FSH and LH receptors are differentially expressed in cumulus cells surrounding developmentally competent and incompetent mouse fully grown antral oocytes

Reproduction, Fertility and Development

Volumn 27, Issue 3, 2015, Pages 497-503

  Vigone, Giulia ^a   Merico, Valeria ^a   Redi, Carlo Alberto ^a,b   Mazzini, Giuliano ^c   Garagna, Silvia ^a   Zuccotti, Maurizio ^d  

^a UNIVERSITY OF PAVIA   (Italy)

^b FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

Author keywords

cumulus oocyte complex; gonadotropin receptors; oocyte quality

Indexed keywords

FOLLITROPIN RECEPTOR; LUTEINIZING HORMONE RECEPTOR; CHROMATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL MATURATION; CELL POPULATION; CHROMATIN; CONTROLLED STUDY; CUMULUS CELL; FEMALE; GENE EXPRESSION; GENE SEQUENCE; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; OOCYTE; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; GENETICS; METABOLISM; OOCYTE DEVELOPMENT;

ANIMALS; CHROMATIN; CUMULUS CELLS; FEMALE; GENE EXPRESSION; MICE; OOCYTES; OOGENESIS; RECEPTORS, FSH; RECEPTORS, LH;

EID: 84924762896     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD13251     Document Type: Article

References (43)

1. Adriaenssens, T., Segers, I., Wathlet, S., and Smitz, J. (2011). The cumulus cell gene expression profile of oocytes with different nuclear maturity and potential for blastocyst formation. J. Assist. Reprod. Genet. 28, 31-40. doi:10.1007/S10815-010-9481-9
2. Armenti, A. E., Zama, A. M., Passantino, L., and Uzumcu, M. (2008). Developmental methoxychlor exposure affects multiple reproductive parameters and ovarian folliculogenesis and gene expression in adult rats. Toxicol. Appl. Pharmacol. 233, 286-296. doi:10.1016/J.TAAP. 2008.09.010
3. Assidi, M., Dufort, I., Ali, A., Hamel, M., Algriany, O., Dielemann, S., and Sirard, M. A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with folliclestimulating hormone and/or phorbol myristate acetate in vitro. Biol. Reprod. 79, 209-222. doi:10.1095/BIOLREPROD.108.067686
4. Assou, S., Haouzi, D., Mahmoud, K., Aouacheria, A., Guillemin, Y., Pantesco, V., Rème, 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. doi:10.1093/MOLEHR/GAN067
5. Bellone, M., Zuccotti, M., Redi, C. A., and Garagna, S. (2009). The position of the germinal vesicle and the chromatin organization together provide a marker of the developmental competence of mouse antral oocytes. Reproduction 138, 639-643. doi:10.1530/REP-09-0230
6. Bettegowda, A., Patel, O. V., Lee, K. B., Park, K. E., Salem, M., Yao, J., Ireland, J. J., and Smith, G. W. (2008). Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol. Reprod. 79, 301-309. doi:10.1095/BIOLREPROD.107.067223
7. Bukovsky, A., Indrapichate, K., Fujiwara, H., Cekanova, M., Ayala, M. E., Dominguez, R., Caudle, M. R., Wimalsena, J., Elder, R. F., Copas, P., Foster, J. S., Fernando, R. I., Henley, D. C., and Upadhyaya, N. B. (2003). Multiple luteinizing hormone receptor (LHR) protein variants, interspecies reactivity of anti-LHR mAb clone 3B5, subcellular localization of LHR in human placenta, pelvic floor and brain, and possible role for LHR in the development of abnormal pregnancy, pelvic floor disorders and Alzheimer's disease. Reprod. Biol. Endocrinol. 1, 46. doi:10.1186/1477-7827-1-46
8. Calder, M. D., Caveney, A. N., Westhusin, M. E., and Watson, A. J. (2001). Cyclooxygenase-2 and prostaglandin E(2) (PGE(2)) receptor messenger RNAs are affected by bovine oocyte maturation time and cumulusoocyte complex quality, and PGE(2) induces moderate expansion of the bovine cumulus in vitro. Biol. Reprod. 65, 135-140. doi:10.1095/BIOLREPROD65.1.135
9. Calder, M. D., Caveney, A. N., Smith, L. C., and Watson, A. J. (2003). Responsiveness of bovine cumulus-oocyte-complexes (COC) to porcine and recombinant human FSH, and the effect of COC quality on gonadotropin receptor and Cx43 marker genemRNAsduring maturation in vitro. Reprod. Biol. Endocrinol. 1, 14. doi:10.1186/1477-7827-1-14
10. Choi, J. H., Kim, G. A., Park, J. H., Song, G. H., Park, J. W., Kim, D. Y., and Lim, J. M. (2011). Generation of viable embryos and embryonic stem cell-like cells from cultured primary follicles in mice. Biol. Reprod. 85, 744-754. doi:10.1095/BIOLREPROD.110.084137
11. 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. doi:10.1530/REP-07-0182
12. Cotterill, M., Catt, S. L., and Picton, H. M. (2012). Characterisation of the cellular and molecular responses of ovine oocytes and their supporting somatic cells to pre-ovulatory levels of LH and FSH during in vitro maturation. Reproduction 144, 195-207. doi:10.1530/REP-12-0031
13. Crozet, N. (1984). Effects of actinomycin D and cycloheximide on the nucleolar ultrastructure of porcine oocytes. Biol. Cell 48, 25-29. doi:10.1111/J.1768-322X.1984.TB00199.X
14. Debey, P., Szöllösi, M. S., Szöllösi, D., Vautier, D., Girousse, A., and Besombes, D. (1993). Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol. Reprod. Dev. 36, 59-74. doi:10.1002/MRD.1080360110
15. Fu, M., Chen, X., Yan, J., Lei, L., Jin, S., Yang, J., Song, X., Zhang, M., and Xia, G. (2007). Luteinizing hormone receptors expression in cumulus cells closely related to mouse oocyte meiotic maturation. Front. Biosci. 12, 1804-1813.
16. Fulton, B. P., and Whittingham, D. G. (1978). Activation of mammalian oocytes by intracellular injection of calcium. Nature 273, 149-151. doi:10.1038/273149A0
17. 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. doi:10.1016/J.FERTNSTERT.2011.04.033
18. Gilchrist, R. B. (2011). Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev. 23, 23-31. doi:10.1071/RD10225
19. Inoue, A., Nakajima, R., Nagata, M., and Aoki, F. (2008). Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum. Reprod. 23, 1377-1384. doi:10.1093/HUMREP/DEN096
20. Lefèvre, B., Gougeon, A., Nomé, F., and Testart, J. (1989). In vivo changes in oocyte germinal vesicle related to follicular quality and size at midfollicular phase during stimulated cycles in the cynomolgus monkey. Reprod. Nutr. Dev. 29, 523-532. doi:10.1051/RND:19890501
21. Li, X., Zhang, H., Sheng, X., Li, B., Zhou, J., Xu, M., Weng, Q., Watanabe, G., and Taya, K. (2012). Immunoreactivities of androgen receptor, estrogen receptors, p450arom, p450c17 proteins in wild ground squirrels ovaries during the nonbreeding and breeding seasons. J. Ovarian Res. 5, 26. doi:10.1186/1757-2215-5-26
22. Lodde, V., Modina, S., Galbusera, C., Franciosi, F., and Luciano, A. M. (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74, 740-749. doi:10.1002/MRD.20639
23. Logan, K. A., Juengel, J. L., and McNatty, K. P. (2002). Onset of steroidogenic enzyme gene expression during ovarian follicular development in sheep. Biol. Reprod. 66, 906-916. doi:10.1095/BIOLREPROD66.4.906
24. Maman, E., Yung, Y., Kedem, A., Yerushalmi, G. M., Konopnicki, S., Cohen, B., Dor, J., and Hourvitz, A. (2012). High expression of luteinizing hormone receptors messenger RNA by human cumulus granulosa cells is in correlation with decreased fertilization. Fertil. Steril. 97, 592-598. doi:10.1016/J.FERTNSTERT.2011.12.027
25. Mandl, A. M., and Zuckerman, S. (1952). The growth of the oocyte and follicle in the adult rat. J. Endocrinol. 8, 126-132. doi:10.1677/JOE.0. 0080126
26. Mattson, B. A., and Albertini, D. F. (1990). Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol. Reprod. Dev. 25, 374-383. doi:10.1002/MRD.1080250411
27. 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. doi:10.1093/HUMREP/DEH535
28. McNatty, K. P., Fidler, A. E., Juengel, J. L., Quirke, L. D., Smith, P. R., Heath, D. A., Lundy, T., O'Connell, A., and Tisdall, D. J. (2000). Growth and paracrine factors regulating follicular formation and cellular function. Mol. Cell. Endocrinol. 163, 11-20. doi:10.1016/S0303-7207(99) 00235-X
29. Papamentzelopoulou, M., Mavrogianni, D., Partsinevelos, G. A., Marinopoulos, S., Dinopoulou, V., Theofanakis, C., Anagnostou, E., and Loutradis, D. (2012). LH receptor gene expression in cumulus cells in women entering anARTprogram. J. Assist. Reprod. Genet. 29, 409-416. doi:10.1007/S10815-012-9729-7
30. Parfenov, V., Potchukalina, G., Dudina, L., Kostyuchek, D., and Gruzova, M. (1989). Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). Gamete Res. 22, 219-231. doi:10.1002/MRD.1120220209
31. Shimada, M., Nishibori, M., Isobe, N., Kawano, N., and Terada, T. (2003). Luteinizing hormone receptor formation in cumulus cells surrounding porcine oocytes and its role during meiotic maturation of porcine oocytes. Biol. Reprod. 68, 1142-1149. doi:10.1095/BIOLREPROD. 102.010082
32. Simões, R. A., Satrapa, R. A., Rosa, F. S., Piagentini, M., Castilho, A. C., Ereno, R. L., Trinca, L. A., Nogueira, M. F., Buratini, J., and Barros, C. M. (2012). Ovulation rate and its relationship with follicle diameter and gene expression of the LH receptor (LHR) in Nelore cows. Theriogenology 77, 139-147. doi:10.1016/J.THERIOGENOLOGY. 2011.07.027
33. Tan, J. H., Wang, H. L., Sun, X. S., Liu, Y., Sui, H. S., and Zhang, J. (2009). Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol. Hum. Reprod. 15, 1-9. doi:10.1093/MOLEHR/GAN069
34. Tisdall, D. J., Watanabe, K., Hudson, N. L., Smith, P., and McNatty, K. P. (1995). FSH receptor gene expression during ovarian follicle development in sheep. J. Mol. Endocrinol. 15, 273-281. doi:10.1677/JME.0. 0150273
35. 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. doi:10.1093/MOLEHR/GAM088
36. Vigone, G., Merico, V., Prigione, A., Mulas, F., Sacchi, L., Gabetta, M., Bellazzi, R., Redi, C. A., Mazzini, G., Adjaye, J., Garagna, S., and Zuccotti, M. (2013). Transcriptome based identification of mouse cumulus cell markers that predict the developmental competence of their enclosed antral oocytes. BMC Genomics 14, 380. doi:10.1186/1471-2164-14-380
37. Yang, S. H., Son, W. Y., Yoon, S. H., Ko, Y., and Lim, J. H. (2005). Correlation between in vitro maturation and expression of LH receptor in cumulus cells of the oocytes collected from PCOS patients in HCGprimed IVM cycles. Hum. Reprod. 20, 2097-2103. doi:10.1093/HUMREP/DEI045
38. 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 (Suppl.1), 1169-1179. doi:10.1016/J.FERTNSTERT.2004.11.030
39. Zuccotti, M., Piccinelli, A., Giorgi Rossi, P., Garagna, S., and Redi, C. A. (1995). Chromatin organization during mouse oocyte growth. Mol. Reprod. Dev. 41, 479-485. doi:10.1002/MRD.1080410410
40. Zuccotti, M., Giorgi Rossi, P., Martinez, A., Garagna, S., Forabosco, A., and Redi, C. A. (1998). Meiotic and developmental competence of mouse antral oocytes. Biol. Reprod. 58, 700-704. doi:10.1095/BIOLREPROD58.3.700
41. Zuccotti, M., Ponce, R. H., Boiani, M., Guizzardi, S., Govoni, P., Scandroglio, R., Garagna, S., and Redi, C. A. (2002). The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote 10, 73-78. doi:10.1017/S0967199402002101
42. Zuccotti, M., Garagna, S., Merico, V., Monti, M., and Alberto Redi, C. (2005). Chromatin organisation and nuclear architecture in growing mouse oocytes. Mol. Cell. Endocrinol. 234, 11-17. doi:10.1016/J.MCE.2004.08.014
43. Zuccotti, M., Merico, V., Cecconi, S., Redi, C. A., and Garagna, S. (2011). What does it take to make a developmentally competent mammalian egg? Hum. Reprod. Update 17, 525-540. doi:10.1093/HUMUPD/DMR009