pendola, F. L., and Eppig, J. J. (2005). Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev. Biol. 279, 20–30.
| Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlemtb4%3D&md5=6f20796c271967b6d76d4e935e4c9465CAS | 15708555PubMed |
Sutton, M. L., Gilchrist, R. B., and Thompson, J. G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 9, 35–48.
| Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVelt7Y%3D&md5=9ebd7426b7806b3a80f3af517260eaf0CAS | 12638780PubMed |
Tam, K. K., Russell, D. L., Peet, D. J., Bracken, C. P., Rodgers, R. J., Thompson, J. G., and Kind, K. L. (2010). Hormonally regulated follicle differentiation and luteinization in the mouse is associated with hypoxia inducible factor activity. Mol. Cell. Endocrinol. 327, 47–55.
| Hormonally regulated follicle differentiation and luteinization in the mouse is associated with hypoxia inducible factor activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFSrtrg%3D&md5=f70a6fb1323a43084dab1baa84943ea3CAS | 20600586PubMed |
Tesfaye, D., Ghanem, N., Carter, F., Fair, T., Sirard, M. A., Hoelker, M., Schellander, K., and Lonergan, P. (2009). Gene expression profile of cumulus cells derived from cumulus–oocyte complexes matured either in vivo or in vitro. Reprod. Fertil. Dev. 21, 451–461.
| Gene expression profile of cumulus cells derived from cumulus–oocyte complexes matured either in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemsb8%3D&md5=cd62386ecab7a413376f2817285aaaf6CAS | 19261222PubMed |
Thompson, J. G. (1997). Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants. Reprod. Fertil. Dev. 9, 341–354.
| Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svgsFaisA%3D%3D&md5=fee8c6153e7bf0690c279840365311e2CAS | 9261882PubMed |
Thompson, J. G., Lane, M., and Gilchrist, R. B. (2007). Metabolism of the bovine cumulus–oocyte complex and influence on subsequent developmental competence. Soc. Reprod. Fertil. Suppl. 64, 179–190.
| 1:CAS:528:DC%2BD1cXpvVyrs7o%3D&md5=42f8ff288e55903c54b9e5bb093af622CAS | 17491147PubMed |
Vaccari, S., Weeks, J. L., Hsieh, M., Menniti, F. S., and Conti, M. (2009). Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol. Reprod. 81, 595–604.
| Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu7zE&md5=c3de2d7480a98a5e5cef31df0e5b432bCAS | 19474061PubMed |
Van Blerkom, J., Antczak, M., and Schrader, R. (1997). The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 12, 1047–1055.
| The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szjsl2qsQ%3D%3D&md5=fb11df80eff8ed7bd07ee56df749bfe9CAS | 9194664PubMed |
van de Leemput, E. E., Vos, P. L., Zeinstra, E. C., Bevers, M. M., van der Weijden, G. C., and Dieleman, S. J. (1999). Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory LH surge. Theriogenology 52, 335–349.
| Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory LH surge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvVKms7k%3D&md5=dec38d0d8328ae403663f59fa8f74b65CAS | 10734399PubMed |
van Montfoort, A. P., Geraedts, J. P., Dumoulin, J. C., Stassen, A. P., Evers, J. L., and Ayoubi, T. A. (2008). Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis. Mol. Hum. Reprod. 14, 157–168.
| Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFSisrs%3D&md5=c7e08c69ecddcee1040ce1476ed0408bCAS | 18204071PubMed |
Vanderhyden, B. C., and Armstrong, D. T. (1989). Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol. Reprod. 40, 720–728.
| Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1Mzitlaltw%3D%3D&md5=3a4f6c373a2d9878fcea7d8658d09398CAS | 2752073PubMed |
Vanderhyden, B. C., Telfer, E. E., and Eppig, J. J. (1992). Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol. Reprod. 46, 1196–1204.
| Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2Fgtlyrsw%3D%3D&md5=67a554d9e01d7ab75c87e515d7e5df18CAS | 1391318PubMed |
Varani, S., Elvin, J. A., Yan, C., DeMayo, J., DeMayo, F. J., Horton, H. F., Byrne, M. C., and Matzuk, M. M. (2002). Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol. Endocrinol. 16, 1154–1167.
| Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWkt7c%3D&md5=53e199da83609465b0cb65aa0f424cdeCAS | 12040004PubMed |
Wathlet, S., Adriaenssens, T., Segers, I., Verheyen, G., Van de Velde, H., Coucke, W., Ron El, R., Devroey, P., and Smitz, J. (2011). Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients. Hum. Reprod. 26, 1035–1051.
| Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlehtrg%3D&md5=f8730e2233621268dcc30b0b53217ab5CAS | 21372047PubMed |
Wells, D., and Patrizio, P. (2008). Gene expression profiling of human oocytes at different maturational stages and after in vitro maturation. Am. J. Obstet. Gynecol. 198, 455e1–455e9.
| Gene expression profiling of human oocytes at different maturational stages and after in vitro maturation.Crossref | GoogleScholarGoogle Scholar |
Yung, Y., Maman, E., Konopnicki, S., Cohen, B., Brengauz, M., Lojkin, I., Dal Canto, M., Fadini, R., Dor, J., and Hourvitz, A. (2010). ADAMTS-1: a new human ovulatory gene and a cumulus marker for fertilization capacity. Mol. Cell. Endocrinol. 328, 104–108.
| ADAMTS-1: a new human ovulatory gene and a cumulus marker for fertilization capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFamsb3J&md5=697c2dddc665baa1480cf4032382fc3eCAS | 20655981PubMed |
Zhang, L., Jiang, S., Wozniak, P. J., Yang, X., and Godke, R. A. (1995). Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro. Mol. Reprod. Dev. 40, 338–344.
| Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkt1Khs7k%3D&md5=03893f1f39e072e90bace174f4161129CAS | 7772344PubMed |
Zhang, X., Jafari, N., Barnes, R. B., Confino, E., Milad, M., and Kazer, R. R. (2005). Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil. Steril. 83, 1169–1179.
| Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFaruro%3D&md5=cf4f6c17b40a44d8801fe2b3265ed5a9CAS | 15831290PubMed |
