{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,2]],"date-time":"2026-05-02T16:04:29Z","timestamp":1777737869615,"version":"3.51.4"},"reference-count":75,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2026,4,27]],"date-time":"2026-04-27T00:00:00Z","timestamp":1777248000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Increased heat levels can affect follicle development, oocyte maturation, and bovine fertility by disrupting amino acid (AA) metabolism and oocyte competence. This study aimed to explore the effect of heat shock on AA metabolism in bovine cumulus cells (CCs) or denuded oocytes (DOs). CCs and DOs were separately cultured for 24 h in vitro at 38.5 \u00b0C (control group), 39.5 \u00b0C (moderate heat shock-CC, MHS-CC group), or 40.5 \u00b0C (high heat shock-CC, HHS-CC group). AA levels were analyzed in 24-h in vitro maturation media using high-performance liquid chromatography. The findings indicated that the HHS-CC group consumed more AAs than the control (p = 0.04) or MHS-CC group (p = 0.03). Compared with the control and HHS-CC groups, the MHS-CC group exhibited elevated alanine levels (p = 0.02). The MHS-CC (p = 0.03) and HHS-CC (p = 0.03) groups exhibited significantly greater glutamine depletion than the control group. The HHS-DO group exhibited significant lysine depletion (p &lt; 0.01) but produced more tryptophan than the control and MHS-DO groups (p = 0.02). In contrast to the control and MHS-DO groups, the HHS-DO group displayed a notably elevated level of appearance (p = 0.005) and net balance (p = 0.005) for all AAs. The findings imply that heat shock may alter the metabolism of certain AAs in CCs and DOs, thereby affecting the developmental competence of bovine oocytes.<\/jats:p>","DOI":"10.3390\/biology15090682","type":"journal-article","created":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T10:34:42Z","timestamp":1777458882000},"page":"682","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Heat Shock Affects Amino Acid Metabolism in Bovine Cumulus Cells and Denuded Oocytes During In Vitro Maturation"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5635-3663","authenticated-orcid":false,"given":"Hayder Radhi Hussein","family":"Mzedawee","sequence":"first","affiliation":[{"name":"Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan 8415683111, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rasoul","family":"Kowsar","sequence":"additional","affiliation":[{"name":"Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan 8415683111, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-6672-1174","authenticated-orcid":false,"given":"Golnaz","family":"Manian","sequence":"additional","affiliation":[{"name":"Department of Animal Science, College of Agriculture, Isfahan University of Technology, Isfahan 8415683111, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mehdi","family":"Hajian","sequence":"additional","affiliation":[{"name":"Department of Animal Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan 8165131378, Iran"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2026,4,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"100082","DOI":"10.1016\/j.csag.2025.100082","article-title":"The impacts of climate change on livestock: An interdisciplinary, scoping review of health, production, and adaptation strategies","volume":"2","author":"Anuta","year":"2025","journal-title":"Clim. Smart Agric."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"390","DOI":"10.3168\/jds.S0022-0302(02)74086-1","article-title":"Effect of season and exposure to heat stress on oocyte competence in Holstein cows","volume":"85","author":"Hansen","year":"2002","journal-title":"J. Dairy Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1530\/rep.0.1210447","article-title":"Seasonal changes in bovine fertility: Relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles","volume":"121","author":"Zeron","year":"2001","journal-title":"Reproduction"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1093\/ajae\/aau002","article-title":"Potential effects of climate change on the productivity of US dairies","volume":"96","author":"Key","year":"2014","journal-title":"Am. J. Agric. Econ."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1007\/s11250-022-03151-5","article-title":"Interrelationship between diseases and calving season and their impact on reproductive parameters and milk production of tropical dairy cows","volume":"54","author":"Mendoza","year":"2022","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"6660","DOI":"10.3168\/jds.2018-16011","article-title":"Influence of on-farm measurements for heat stress indicators on dairy cow productivity, female fertility, and health","volume":"102","author":"Gernand","year":"2019","journal-title":"J. Dairy Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"267","DOI":"10.3945\/an.112.003376","article-title":"Nutritional interventions to alleviate the negative consequences of heat stress","volume":"4","author":"Rhoads","year":"2013","journal-title":"Adv. Nutr."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.anireprosci.2012.07.009","article-title":"In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression","volume":"134","author":"Gendelman","year":"2012","journal-title":"Anim. Reprod. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2034","DOI":"10.2527\/jas.2014-8625","article-title":"Physiology and endocrinology symposium: Cellular and molecular mechanisms of heat stress related to bovine ovarian function","volume":"93","author":"Roth","year":"2015","journal-title":"J. Anim. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4326","DOI":"10.3168\/jds.S0022-0302(05)73119-2","article-title":"Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes","volume":"88","author":"Edwards","year":"2005","journal-title":"J. Dairy Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1530\/rep.1.00394","article-title":"Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation","volume":"129","author":"Roth","year":"2005","journal-title":"Reproduction"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1303","DOI":"10.1095\/biolreprod.104.029892","article-title":"Susceptibility of Bovine Germinal Vesicle-Stage Oocytes from Antral Follicles to Direct Effects of Heat Stress In Vitro","volume":"71","author":"Payton","year":"2004","journal-title":"Biol. Reprod."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"G\u00f3mez-Guzm\u00e1n, J.A., Parra-Bracamonte, G.M., and Velazquez, M.A. (2024). Impact of heat stress on oocyte developmental competence and pre-implantation embryo viability in cattle. Animals, 14.","DOI":"10.3390\/ani14152280"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1146\/annurev-physiol-022516-034102","article-title":"Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle","volume":"79","author":"Jaffe","year":"2017","journal-title":"Annu. Rev. Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.2527\/jas.2012-5802","article-title":"Physiology and endocrinology symposium: Influence of cattle genotype (Bos indicus vs. Bos taurus) on oocyte and preimplantation embryo resistance to increased temperature","volume":"91","author":"Lima","year":"2013","journal-title":"J. Anim. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/S0301-6226(00)00232-3","article-title":"Influence of heat stress or feed restriction on plasma progesterone, oestradiol-17\u03b2, LH, FSH, prolactin and cortisol in Holstein heifers","volume":"68","author":"Ronchi","year":"2001","journal-title":"Livest. Prod. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1016\/S0378-4320(00)00102-0","article-title":"Impaired reproduction in heat-stressed cattle: Basic and applied aspects","volume":"60","author":"Wolfenson","year":"2000","journal-title":"Anim. Reprod. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.theriogenology.2019.09.005","article-title":"The effects of glycine-glutamine dipeptide replaced l-glutamine on bovine parthenogenetic and IVF embryo development","volume":"141","author":"Zuo","year":"2020","journal-title":"Theriogenology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2111","DOI":"10.3168\/jds.2023-23804","article-title":"The effect of heat stress on performance, fertility, and adipokines involved in regulating systemic immune response during lipolysis of early lactating dairy cows","volume":"107","author":"Stefanska","year":"2024","journal-title":"J. Dairy Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1530\/reprod\/120.1.83","article-title":"Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows","volume":"120","author":"Roth","year":"2000","journal-title":"J. Reprod. Fertil."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.theriogenology.2020.05.040","article-title":"Reproductive physiology and endocrinology responses of cows exposed to environmental heat stress\u2014Experiences from the past and lessons for the present","volume":"155","author":"Roth","year":"2020","journal-title":"Theriogenology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1007\/s00726-023-03370-6","article-title":"Heat shock interferes with the amino acid metabolism of bovine cumulus-oocyte complexes in vitro: A multistep analysis","volume":"56","author":"Mzedawee","year":"2024","journal-title":"Amino Acids"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1093\/humrep\/des458","article-title":"Amino acid turnover by human oocytes is influenced by gamete developmental competence, patient characteristics and gonadotrophin treatment","volume":"28","author":"Hemmings","year":"2013","journal-title":"Hum. Reprod."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1756","DOI":"10.1093\/humrep\/deg389","article-title":"Non-invasive amino acid turnover predicts human embryo developmental capacity","volume":"18","author":"Houghton","year":"2003","journal-title":"Hum. Reprod."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1387\/ijdb.120140ec","article-title":"Metabolism throughout follicle and oocyte development in mammals","volume":"56","author":"Picton","year":"2012","journal-title":"Int. J. Dev. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1095\/biolreprod.111.092585","article-title":"Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro","volume":"86","author":"Hemmings","year":"2012","journal-title":"Biol. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1210\/me.2013-1413","article-title":"Minireview: Metabolism of female reproduction: Regulatory mechanisms and clinical implications","volume":"28","author":"Seli","year":"2014","journal-title":"Mol. Endocrinol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.theriogenology.2023.04.009","article-title":"Oocyte-cumulus cells crosstalk: New comparative insights","volume":"205","author":"Martinez","year":"2023","journal-title":"Theriogenology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1042\/BSR20192188","article-title":"Dynamic characteristics of lipid metabolism in cultured granulosa cells from geese follicles at different developmental stages","volume":"39","author":"Gao","year":"2019","journal-title":"Biosci. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1093\/humupd\/dmm040","article-title":"Oocyte-secreted factors: Regulators of cumulus cell function and oocyte quality","volume":"14","author":"Gilchrist","year":"2008","journal-title":"Hum. Reprod. Update"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1093\/humupd\/dmaa043","article-title":"Metabolic co-dependence of the oocyte and cumulus cells: Essential role in determining oocyte developmental competence","volume":"27","author":"Richani","year":"2021","journal-title":"Hum. Reprod. Update"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1095\/biolreprod.105.041798","article-title":"Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: Amino acid transport","volume":"73","author":"Eppig","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1093\/molehr\/gaq031","article-title":"The human oocyte and cumulus cells relationship: New insights from the cumulus cell transcriptome","volume":"16","author":"Huang","year":"2010","journal-title":"Mol. Hum. Reprod."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"43193","DOI":"10.1074\/jbc.M111.297358","article-title":"Regulation of oocyte and cumulus cell interactions by intermedin\/adrenomedullin 2","volume":"286","author":"Chang","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"100055","DOI":"10.59717\/j.xinn-med.2024.100055","article-title":"Future perspectives of non-invasive techniques for evaluating oocyte and embryo quality","volume":"2","author":"Zeng","year":"2024","journal-title":"Innov. Med."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1071\/RD22217","article-title":"Non-invasive assessment of oocyte developmental competence","volume":"35","author":"Tan","year":"2022","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1002\/mrd.21145","article-title":"Amino acid metabolism of bovine blastocysts: A biomarker of sex and viability","volume":"77","author":"Sturmey","year":"2010","journal-title":"Mol. Reprod. Dev."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"12191","DOI":"10.1038\/s41598-018-30774-2","article-title":"Urea influences amino acid turnover in bovine cumulus-oocyte complexes, cumulus cells and denuded oocytes, and affects in vitro fertilization outcome","volume":"8","author":"Kowsar","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Liu, X., Hao, Y., Li, Z., Zhou, J., Zhu, H., Bu, G., Liu, Z., Hou, X., Zhang, X., and Miao, Y.L. (2020). Maternal cytokines CXCL12, VEGFA, and WNT5A promote porcine oocyte maturation via MAPK Activation and canonical WNT inhibition. Front. Cell Dev. Biol., 8.","DOI":"10.3389\/fcell.2020.00578"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1262\/jrd.2018-130","article-title":"Removal of cumulus cells around 20 h after the start of in vitro maturation improves the meiotic competence of porcine oocytes via reduction in cAMP and cGMP levels","volume":"65","author":"Nguyen","year":"2019","journal-title":"J. Reprod. Dev."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2376","DOI":"10.1016\/j.fertnstert.2007.10.054","article-title":"Coculture with cumulus cells improves maturation of mouse oocytes denuded of the cumulus oophorus: Observations of nuclear and cytoplasmic events","volume":"90","author":"Ge","year":"2008","journal-title":"Fertil. Steril."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Lipinska, P., Sell-Kubiak, E., Pawlak, P., Madeja, Z.E., and Warzych, E. (2021). Response of bovine cumulus-oocytes complexes to energy pathway inhibition during in vitro maturation. Genes, 12.","DOI":"10.3390\/genes12060838"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"16082","DOI":"10.1038\/s41598-020-73225-7","article-title":"A multilevel analysis identifies the different relationships between amino acids and the competence of oocytes matured individually or in groups","volume":"10","author":"Kowsar","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1177\/000456329503200103","article-title":"Quantitative methods for amino acid analysis in biological fluids","volume":"32","author":"Walker","year":"1995","journal-title":"Ann. Clin. Biochem."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"D\u2019Mello, J.P.F. (2003). Amino acids as multifunctional molecules. Amino Acids in Animal Nutrition, CABI. [2nd ed.].","DOI":"10.1079\/9780851996547.0000"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1177\/1535370215587913","article-title":"Dietary essentiality of \u201cnutritionally non-essential amino acids\u201d for animals and humans","volume":"240","author":"Hou","year":"2015","journal-title":"Exp. Biol. Med."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s00726-008-0210-y","article-title":"Arginine metabolism and nutrition in growth, health and disease","volume":"37","author":"Wu","year":"2009","journal-title":"Amino Acids"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"839","DOI":"10.2298\/JSC120712144J","article-title":"Validation of an HPLC method for the determination of amino acids in feed","volume":"78","year":"2013","journal-title":"J. Serb. Chem. Soc."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1093\/biolre\/ioaf070","article-title":"Heat stress during maturation of bovine oocytes profoundly impacts the mitochondrial bioenergetic profile and causes endoplasmic reticulum stress in subsequent blastocysts","volume":"112","author":"Haake","year":"2025","journal-title":"Biol. Reprod."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Ga\u0142eska, E., Kowalczyk, A., Wrzecinska, M., Garcia, M.C., Czerniawska-Piatkowska, E., Gwo\u017adziewicz, S., Witkiewicz, W., and Dobrza\u0144ski, Z. (2025). The importance of mitochondrial processes in the maturation and acquisition of competences of oocytes and embryo culture. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26094098"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1210\/me.2014-1049","article-title":"Fatty acid synthesis and oxidation in cumulus cells support oocyte maturation in bovine","volume":"28","author":"Brisard","year":"2014","journal-title":"Mol. Endocrinol."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Sammad, A., Hu, L., Luo, H., Abbas, Z., Umer, S., Zhao, S., Xu, Q., Khan, A., Wang, Y., and Zhu, H. (2022). Investigation of metabolome underlying the biological mechanisms of acute heat stressed granulosa cells. Int. J. Mol. Sci., 15.","DOI":"10.3390\/ijms23042146"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Turathum, B., Gao, E.M., and Chian, R.C. (2021). The Function of Cumulus Cells in Oocyte Growth and Maturation and in Subsequent Ovulation and Fertilization. Cells, 10.","DOI":"10.3390\/cells10092292"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"M\u00e1rquez, D., Escalera-Fanjul, X., el Hafidi, M., Aguirre-L\u00f3pez, B., Riego-Ruiz, L., and Gonz\u00e1lez, A. (2021). Alanine represses -aminobutyric acid utilization and induces alanine transaminase required for mitochondrial function in saccharomyces cerevisiae. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.695382"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3811","DOI":"10.1038\/s41467-020-17512-x","article-title":"Purine metabolism regulates DNA repair and therapy resistance in glioblastoma","volume":"11","author":"Zhou","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1556","DOI":"10.1038\/ncb3272","article-title":"Glutamine synthetase activity fuels nucleotide biosynthesis and supports growth of glutamine-restricted glioblastoma","volume":"17","author":"Tardito","year":"2015","journal-title":"Nat. Cell Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"103927","DOI":"10.1016\/j.jtherbio.2024.103927","article-title":"The effects and mechanisms of heat stress on mammalian oocyte and embryo development","volume":"124","author":"Li","year":"2024","journal-title":"J. Therm. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s40560-024-00774-8","article-title":"Impact of hyper- and hypothermia on cellular and whole-body physiology","volume":"13","author":"Iba","year":"2025","journal-title":"J. Intensive Care"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1426","DOI":"10.1093\/jn\/nxy140","article-title":"Lysine stimulates protein synthesis by promoting the expression of ATB0,+ and activating the mTOR pathway in bovine mammary epithelial cells","volume":"148","author":"Lin","year":"2018","journal-title":"J. Nutr."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"103375","DOI":"10.1016\/j.jtherbio.2022.103375","article-title":"Lysine promotes proliferation and \u03b2-casein synthesis through the SLC6A14-ERK1\/2-CDK1-mTOR signaling pathway in bovine primary mammary epithelial cells","volume":"110","author":"Cao","year":"2022","journal-title":"J. Therm. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"8952520","DOI":"10.1155\/2016\/8952520","article-title":"Tryptophan biochemistry: Structural, nutritional, metabolic, and medical aspects in humans","volume":"2016","author":"Palego","year":"2016","journal-title":"J. Amino Acids"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1007\/s43032-021-00505-6","article-title":"Reprogramming of glucose metabolism of cumulus cells and oocytes and its therapeutic significance","volume":"29","author":"Imanaka","year":"2022","journal-title":"Reprod. Sci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1071\/RD21282","article-title":"Nurturing the egg: The essential connection between cumulus cells and the oocyte","volume":"34","author":"Robert","year":"2021","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1530\/REP-09-0345","article-title":"The pivotal role of glucose metabolism in determining oocyte developmental competence","volume":"139","author":"Gilchrist","year":"2010","journal-title":"Reproduction"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1089\/ars.2019.7984","article-title":"Redox Biology of Human Cumulus Cells: Basic Concepts, Impact on Oocyte Quality, and Potential Clinical Use","volume":"32","author":"Klamt","year":"2020","journal-title":"Antioxid. Redox Signal."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Del Bianco, D., Gentile, R., Sallicandro, L., Biagini, A., Quellari, P.T., Gliozheni, E., Sabbatini, P., Ragonese, F., Malvasi, A., and D\u2019Amato, A. (2024). Electro-metabolic coupling of cumulus-oocyte complex. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25105349"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Regassa, A., Rings, F., Hoelker, M., Cinar, U., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2011). Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genom., 12.","DOI":"10.1186\/1471-2164-12-57"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"E599","DOI":"10.1152\/ajpendo.00469.2012","article-title":"Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes","volume":"67","author":"Auclair","year":"2013","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref_69","first-page":"3091","article-title":"Oocyte-dependent activation of MTOR in cumulus cells controls the development and survival of cumulus-oocyte complexes","volume":"29","author":"Guo","year":"2016","journal-title":"J. Cell Sci."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Fountas, S., Petinaki, E., Bolaris, S., Kargakou, M., Dafopoulos, S., Zikopoulos, A., Moustakli, E., Sotiriou, S., and Dafopoulos, K. (2024). The roles of GDF-9, BMP-15, BMP-4 and EMMPRIN in folliculogenesis and in vitro fertilization. J. Clin. Med., 13.","DOI":"10.3390\/jcm13133775"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1093\/molehr\/gaq040","article-title":"Association between amino acid turnover and chromosome aneuploidy during human preimplantation embryo development in vitro","volume":"16","author":"Picton","year":"2010","journal-title":"Mol. Hum. Reprod."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1007\/s10616-016-0022-y","article-title":"Developmental competence and expression profile of genes in buffalo (Bubalus bubalis) oocytes and embryos collected under different environmental stress","volume":"68","author":"Sadeesh","year":"2016","journal-title":"Cytotechnology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1093\/biolre\/ioaa194","article-title":"Effect of mitophagy in oocytes and granulosa cells on oocyte quality","volume":"104","author":"Shen","year":"2021","journal-title":"Biol. Reprod."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Sadeesh, E.M., Lahamge, M.S., Kumari, S., and Singh, P. (2025). Tissue-specific diversity of nuclear-encoded mitochondrial genes related to lipid and carbohydrate metabolism in buffalo. Mol. Biotechnol.","DOI":"10.1007\/s00726-025-03447-4"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s00726-025-03447-4","article-title":"Unveiling the tissue-specific landscape of nuclear-encoded mitochondrial genes involved in amino acid metabolism in buffalo","volume":"57","author":"Sadeesh","year":"2025","journal-title":"Amino Acids"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/9\/682\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T11:20:38Z","timestamp":1777461638000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/9\/682"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,27]]},"references-count":75,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,5]]}},"alternative-id":["biology15090682"],"URL":"https:\/\/doi.org\/10.3390\/biology15090682","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,27]]}}}