Characterization of metabolic patterns in porcine cumulus cells during meiotic maturation

被引:3
作者
Gao, Ming [1 ]
Wang, Hengjie [2 ]
Chen, Minjian [3 ]
Zhu, Shuai [2 ]
He, Yongfu
Wang, Qiang [2 ]
Gu, Ling [1 ]
机构
[1] Nanjing Agr Univ, Coll Anim Sci & Technol, 1 Weigang, Nanjing 210095, Jiangsu, Peoples R China
[2] Nanjing Med Univ, Changzhou Matern & Child Hlth Care Hosp, Changzhou Med Ctr, State Key Lab Reprod Med & Offspring Hlth, Nanjing, Peoples R China
[3] Nanjing Med Univ, Sch Publ Hlth, Key Lab Modern Toxicol, Minist Educ, Nanjing, Peoples R China
基金
中国国家自然科学基金;
关键词
Cumulus cells; Energy metabolism; Metabolomics; Reproduction; ARGININE SUPPLEMENTATION; OOCYTE; RESUMPTION; ACID; PROGESTERONE; POLYAMINES; ADENOSINE; ARREST;
D O I
10.1016/j.theriogenology.2024.03.002
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Metabolic coupling between oocytes and the surrounding somatic cells allows for normal two-way communication, and their interactions is necessary for generating developmentally competent eggs. However, the metabolic framework that support oocyte maturation in surrounding cumulus cells is still lacking. Herin, we established a temporal metabolome profile of porcine cumulus cells at three key stages during oocyte maturation, illustrating the picture of global metabolic network in cumulus cells. Importantly, we discovered the novel metabolic signature in cumulus cells during meiotic maturation, in specific, significant consumption of fatty acids, elevated activity of hexosamine biosynthetic pathway (HBP), and enhanced polyamine biosynthesis. Meanwhile, we observed the different utilization of tryptophan, active biosynthesis of progesterone, and progressive decrease in purine and pyrimidine metabolism as the oocytes progress through meiosis. Collectively, our metabolomic data serves an entree to elaborate on the dynamic changes in these metabolic pathways, which not only reveals the metabolic networks controlling oocyte development, but also lays a foundation for the discovery of biomarkers in the improvement in porcine oocyte culture system.
引用
收藏
页码:56 / 69
页数:14
相关论文
共 55 条
[1]   Stearoyl-CoA desaturase activity in bovine cumulus cells protects the oocyte against saturated fatty acid stress [J].
Aardema, Hilde ;
van Tol, Helena T. A. ;
Wubbolts, Richard W. ;
Brouwers, Jos F. H. M. ;
Gadella, Bart M. ;
Roelen, Bernard A. J. .
BIOLOGY OF REPRODUCTION, 2017, 96 (05) :982-992
[2]   Oleic Acid Prevents Detrimental Effects of Saturated Fatty Acids on Bovine Oocyte Developmental Competence [J].
Aardema, Hilde ;
Vos, Peter L. A. M. ;
Lolicato, Francesca ;
Roelen, Bernard A. J. ;
Knijn, Hiemke M. ;
Vaandrager, Arie B. ;
Helms, J. Bernd ;
Gadella, Bart M. .
BIOLOGY OF REPRODUCTION, 2011, 85 (01) :62-69
[3]   NAD+ Repletion Rescues Female Fertility during Reproductive Aging [J].
Bertoldo, Michael J. ;
Listijono, Dave R. ;
Ho, Wing-Hong Jonathan ;
Riepsamen, Angelique H. ;
Goss, Dale M. ;
Richani, Dulama ;
Jin, Xing L. ;
Mahbub, Saabah ;
Campbell, Jared M. ;
Habibalahi, Abbas ;
Loh, Wei-Guo Nicholas ;
Youngson, Neil A. ;
Maniam, Jayanthi ;
Wong, Ashley S. A. ;
Selesniemi, Kaisa ;
Bustamante, Sonia ;
Li, Catherine ;
Zhao, Yiqing ;
Marinova, Maria B. ;
Kim, Lynn-Jee ;
Lau, Laurin ;
Wu, Rachael M. ;
Mikolaizak, A. Stefanie ;
Araki, Toshiyuki ;
Le Couteur, David G. ;
Turner, Nigel ;
Morris, Margaret J. ;
Walters, Kirsty A. ;
Goldys, Ewa ;
O'Neill, Christopher ;
Gilchrist, Robert B. ;
Sinclair, David A. ;
Homer, Hayden A. ;
Wu, Lindsay E. .
CELL REPORTS, 2020, 30 (06) :1670-+
[4]   Tribbles expression in cumulus cells is related to oocyte maturation and fatty acid metabolism [J].
Brisard, Daphne ;
Chesnel, Franck ;
Elis, Sebastien ;
Desmarchais, Alice ;
Sanchez-Lazo, Laura ;
Chasles, Manon ;
Maillard, Virginie ;
Uzbekova, Svetlana .
JOURNAL OF OVARIAN RESEARCH, 2014, 7
[5]  
Cameron WD, 2016, NAT METHODS, V13, P352, DOI [10.1038/NMETH.3764, 10.1038/nmeth.3764]
[6]   Metabolic disorder of amino acids, fatty acids and purines reflects the decreases in oocyte quality and potential in sows [J].
Chen, Meixia ;
Zhang, Bo ;
Cai, Shuang ;
Zeng, Xiangfang ;
Ye, Qianhong ;
Mao, Xiangbing ;
Zhang, Shihai ;
Zeng, Xiangzhou ;
Ye, Changchuan ;
Qiao, Shiyan .
JOURNAL OF PROTEOMICS, 2019, 200 :134-143
[7]   Role of cyclic nucleotide signaling in oocyte maturation [J].
Conti, M ;
Andersen, CB ;
Richard, F ;
Mehats, C ;
Chun, SY ;
Horner, K ;
Jin, C ;
Tsafriri, A .
MOLECULAR AND CELLULAR ENDOCRINOLOGY, 2002, 187 (1-2) :153-159
[8]   Bisphenol S Impaired In Vitro Ovine Early Developmental Oocyte Competence [J].
Desmarchais, Alice ;
Teteau, Ophelie ;
Papillier, Pascal ;
Jaubert, Manon ;
Druart, Xavier ;
Binet, Aurelien ;
Maillard, Virginie ;
Elis, Sebastien .
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 2020, 21 (04)
[9]   MAINTENANCE OF MURINE OOCYTE MEIOTIC ARREST - UPTAKE AND METABOLISM OF HYPOXANTHINE AND ADENOSINE BY CUMULUS CELL-ENCLOSED AND DENUDED OOCYTES [J].
DOWNS, SM ;
COLEMAN, DL ;
EPPIG, JJ .
DEVELOPMENTAL BIOLOGY, 1986, 117 (01) :174-183
[10]   Integration of parallel metabolomics and transcriptomics reveals metabolic patterns in porcine oocytes during maturation [J].
Gao, Ming ;
Chen, Minjian ;
Chen, Qiuzhen ;
Zhu, Shuai ;
Wang, Hengjie ;
Yang, Weizheng ;
Wang, Xi ;
Wang, Qiang ;
Gu, Ling .
FRONTIERS IN ENDOCRINOLOGY, 2023, 14