Multi-Omics Reveals the Role of Arachidonic Acid Metabolism in the Gut-Follicle Axis for the Antral Follicular Development of Holstein Cows

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 Sep 14

PMID 39273467

Authors

Yajun Guo

Shiwei Wang

Xuan Wu

Rong Zhao

Siyu Chang

Chen Ma

Shuang Song

Shenming Zeng

Affiliations

Soon will be listed here.

Abstract

In vitro embryonic technology is crucial for improving farm animal reproduction but is hampered by the poor quality of oocytes and insufficient development potential. This study investigated the relationships among changes in the gut microbiota and metabolism, serum features, and the follicular fluid metabolome atlas. Correlation network maps were constructed to reveal how the metabolites affect follicular development by regulating gene expression in granulosa cells. The superovulation synchronization results showed that the number of follicle diameters from 4 to 8 mm, qualified oocyte number, cleavage, and blastocyst rates were improved in the dairy heifers (DH) compared with the non-lactating multiparous dairy cows (NDC) groups. The gut microbiota was decreased in , , and , but increased in , , , , and in the NDC group, which was highly associated with phospholipid-related metabolites of gut microbiota and serum. Metabolomic profiling of the gut microbiota, serum, and follicular fluid further demonstrated that the co-metabolites were phosphocholine and linoleic acid. Moreover, the expression of genes related to arachidonic acid metabolism in granulosa cells was significantly correlated with phosphocholine and linoleic acid. The results in granulosa cells showed that the levels of PLCB1 and COX2, participating in arachidonic acid metabolism, were increased in the DH group, which improved the concentrations of PGD and PGF in the follicular fluid. Finally, the expression levels of apoptosis-related proteins, cytokines, and steroidogenesis-related genes in granulosa cells and the concentrations of steroid hormones in follicular fluid were determinants of follicular development. According to our results, gut microbiota-related phosphocholine and linoleic acid participate in arachidonic acid metabolism in granulosa cells through the gut-follicle axis, which regulates follicular development. These findings hold promise for enhancing follicular development and optimizing oocyte quality in subfertile dairy cows.

Citing Articles

Multi-omics insights into the energy compensation of rumen microbiota of grazing yaks in cold season.

Bai J, Tang L, Bi Y, Li M Front Microbiol. 2024; 15:1467841.

PMID: 39444681 PMC: 11496799. DOI: 10.3389/fmicb.2024.1467841.

References

Turnbaugh P, Ley R, Mahowald M, Magrini V, Mardis E, Gordon J . An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444(7122):1027-31. DOI: 10.1038/nature05414. View

Ribeiro E, Gomes G, Greco L, Cerri R, Vieira-Neto A, Monteiro Jr P . Carryover effect of postpartum inflammatory diseases on developmental biology and fertility in lactating dairy cows. J Dairy Sci. 2016; 99(3):2201-2220. DOI: 10.3168/jds.2015-10337. View

Zhang T, Sun P, Geng Q, Fan H, Gong Y, Hu Y . Disrupted spermatogenesis in a metabolic syndrome model: the role of vitamin A metabolism in the gut-testis axis. Gut. 2021; 71(1):78-87. PMC: 8666830. DOI: 10.1136/gutjnl-2020-323347. View

Martin-Vazquez E, Cobo-Vuilleumier N, Lopez-Noriega L, Lorenzo P, Gauthier B . The PTGS2/COX2-PGE signaling cascade in inflammation: Pro or anti? A case study with type 1 diabetes mellitus. Int J Biol Sci. 2023; 19(13):4157-4165. PMC: 10496497. DOI: 10.7150/ijbs.86492. View

Gabor G, Kastelic J, Abonyi-Toth Z, Gabor P, Endrodi T, Balogh O . Pregnancy Loss in Dairy Cattle: Relationship of Ultrasound, Blood Pregnancy-Specific Protein B, Progesterone and Production Variables. Reprod Domest Anim. 2016; 51(4):467-73. DOI: 10.1111/rda.12703. View

Guo Y, Qi Y, Yang X, Zhao L, Wen S, Liu Y . Association between Polycystic Ovary Syndrome and Gut Microbiota. PLoS One. 2016; 11(4):e0153196. PMC: 4836746. DOI: 10.1371/journal.pone.0153196. View

Sirard M, Richard F, Blondin P, Robert C . Contribution of the oocyte to embryo quality. Theriogenology. 2005; 65(1):126-36. DOI: 10.1016/j.theriogenology.2005.09.020. View

Sangsritavong S, Combs D, Sartori R, Armentano L, Wiltbank M . High feed intake increases liver blood flow and metabolism of progesterone and estradiol-17beta in dairy cattle. J Dairy Sci. 2002; 85(11):2831-42. DOI: 10.3168/jds.S0022-0302(02)74370-1. View

Li L, Zhu S, Shu W, Guo Y, Guan Y, Zeng J . Characterization of Metabolic Patterns in Mouse Oocytes during Meiotic Maturation. Mol Cell. 2020; 80(3):525-540.e9. PMC: 8034554. DOI: 10.1016/j.molcel.2020.09.022. View

10.

Burns D, Jimenez-Krassel F, Ireland J, Knight P, Ireland J . Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations. Biol Reprod. 2005; 73(1):54-62. DOI: 10.1095/biolreprod.104.036277. View

11.

Boruszewska D, Kowalczyk-Zieba I, Suwik K, Staszkiewicz-Chodor J, Jaworska J, Lukaszuk K . Prostaglandin E affects in vitro maturation of bovine oocytes. Reprod Biol Endocrinol. 2020; 18(1):40. PMC: 7216604. DOI: 10.1186/s12958-020-00598-9. View

12.

. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486(7402):207-14. PMC: 3564958. DOI: 10.1038/nature11234. View

13.

Hansen P . Implications of Assisted Reproductive Technologies for Pregnancy Outcomes in Mammals. Annu Rev Anim Biosci. 2020; 8:395-413. DOI: 10.1146/annurev-animal-021419-084010. View

14.

Kriebs A . IL-22 links gut microbiota to PCOS. Nat Rev Endocrinol. 2019; 15(10):565. DOI: 10.1038/s41574-019-0255-x. View

15.

Zhang T, Gao H, Fan Y, Chen S, Li Y, Liu R . Gut microbiota disorder induces liver dysfunction in polycystic ovary syndrome rats' model by regulating metabolite rosmarinic acid. Life Sci. 2023; 330:121912. DOI: 10.1016/j.lfs.2023.121912. View

16.

Pacella-Ince L, Zander-Fox D, Lane M . Mitochondrial SIRT5 is present in follicular cells and is altered by reduced ovarian reserve and advanced maternal age. Reprod Fertil Dev. 2013; 26(8):1072-83. DOI: 10.1071/RD13178. View

17.

Qi X, Yun C, Pang Y, Qiao J . The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes. 2021; 13(1):1-21. PMC: 7971312. DOI: 10.1080/19490976.2021.1894070. View

18.

Weigel K . Prospects for improving reproductive performance through genetic selection. Anim Reprod Sci. 2006; 96(3-4):323-30. DOI: 10.1016/j.anireprosci.2006.08.010. View

19.

Sommer F, Backhed F . The gut microbiota--masters of host development and physiology. Nat Rev Microbiol. 2013; 11(4):227-38. DOI: 10.1038/nrmicro2974. View

20.

Park J, Lee C, Jang J, Ghim J, Kim Y, You S . Phospholipase signalling networks in cancer. Nat Rev Cancer. 2012; 12(11):782-92. DOI: 10.1038/nrc3379. View