Extracellular Vesicles from Follicular and Ampullary Fluid Isolated by Density Gradient Ultracentrifugation Improve Bovine Embryo Development and Quality

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2021 Jan 12

PMID 33430094

Citations 23

Authors

Anise Asaadi

Nima Azari Dolatabad

Hadi Atashi

Annelies Raes

Petra Van Damme

Michael Hoelker

An Hendrix

Osvaldo Bogado Pascottini

Ann Van Soom

Mojtaba Kafi

Krishna Chaitanya Pavani

Affiliations

Soon will be listed here.

Abstract

Extracellular vesicles (EVs) have been isolated from follicular (FF) and ampullary oviduct fluid (AOF), using different isolation methods. However, it is not clear whether different purification methods can affect the functionality of resulting EVs. Here, we compared two methods (OptiPrep™ density gradient ultracentrifugation (ODG UC) and single-step size exclusion chromatography (SEC) (qEV IZON™ single column)) for the isolation of EVs from bovine FF and AOF. Additionally, we evaluated whether the addition of EVs derived either by ODG UC or SEC from FF or AOF during oocyte maturation would yield extra benefits for embryo developmental competence. The characterization of EVs isolated using ODG UC or SEC from FF and AOF did not show any differences in terms of EV sizes (40-400 nm) and concentrations (2.4 ± 0.2 × 10-1.8 ± 0.2 × 10 particles/mL). Blastocyst yield and quality was higher in groups supplemented with EVs isolated from FF and AOF by ODG UC, with higher total cell numbers and a lower apoptotic cell ratio compared with the other groups ( < 0.05). Supplementing in vitro maturation media with EVs derived by ODG UC from AOF was beneficial for bovine embryo development and quality.

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References

Hailay T, Hoelker M, Poirier M, Gebremedhn S, Rings F, Saeed-Zidane M . Extracellular vesicle-coupled miRNA profiles in follicular fluid of cows with divergent post-calving metabolic status. Sci Rep. 2019; 9(1):12851. PMC: 6731312. DOI: 10.1038/s41598-019-49029-9. View

Mol E, Goumans M, Doevendans P, Sluijter J, Vader P . Higher functionality of extracellular vesicles isolated using size-exclusion chromatography compared to ultracentrifugation. Nanomedicine. 2017; 13(6):2061-2065. DOI: 10.1016/j.nano.2017.03.011. View

Wydooghe E, Vandaele L, Beek J, Favoreel H, Heindryckx B, De Sutter P . Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining. Anal Biochem. 2011; 416(2):228-30. DOI: 10.1016/j.ab.2011.05.033. View

Boing A, van der Pol E, Grootemaat A, Coumans F, Sturk A, Nieuwland R . Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2014; 3. PMC: 4159761. DOI: 10.3402/jev.v3.23430. View

Davachi N, Kohram H, Shahneh A, Zhandi M, Goudarzi A, Fallahi R . The effect of conspecific ampulla oviductal epithelial cells during in vitro maturation on oocyte developmental competence and maturation-promoting factor (MPF) activity in sheep. Theriogenology. 2017; 88:207-214. DOI: 10.1016/j.theriogenology.2016.09.034. View

Lopera-Vasquez R, Hamdi M, Maillo V, Gutierrez-Adan A, Bermejo-Alvarez P, Ramirez M . Effect of bovine oviductal extracellular vesicles on embryo development and quality . Reproduction. 2017; 153(4):461-470. DOI: 10.1530/REP-16-0384. View

Pavani K, Hendrix A, Van Den Broeck W, Couck L, Szymanska K, Lin X . Isolation and Characterization of Functionally Active Extracellular Vesicles from Culture Medium Conditioned by Bovine Embryos In Vitro. Int J Mol Sci. 2018; 20(1). PMC: 6337605. DOI: 10.3390/ijms20010038. View

Rizos D, Clemente M, Bermejo-Alvarez P, de la Fuente J, Lonergan P, Gutierrez-Adan A . Consequences of in vitro culture conditions on embryo development and quality. Reprod Domest Anim. 2008; 43 Suppl 4:44-50. DOI: 10.1111/j.1439-0531.2008.01230.x. View

Kowal J, Arras G, Colombo M, Jouve M, Morath J, Primdal-Bengtson B . Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016; 113(8):E968-77. PMC: 4776515. DOI: 10.1073/pnas.1521230113. View

10.

Davachi N, Shahneh A, Kohram H, Zhandi M, Shamsi H, Hajiyavand A . Differential influence of ampullary and isthmic derived epithelial cells on zona pellucida hardening and in vitro fertilization in ovine. Reprod Biol. 2016; 16(1):61-9. DOI: 10.1016/j.repbio.2015.11.002. View

11.

Silveira J, Andrade G, Del Collado M, Sampaio R, Sangalli J, Silva L . Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development. PLoS One. 2017; 12(6):e0179451. PMC: 5472319. DOI: 10.1371/journal.pone.0179451. View

12.

Wydooghe E, Heras S, Dewulf J, Piepers S, Van den Abbeel E, De Sutter P . Replacing serum in culture medium with albumin and insulin, transferrin and selenium is the key to successful bovine embryo development in individual culture. Reprod Fertil Dev. 2013; 26(5):717-24. DOI: 10.1071/RD13043. View

13.

Rodgers R, Irving-Rodgers H . Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod. 2010; 82(6):1021-9. DOI: 10.1095/biolreprod.109.082941. View

14.

Van Deun J, Mestdagh P, Sormunen R, Cocquyt V, Vermaelen K, Vandesompele J . The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014; 3. PMC: 4169610. DOI: 10.3402/jev.v3.24858. View

15.

Lonergan P, Fair T . In vitro-produced bovine embryos: dealing with the warts. Theriogenology. 2007; 69(1):17-22. DOI: 10.1016/j.theriogenology.2007.09.007. View

16.

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

17.

Takov K, Yellon D, Davidson S . Comparison of small extracellular vesicles isolated from plasma by ultracentrifugation or size-exclusion chromatography: yield, purity and functional potential. J Extracell Vesicles. 2019; 8(1):1560809. PMC: 6327926. DOI: 10.1080/20013078.2018.1560809. View

18.

Silveira J, Veeramachaneni D, Winger Q, Carnevale E, Bouma G . Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol Reprod. 2011; 86(3):71. DOI: 10.1095/biolreprod.111.093252. View

19.

Matzuk M, Burns K, Viveiros M, Eppig J . Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002; 296(5576):2178-80. DOI: 10.1126/science.1071965. View

20.

Lamy J, Liere P, Pianos A, Aprahamian F, Mermillod P, Saint-Dizier M . Steroid hormones in bovine oviductal fluid during the estrous cycle. Theriogenology. 2016; 86(6):1409-1420. DOI: 10.1016/j.theriogenology.2016.04.086. View