Comprehensive Proteomics Analysis of In Vitro Canine Oviductal Cell-Derived Extracellular Vesicles

Overview

Journal Animals (Basel)

Date 2021 Mar 6

PMID 33672125

Citations 5

Authors

Seok Hee Lee

Saul Lira-Albarran

Islam M Saadeldin

Affiliations

Soon will be listed here.

Abstract

Dogs (Canis lupus familiaris) have unique and peculiar reproductive characteristics. While the interplay between in vitro oviductal cell-derived extracellular vesicles (OC-EVs) and cumulus-oocyte complexes in dogs has begun to be elucidated, no study has yet provided extensive information on the biological content and physiological function of OC-EVs and their role in canine oocyte development. Here, we aimed to provide the first comprehensive proteomic analysis of OC-EVs. We identified 398 proteins as present in all OC-EVs samples. The functional enrichment analysis using Gene Ontology terms and an Ingenuity Pathway Analysis revealed that the identified proteins were involved in several cellular metabolic processes, including translation, synthesis, expression, and protein metabolism. Notably, the proteins were also involved in critical canonical pathways with essential functions in oocyte and embryo development, such as ERK/MAPK, EIF2, PI3K/AKT, and mTOR signaling. These data would be an important resource for studying canine reproductive physiology and establishing a successful in vitro embryo production system in dogs.

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References

Lee S, Oh H, Kim M, Kim G, Choi Y, Jo Y . Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of co-culture with oviduct cells on in vitro maturation of oocytes. J Assist Reprod Genet. 2017; 34(7):929-938. PMC: 5476537. DOI: 10.1007/s10815-017-0910-x. View

Kurian N, Modi D . Extracellular vesicle mediated embryo-endometrial cross talk during implantation and in pregnancy. J Assist Reprod Genet. 2018; 36(2):189-198. PMC: 6420537. DOI: 10.1007/s10815-018-1343-x. View

Griffiths G, Miller K, Galileo D, Martin-DeLeon P . Murine SPAM1 is secreted by the estrous uterus and oviduct in a form that can bind to sperm during capacitation: acquisition enhances hyaluronic acid-binding ability and cumulus dispersal efficiency. Reproduction. 2008; 135(3):293-301. DOI: 10.1530/REP-07-0340. View

Yu H, Hackenbroch L, Meyer F, Reiser J, Razzazi-Fazeli E, Nobauer K . Identification of Rabbit Oviductal Fluid Proteins Involved in Pre-Fertilization Processes by Quantitative Proteomics. Proteomics. 2019; 19(5):e1800319. DOI: 10.1002/pmic.201800319. View

Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J . Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25(1):25-9. PMC: 3037419. DOI: 10.1038/75556. View

Intawicha P, Tsai L, Yen S, Lo N, Ju J . Nucleus, Cytoskeleton, and Mitogen-Activated Protein Kinase p38 Dynamics during In Vitro Maturation of Porcine Oocytes. Animals (Basel). 2019; 9(4). PMC: 6523277. DOI: 10.3390/ani9040163. View

Smits K, Nelis H, Van Steendam K, Govaere J, Roels K, Ververs C . Proteome of equine oviducal fluid: effects of ovulation and pregnancy. Reprod Fertil Dev. 2016; 29(6):1085-1095. DOI: 10.1071/RD15481. View

Pillai V, Weber D, Phinney B, Selvaraj V . Profiling of proteins secreted in the bovine oviduct reveals diverse functions of this luminal microenvironment. PLoS One. 2017; 12(11):e0188105. PMC: 5695823. DOI: 10.1371/journal.pone.0188105. View

Lee S, Oh H, Kim M, Lee B . Canine oviductal exosomes improve oocyte development via EGFR/MAPK signaling pathway. Reproduction. 2020; 160(4):613-625. DOI: 10.1530/REP-19-0600. View

10.

Kalra H, Adda C, Liem M, Ang C, Mechler A, Simpson R . Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics. 2013; 13(22):3354-64. DOI: 10.1002/pmic.201300282. View

11.

Machtinger R, Laurent L, Baccarelli A . Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum Reprod Update. 2015; 22(2):182-93. PMC: 4755440. DOI: 10.1093/humupd/dmv055. View

12.

Jansova D, Tetkova A, Koncicka M, Kubelka M, Susor A . Localization of RNA and translation in the mammalian oocyte and embryo. PLoS One. 2018; 13(3):e0192544. PMC: 5846722. DOI: 10.1371/journal.pone.0192544. View

13.

Matsuyama M, Tanaka H, Inoko A, Goto H, Yonemura S, Kobori K . Defect of mitotic vimentin phosphorylation causes microophthalmia and cataract via aneuploidy and senescence in lens epithelial cells. J Biol Chem. 2013; 288(50):35626-35. PMC: 3861614. DOI: 10.1074/jbc.M113.514737. View

14.

Bauersachs S, Mermillod P, Alminana C . The Oviductal Extracellular Vesicles' RNA Cargo Regulates the Bovine Embryonic Transcriptome. Int J Mol Sci. 2020; 21(4). PMC: 7072903. DOI: 10.3390/ijms21041303. View

15.

Tiruvayipati S, Wolfgeher D, Yue M, Duan F, Andrade J, Jiang H . Variability in protein cargo detection in technical and biological replicates of exosome-enriched extracellular vesicles. PLoS One. 2020; 15(3):e0228871. PMC: 7051218. DOI: 10.1371/journal.pone.0228871. View

16.

Alcantara-Neto A, Schmaltz L, Caldas E, Blache M, Mermillod P, Alminana C . Porcine oviductal extracellular vesicles interact with gametes and regulate sperm motility and survival. Theriogenology. 2020; 155:240-255. DOI: 10.1016/j.theriogenology.2020.05.043. View

17.

Nakano S, Yamamoto S, Okada A, Nakajima T, Sato M, Takagi T . Role of extracellular vesicles in the interaction between epithelial and mesenchymal cells during oviductal ciliogenesis. Biochem Biophys Res Commun. 2016; 483(1):245-251. DOI: 10.1016/j.bbrc.2016.12.158. View

18.

Alminana C, Bauersachs S . Extracellular Vesicles in the Oviduct: Progress, Challenges and Implications for the Reproductive Success. Bioengineering (Basel). 2019; 6(2). PMC: 6632016. DOI: 10.3390/bioengineering6020032. View

19.

Fu B, Ma H, Liu D . Extracellular Vesicles Function as Bioactive Molecular Transmitters in the Mammalian Oviduct: An Inspiration for Optimizing in Vitro Culture Systems and Improving Delivery of Exogenous Nucleic Acids during Preimplantation Embryonic Development. Int J Mol Sci. 2020; 21(6). PMC: 7139358. DOI: 10.3390/ijms21062189. View

20.

Hewitt D, Watson P, England G . Nuclear staining and culture requirements for in vitro maturation of domestic bitch oocytes. Theriogenology. 2000; 49(6):1083-101. DOI: 10.1016/s0093-691x(98)00058-2. View