A simple method for assessing hyaluronic acid production by cumulus-oocyte complexes
K. Zámostná, J. Nevoral, T. Kott, R. Procházka, M. Orsák, M. Šulc, V. Pajkošová, V. Pavlík, T. Žalmanová, K. Hošková, F. Jílek, P. Klein
https://doi.org/10.17221/51/2015-CJASCitation:Zámostná K., Nevoral J., Kott T., Procházka R., Orsák M., Šulc M., Pajkošová V., Pavlík V., Žalmanová T., Hošková K., Jílek F., Klein P. (2016): A simple method for assessing hyaluronic acid production by cumulus-oocyte complexes. Czech J. Anim. Sci., 61: 251-261.The cumulus expansion of cumulus-oocyte complex (COC) is an essential regulating process of oocyte maturation and as such it is a possible biomarker of the in vitro maturing oocytes quality. Cumulus expansion is usually assessed by non-invasive methods based on visual evaluation with many inaccuracies. On the other hand, analytical measurement of the quantity of hyaluronic acid (HA), the most abundant compound of expanded cumuli, is one of possible methods to evaluate cumulus expansion precisely. Therefore, this study aimed to verify the applicability of HA analysis for evaluating the cumulus expansion and testing oocyte maturation. The COCs were cultured in modified M199 medium for 8–48 h. The samples for the HA analysis were prepared on an 8-hour time scale, and HA retained in COCs was measured using a spectrophotometric method adapted for this purpose. We observed an increasing quantity of HA during the in vitro cultivation. A comparison with expanded COCs’ classification or expansion area proved the proposed method of HA analysis suitable for the evaluation of cumulus expansion in vitro. Our findings consider the quantity of HA-expressed cumulus expansion to be a valuable marker of COC quality enabling an adequate oocyte meiotic stage estimation.
Keywords:oocyte; meiotic maturation; cumulus expansion; glycosaminoglycans; spectrophotometry
References:Abeydeera L.R, Wang W.H, Cantley T.C, Prather R.S, Day B.N (1998): Presence of β-mercaptoethanol can increase the glutathione content of pig oocytes matured in vitro and the rate of blastocyst development after in vitro fertilization. Theriogenology, 50, 747-756 https://doi.org/10.1016/S0093-691X(98)00180-0 Alkrad Jamal Alyoussef, Mrestani Yahya, Stroehl Dieter, Wartewig Siegfried, Neubert Reinhard (2003): Characterization of enzymatically digested hyaluronic acid using NMR, Raman, IR, and UV–Vis spectroscopies. Journal of Pharmaceutical and Biomedical Analysis, 31, 545-550 https://doi.org/10.1016/S0731-7085(02)00682-9 Appeltant R., Somfai T., Nakai M., Bodó S., Maes D., Kikuchi K., Van Soom A. (2015): Interactions between oocytes and cumulus cells during in vitro maturation of porcine cumulus-oocyte complexes in a chemically defined medium: Effect of denuded oocytes on cumulus expansion and oocyte maturation. Theriogenology, 83, 567-576 https://doi.org/10.1016/j.theriogenology.2014.10.026 Assidi M., Dieleman S. J., Sirard M.-A. (): Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction, 140, 835-852 https://doi.org/10.1530/REP-10-0248 Assou S., Haouzi D., De Vos J., Hamamah S. (): Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Molecular Human Reproduction, 16, 531-538 https://doi.org/10.1093/molehr/gaq032 Bergandi L., Basso G., Evangelista F., Canosa S., Dalmasso P., Aldieri E., Revelli A., Benedetto C., Ghigo D. (): Inducible Nitric Oxide Synthase and Heme Oxygenase 1 Are Expressed in Human Cumulus Cells and May Be Used as Biomarkers of Oocyte Competence. Reproductive Sciences, , - https://doi.org/10.1177/1933719114525268 Chen Lin, Wert Susan E., Hendrix E. Michael, Russell Paul T., Cannon Michelle, Larsen William J. (1990): Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Molecular Reproduction and Development, 26, 236-247 https://doi.org/10.1002/mrd.1080260307 Daen F. P., Sato E., Naito K., Toyoda Y. (1994): The effect of pig follicular fluid fractions on cumulus expansion and male pronucleus formation in porcine oocytes matured and fertilized in vitro. Reproduction, 101, 667-673 https://doi.org/10.1530/jrf.0.1010667 Dadashpour Davachi N., Kohram H., Zainoaldini S. (2012): Cumulus cell layers as a critical factor in meiotic competence and cumulus expansion of ovine oocytes. Small Ruminant Research, 102, 37-42 https://doi.org/10.1016/j.smallrumres.2011.09.007 DEKEL N. (1979): Maturational Effects of Gonadotropins on the Cumulus-Oocyte Complex of the Rat. Biology of Reproduction, 20, 191-197 https://doi.org/10.1095/biolreprod20.2.191 Dekel Nava, Lawrence Theodore S., Gilula Norton B., Beers William H. (1981): Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. Developmental Biology, 86, 356-362 https://doi.org/10.1016/0012-1606(81)90193-7 Dragovic Rebecca A., Ritter Lesley J., Schulz Samantha J., Amato Fred, Armstrong David T., Gilchrist Robert B. (2005): Role of Oocyte-Secreted Growth Differentiation Factor 9 in the Regulation of Mouse Cumulus Expansion. Endocrinology, 146, 2798-2806 https://doi.org/10.1210/en.2005-0098 Eppig John J. (1979): FSH stimulates hyaluronic acid synthesis by oocyte–cumulus cellcomplexes from mouse preovulatory follicles. Nature, 281, 483-484 https://doi.org/10.1038/281483a0 Eppig John J. (1980): Role of Serum in FSH Stimulated Cumulus Expansion by Mouse Oocyte-Cumulus Cell Complexes in vitro. Biology of Reproduction, 22, 629-633 https://doi.org/10.1093/biolreprod/22.3.629 Fagbohun C. F. (1990): Maturation of the mouse oocyte-cumulus cell complex: stimulation by lectins. Biology of Reproduction, 42, 413-423 https://doi.org/10.1095/biolreprod42.3.413 Feuerstein Prisca, Puard Vincent, Chevalier Catherine, Teusan Raluca, Cadoret Veronique, Guerif Fabrice, Houlgatte Remi, Royere Dominique, Panepucci Rodrigo Alexandre (2012): Genomic Assessment of Human Cumulus Cell Marker Genes as Predictors of Oocyte Developmental Competence: Impact of Various Experimental Factors. PLoS ONE, 7, e40449- https://doi.org/10.1371/journal.pone.0040449
Flechon J.E., Degrouard J., Kopecny V., Pivko J., Pavlok A., Motlik J. (2003): The extracellular matrix of porcine mature oocytes: origin, composition and presumptive roles. Reproductive Biology and Endocrinology, 1, 124. https://doi.org/10.1186/1477-7827-1-124 Huang Z., Wells D. (): The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Molecular Human Reproduction, 16, 715-725 https://doi.org/10.1093/molehr/gaq031 Kimura N. (2002): Expression of Hyaluronan Synthases and CD44 Messenger RNAs in Porcine Cumulus-Oocyte Complexes During In Vitro Maturation. Biology of Reproduction, 66, 707-717 https://doi.org/10.1095/biolreprod66.3.707 Kubo Naoko, Cayo-Colca Ilse Silvia, Miyano Takashi (2015): Effect of estradiol-17β during in vitro growth culture on the growth, maturation, cumulus expansion and development of porcine oocytes from early antral follicles. Animal Science Journal, 86, 251-259 https://doi.org/10.1111/asj.12283 Machado Mariana Fernandes, Caixeta Ester Siqueira, Sudiman Jaqueline, Gilchrist Robert B., Thompson Jeremy G., Lima Paula Fernanda, Price Christopher A., Buratini José (2015): Fibroblast growth factor 17 and bone morphogenetic protein 15 enhance cumulus expansion and improve quality of in vitro–produced embryos in cattle. Theriogenology, 84, 390-398 https://doi.org/10.1016/j.theriogenology.2015.03.031 McKenzie L.J. (2004): Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Human Reproduction, 19, 2869-2874 https://doi.org/10.1093/humrep/deh535 Motlík Jan, Fulka Josef (1976): Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. Journal of Experimental Zoology, 198, 155-162 https://doi.org/10.1002/jez.1401980205 Nakayama T (1996): Effect of oocytectomy on glycosaminoglycan composition during cumulus expansion of porcine cumulus-oocyte complexes cultured in vitro. Biology of Reproduction, 55, 1299-1304 https://doi.org/10.1095/biolreprod55.6.1299 Nemcova L., Nagyova E., Petlach M., Tomanek M., Prochazka R. (): Molecular Mechanisms of Insulin-Like Growth Factor 1 Promoted Synthesis and Retention of Hyaluronic Acid in Porcine Oocyte-Cumulus Complexes. Biology of Reproduction, 76, 1016-1024 https://doi.org/10.1095/biolreprod.106.057927
Nevoral J., Orsak M., Klein P., Petr J., Dvorakova M., Weingartova I., Vyskocilova A., Zamostna K., Krejcova T., Jilek F. (2014): Cumulus cell expansion, its role in oocyte biology and perspectives of measurement: A review. Scientia Agriculturae Bohemica, 45, 212–225. Procházka Radek, Nagyov Eva, Brem Gottfried, Schellander Karl, Motlík Jan (1998): Secretion of cumulus expansion-enabling factor (CEEF) in porcine follicles. Molecular Reproduction and Development, 49, 141-149 https://doi.org/10.1002/(SICI)1098-2795(199802)49:2<141::AID-MRD5>3.0.CO;2-P Prochazka R., Petlach M., Nagyova E., Nemcova L. (): Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation, and acquisition of developmental competence in vitro: comparison with gonadotropins. Reproduction, 141, 425-435 https://doi.org/10.1530/REP-10-0418 QIAN Yun, SHI Wei Qun, DING Jia Tong, SHA Jia Hao, FAN Bi Qin (2003): Predictive Value of the Area of Expanded Cumulus Mass on Development of Porcine Oocytes Matured and Fertilized In Vitro. Journal of Reproduction and Development, 49, 167-174 https://doi.org/10.1262/jrd.49.167
Salustri A., Yanagishita M., Hascall V.C. (1989): Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification. Journal of Biological Chemistry, 264, 13840–13847.
Salustri A., Camaioni A., Tirone E., D’Alessandris C. (1995): Hyaluronic acid and proteoglycan accumulation in the cumulus oophorus matrix. Italian Journal of Anatomy and Embryology, 100, 479–484. Solursh Michael (1976): Glycosaminoglycan synthesis in the chick gastrula. Developmental Biology, 50, 525-530 https://doi.org/10.1016/0012-1606(76)90171-8 Takagaki Keiichi, Takeda Yusuke, Nakamura Toshiya, Daidouji Kouichi, Narita Hozumi, Endo Masahiko (1994): Analysis of glycosaminoglycans by high-performance liquid chromatography. Journal of Biochemical and Biophysical Methods, 28, 313-320 https://doi.org/10.1016/0165-022X(94)90007-8 Vanderhyden B. C. (1993): Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). Reproduction, 98, 219-227 https://doi.org/10.1530/jrf.0.0980219 Vanderhyden Barbara C., Caron Philip J., Buccione Roberto, Eppig John J. (1990): Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Developmental Biology, 140, 307-317 https://doi.org/10.1016/0012-1606(90)90081-S Volpi Nicola (2000): Hyaluronic Acid and Chondroitin Sulfate Unsaturated Disaccharides Analysis by High-Performance Liquid Chromatography and Fluorimetric Detection with Dansylhydrazine. Analytical Biochemistry, 277, 19-24 https://doi.org/10.1006/abio.1999.4366 Yokoo Masaki, Tienthai Paisan, Kimura Naoko, Niwa Koji, Sato Eimei, Rodriguez-Martinez Heriberto (2002): Localisation of the hyaluronan receptor CD44 in porcine cumulus cells during in vivo and in vitro maturation. Zygote, 10, - https://doi.org/10.1017/S0967199402004057 YOKOO Masaki, SHIMIZU Takashi, KIMURA Naoko, TUNJUNG Woro Anindito Sri, MATSUMOTO Hiromichi, ABE Hiroyuki, SASADA Hiroshi, RODRIGUEZ-MARTINEZ Heriberto, SATO Eimei (2007): Role of the Hyaluronan Receptor CD44 During Porcine Oocyte Maturation. Journal of Reproduction and Development, 53, 263-270 https://doi.org/10.1262/jrd.18047 YOKOO Masaki, KIMURA Naoko, SATO Eimei (2010): Induction of Oocyte Maturation by Hyaluronan-CD44 Interaction in Pigs. Journal of Reproduction and Development, 56, 15-19 https://doi.org/10.1262/jrd.09-173E Yosizawa Zensaku, Ototani Noboru, Satake Shigeo (1983): A simple method for the quantitation of glycuronic acid-containing glycosaminoglycans with mucopolysaccharidases. Analytical Biochemistry, 128, 250-256 https://doi.org/10.1016/0003-2697(83)90373-1 Yuan Ye, Ida Jennifer M., Paczkowski Melissa, Krisher Rebecca L. (2011): Identification of developmental competence-related genes in mature porcine oocytes. Molecular Reproduction and Development, 78, 565-575 https://doi.org/10.1002/mrd.21351 Zhang Meijia, Tao Yong, Xia Guoliang, Xie Huirong, Hong Haiyan, Wang Fengchao, Lei Lei (2005): Atrial natriuretic peptide negatively regulates follicle-stimulating hormone-induced porcine oocyte maturation and cumulus expansion via cGMP-dependent protein kinase pathway. Theriogenology, 64, 902-916 https://doi.org/10.1016/j.theriogenology.2004.12.012 Abeydeera L.R, Wang W.H, Cantley T.C, Prather R.S, Day B.N (1998): Presence of β-mercaptoethanol can increase the glutathione content of pig oocytes matured in vitro and the rate of blastocyst development after in vitro fertilization. Theriogenology, 50, 747-756 https://doi.org/10.1016/S0093-691X(98)00180-0 Alkrad Jamal Alyoussef, Mrestani Yahya, Stroehl Dieter, Wartewig Siegfried, Neubert Reinhard (2003): Characterization of enzymatically digested hyaluronic acid using NMR, Raman, IR, and UV–Vis spectroscopies. Journal of Pharmaceutical and Biomedical Analysis, 31, 545-550 https://doi.org/10.1016/S0731-7085(02)00682-9 Appeltant R., Somfai T., Nakai M., Bodó S., Maes D., Kikuchi K., Van Soom A. (2015): Interactions between oocytes and cumulus cells during in vitro maturation of porcine cumulus-oocyte complexes in a chemically defined medium: Effect of denuded oocytes on cumulus expansion and oocyte maturation. Theriogenology, 83, 567-576 https://doi.org/10.1016/j.theriogenology.2014.10.026 Assidi M., Dieleman S. J., Sirard M.-A. (): Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction, 140, 835-852 https://doi.org/10.1530/REP-10-0248 Assou S., Haouzi D., De Vos J., Hamamah S. (): Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Molecular Human Reproduction, 16, 531-538 https://doi.org/10.1093/molehr/gaq032 Bergandi L., Basso G., Evangelista F., Canosa S., Dalmasso P., Aldieri E., Revelli A., Benedetto C., Ghigo D. (): Inducible Nitric Oxide Synthase and Heme Oxygenase 1 Are Expressed in Human Cumulus Cells and May Be Used as Biomarkers of Oocyte Competence. Reproductive Sciences, , - https://doi.org/10.1177/1933719114525268 Chen Lin, Wert Susan E., Hendrix E. Michael, Russell Paul T., Cannon Michelle, Larsen William J. (1990): Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Molecular Reproduction and Development, 26, 236-247 https://doi.org/10.1002/mrd.1080260307 Daen F. P., Sato E., Naito K., Toyoda Y. (1994): The effect of pig follicular fluid fractions on cumulus expansion and male pronucleus formation in porcine oocytes matured and fertilized in vitro. Reproduction, 101, 667-673 https://doi.org/10.1530/jrf.0.1010667 Dadashpour Davachi N., Kohram H., Zainoaldini S. (2012): Cumulus cell layers as a critical factor in meiotic competence and cumulus expansion of ovine oocytes. Small Ruminant Research, 102, 37-42 https://doi.org/10.1016/j.smallrumres.2011.09.007 DEKEL N. (1979): Maturational Effects of Gonadotropins on the Cumulus-Oocyte Complex of the Rat. Biology of Reproduction, 20, 191-197 https://doi.org/10.1095/biolreprod20.2.191 Dekel Nava, Lawrence Theodore S., Gilula Norton B., Beers William H. (1981): Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. Developmental Biology, 86, 356-362 https://doi.org/10.1016/0012-1606(81)90193-7 Dragovic Rebecca A., Ritter Lesley J., Schulz Samantha J., Amato Fred, Armstrong David T., Gilchrist Robert B. (2005): Role of Oocyte-Secreted Growth Differentiation Factor 9 in the Regulation of Mouse Cumulus Expansion. Endocrinology, 146, 2798-2806 https://doi.org/10.1210/en.2005-0098 Eppig John J. (1979): FSH stimulates hyaluronic acid synthesis by oocyte–cumulus cellcomplexes from mouse preovulatory follicles. Nature, 281, 483-484 https://doi.org/10.1038/281483a0 Eppig John J. (1980): Role of Serum in FSH Stimulated Cumulus Expansion by Mouse Oocyte-Cumulus Cell Complexes in vitro. Biology of Reproduction, 22, 629-633 https://doi.org/10.1093/biolreprod/22.3.629 Fagbohun C. F. (1990): Maturation of the mouse oocyte-cumulus cell complex: stimulation by lectins. Biology of Reproduction, 42, 413-423 https://doi.org/10.1095/biolreprod42.3.413 Feuerstein Prisca, Puard Vincent, Chevalier Catherine, Teusan Raluca, Cadoret Veronique, Guerif Fabrice, Houlgatte Remi, Royere Dominique, Panepucci Rodrigo Alexandre (2012): Genomic Assessment of Human Cumulus Cell Marker Genes as Predictors of Oocyte Developmental Competence: Impact of Various Experimental Factors. PLoS ONE, 7, e40449- https://doi.org/10.1371/journal.pone.0040449
Flechon J.E., Degrouard J., Kopecny V., Pivko J., Pavlok A., Motlik J. (2003): The extracellular matrix of porcine mature oocytes: origin, composition and presumptive roles. Reproductive Biology and Endocrinology, 1, 124. https://doi.org/10.1186/1477-7827-1-124 Huang Z., Wells D. (): The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Molecular Human Reproduction, 16, 715-725 https://doi.org/10.1093/molehr/gaq031 Kimura N. (2002): Expression of Hyaluronan Synthases and CD44 Messenger RNAs in Porcine Cumulus-Oocyte Complexes During In Vitro Maturation. Biology of Reproduction, 66, 707-717 https://doi.org/10.1095/biolreprod66.3.707 Kubo Naoko, Cayo-Colca Ilse Silvia, Miyano Takashi (2015): Effect of estradiol-17β during in vitro growth culture on the growth, maturation, cumulus expansion and development of porcine oocytes from early antral follicles. Animal Science Journal, 86, 251-259 https://doi.org/10.1111/asj.12283 Machado Mariana Fernandes, Caixeta Ester Siqueira, Sudiman Jaqueline, Gilchrist Robert B., Thompson Jeremy G., Lima Paula Fernanda, Price Christopher A., Buratini José (2015): Fibroblast growth factor 17 and bone morphogenetic protein 15 enhance cumulus expansion and improve quality of in vitro–produced embryos in cattle. Theriogenology, 84, 390-398 https://doi.org/10.1016/j.theriogenology.2015.03.031 McKenzie L.J. (2004): Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Human Reproduction, 19, 2869-2874 https://doi.org/10.1093/humrep/deh535 Motlík Jan, Fulka Josef (1976): Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. Journal of Experimental Zoology, 198, 155-162 https://doi.org/10.1002/jez.1401980205 Nakayama T (1996): Effect of oocytectomy on glycosaminoglycan composition during cumulus expansion of porcine cumulus-oocyte complexes cultured in vitro. Biology of Reproduction, 55, 1299-1304 https://doi.org/10.1095/biolreprod55.6.1299 Nemcova L., Nagyova E., Petlach M., Tomanek M., Prochazka R. (): Molecular Mechanisms of Insulin-Like Growth Factor 1 Promoted Synthesis and Retention of Hyaluronic Acid in Porcine Oocyte-Cumulus Complexes. Biology of Reproduction, 76, 1016-1024 https://doi.org/10.1095/biolreprod.106.057927
Nevoral J., Orsak M., Klein P., Petr J., Dvorakova M., Weingartova I., Vyskocilova A., Zamostna K., Krejcova T., Jilek F. (2014): Cumulus cell expansion, its role in oocyte biology and perspectives of measurement: A review. Scientia Agriculturae Bohemica, 45, 212–225. Procházka Radek, Nagyov Eva, Brem Gottfried, Schellander Karl, Motlík Jan (1998): Secretion of cumulus expansion-enabling factor (CEEF) in porcine follicles. Molecular Reproduction and Development, 49, 141-149 https://doi.org/10.1002/(SICI)1098-2795(199802)49:2<141::AID-MRD5>3.0.CO;2-P Prochazka R., Petlach M., Nagyova E., Nemcova L. (): Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation, and acquisition of developmental competence in vitro: comparison with gonadotropins. Reproduction, 141, 425-435 https://doi.org/10.1530/REP-10-0418 QIAN Yun, SHI Wei Qun, DING Jia Tong, SHA Jia Hao, FAN Bi Qin (2003): Predictive Value of the Area of Expanded Cumulus Mass on Development of Porcine Oocytes Matured and Fertilized In Vitro. Journal of Reproduction and Development, 49, 167-174 https://doi.org/10.1262/jrd.49.167
Salustri A., Yanagishita M., Hascall V.C. (1989): Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification. Journal of Biological Chemistry, 264, 13840–13847.
Salustri A., Camaioni A., Tirone E., D’Alessandris C. (1995): Hyaluronic acid and proteoglycan accumulation in the cumulus oophorus matrix. Italian Journal of Anatomy and Embryology, 100, 479–484. Solursh Michael (1976): Glycosaminoglycan synthesis in the chick gastrula. Developmental Biology, 50, 525-530 https://doi.org/10.1016/0012-1606(76)90171-8 Takagaki Keiichi, Takeda Yusuke, Nakamura Toshiya, Daidouji Kouichi, Narita Hozumi, Endo Masahiko (1994): Analysis of glycosaminoglycans by high-performance liquid chromatography. Journal of Biochemical and Biophysical Methods, 28, 313-320 https://doi.org/10.1016/0165-022X(94)90007-8 Vanderhyden B. C. (1993): Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). Reproduction, 98, 219-227 https://doi.org/10.1530/jrf.0.0980219 Vanderhyden Barbara C., Caron Philip J., Buccione Roberto, Eppig John J. (1990): Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Developmental Biology, 140, 307-317 https://doi.org/10.1016/0012-1606(90)90081-S Volpi Nicola (2000): Hyaluronic Acid and Chondroitin Sulfate Unsaturated Disaccharides Analysis by High-Performance Liquid Chromatography and Fluorimetric Detection with Dansylhydrazine. Analytical Biochemistry, 277, 19-24 https://doi.org/10.1006/abio.1999.4366 Yokoo Masaki, Tienthai Paisan, Kimura Naoko, Niwa Koji, Sato Eimei, Rodriguez-Martinez Heriberto (2002): Localisation of the hyaluronan receptor CD44 in porcine cumulus cells during in vivo and in vitro maturation. Zygote, 10, - https://doi.org/10.1017/S0967199402004057 YOKOO Masaki, SHIMIZU Takashi, KIMURA Naoko, TUNJUNG Woro Anindito Sri, MATSUMOTO Hiromichi, ABE Hiroyuki, SASADA Hiroshi, RODRIGUEZ-MARTINEZ Heriberto, SATO Eimei (2007): Role of the Hyaluronan Receptor CD44 During Porcine Oocyte Maturation. Journal of Reproduction and Development, 53, 263-270 https://doi.org/10.1262/jrd.18047 YOKOO Masaki, KIMURA Naoko, SATO Eimei (2010): Induction of Oocyte Maturation by Hyaluronan-CD44 Interaction in Pigs. Journal of Reproduction and Development, 56, 15-19 https://doi.org/10.1262/jrd.09-173E Yosizawa Zensaku, Ototani Noboru, Satake Shigeo (1983): A simple method for the quantitation of glycuronic acid-containing glycosaminoglycans with mucopolysaccharidases. Analytical Biochemistry, 128, 250-256 https://doi.org/10.1016/0003-2697(83)90373-1 Yuan Ye, Ida Jennifer M., Paczkowski Melissa, Krisher Rebecca L. (2011): Identification of developmental competence-related genes in mature porcine oocytes. Molecular Reproduction and Development, 78, 565-575 https://doi.org/10.1002/mrd.21351 Zhang Meijia, Tao Yong, Xia Guoliang, Xie Huirong, Hong Haiyan, Wang Fengchao, Lei Lei (2005): Atrial natriuretic peptide negatively regulates follicle-stimulating hormone-induced porcine oocyte maturation and cumulus expansion via cGMP-dependent protein kinase pathway. Theriogenology, 64, 902-916 https://doi.org/10.1016/j.theriogenology.2004.12.012 Abeydeera L.R, Wang W.H, Cantley T.C, Prather R.S, Day B.N (1998): Presence of β-mercaptoethanol can increase the glutathione content of pig oocytes matured in vitro and the rate of blastocyst development after in vitro fertilization. Theriogenology, 50, 747-756 https://doi.org/10.1016/S0093-691X(98)00180-0 Alkrad Jamal Alyoussef, Mrestani Yahya, Stroehl Dieter, Wartewig Siegfried, Neubert Reinhard (2003): Characterization of enzymatically digested hyaluronic acid using NMR, Raman, IR, and UV–Vis spectroscopies. Journal of Pharmaceutical and Biomedical Analysis, 31, 545-550 https://doi.org/10.1016/S0731-7085(02)00682-9 Appeltant R., Somfai T., Nakai M., Bodó S., Maes D., Kikuchi K., Van Soom A. (2015): Interactions between oocytes and cumulus cells during in vitro maturation of porcine cumulus-oocyte complexes in a chemically defined medium: Effect of denuded oocytes on cumulus expansion and oocyte maturation. Theriogenology, 83, 567-576 https://doi.org/10.1016/j.theriogenology.2014.10.026 Assidi M., Dieleman S. J., Sirard M.-A. (): Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Reproduction, 140, 835-852 https://doi.org/10.1530/REP-10-0248 Assou S., Haouzi D., De Vos J., Hamamah S. (): Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Molecular Human Reproduction, 16, 531-538 https://doi.org/10.1093/molehr/gaq032 Bergandi L., Basso G., Evangelista F., Canosa S., Dalmasso P., Aldieri E., Revelli A., Benedetto C., Ghigo D. (): Inducible Nitric Oxide Synthase and Heme Oxygenase 1 Are Expressed in Human Cumulus Cells and May Be Used as Biomarkers of Oocyte Competence. Reproductive Sciences, , - https://doi.org/10.1177/1933719114525268 Chen Lin, Wert Susan E., Hendrix E. Michael, Russell Paul T., Cannon Michelle, Larsen William J. (1990): Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Molecular Reproduction and Development, 26, 236-247 https://doi.org/10.1002/mrd.1080260307 Daen F. P., Sato E., Naito K., Toyoda Y. (1994): The effect of pig follicular fluid fractions on cumulus expansion and male pronucleus formation in porcine oocytes matured and fertilized in vitro. Reproduction, 101, 667-673 https://doi.org/10.1530/jrf.0.1010667 Dadashpour Davachi N., Kohram H., Zainoaldini S. (2012): Cumulus cell layers as a critical factor in meiotic competence and cumulus expansion of ovine oocytes. Small Ruminant Research, 102, 37-42 https://doi.org/10.1016/j.smallrumres.2011.09.007 DEKEL N. (1979): Maturational Effects of Gonadotropins on the Cumulus-Oocyte Complex of the Rat. Biology of Reproduction, 20, 191-197 https://doi.org/10.1095/biolreprod20.2.191 Dekel Nava, Lawrence Theodore S., Gilula Norton B., Beers William H. (1981): Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. 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2018: 1.008
Q3 – Agriculture, Dairy and Animal Science
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