Characterization of bovine uterine fluid extracellular vesicles proteomic profiles at follicular and luteal phases of the oestrous cycle
Tóm tắt
Extracellular vesicles (EV) have been identified in uterine fluid (UF), however the bovine UF-EV profile during different phases of the oestrous cycle has not yet been established. Therefore, we compared the UF-EV, and their protein profile at follicular and luteal phases of the oestrous cycle. UF samples were collected from healthy uteri of six live and six slaughtered cows at follicular or luteal phases. Isolation of EV was performed using tangential flow filtration followed by size exclusion chromatography. EV were characterized by nanoparticle tracking analysis (NTA), fluorescence NTA, zeta potential, and transmission electron microscopy. Mass-spectrometry was used to evaluate EV protein profile from live cows. Particle concentrations (mean ± SD) were higher (P < 0.05) at follicular than at luteal phase in both live (1.01 × 108 ± 1.66 × 107 vs 7.56 × 107 ± 1.80 × 107, respectively) and slaughtered cows (1.17 × 108 ± 2.34 × 107 vs 9.12 × 107 ± 9.77 × 106, respectively). The proportion of fluorescently labelled EV varied significantly between follicular and luteal phases across live (28.9 ± 1.9% vs 19.3 ± 2.8%, respectively) and slaughtered cows (26.5 ± 6.3% vs 27.3 ± 2 .7%, respectively). In total, 41 EV proteins were differentially expressed between the phases. Some of the proteins were involved in reproductive processes, cell adhesion and proliferation, and cellular metabolic processes. The results indicated differences in bovine UF-EV concentration and protein profile at follicular and luteal phases, which would suggest that EV modulate uterine microenvironment across the oestrous cycle. Further research is needed to understand the effect of EV changes throughout the oestrous cycle.
Tài liệu tham khảo
Akagi T, Ichiki T (2008) Cell electrophoresis on a chip: what can we know from the changes in electrophoretic mobility? Anal Bioanal Chem 391(7):2433–2441. https://doi.org/10.1007/s00216-008-2203-9
Andrade GM, Bridi A, Gimenes LU et al (2019) Extracellular vesicles and its advances infemale reproduction. Anim Reprod 16(1):31–38. https://doi.org/10.21451/1984-3143-AR2018-0101
Arosh JA, Parent J, Chapdelaine P et al (2002) Expression of cyclooxygenases 1 and 2 and prostaglandin E synthase in bovine endometrial tissue during the estrous cycle. Bio Reprod 67(1):161–169. https://doi.org/10.1095/biolreprod67.1.161
Bridi A, Perecin F, Silveira JCD (2020) Extracellular vesicles mediated early embryo-maternal interactions. Int J Mol Sci 21(3):1163. https://doi.org/10.3390/ijms21031163
Burns G, Brooks K, Wildung M et al (2014) Extracellular vesicles in luminal fluid of the ovine uterus. PLoS ONE 9(3):e90913. https://doi.org/10.1371/journal.pone.0090913
Burns GW, Brooks KE, Spencer TE (2016) Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. Biol Reprod 94(3):56. https://doi.org/10.1095/biolreprod.115.134973
Burns GW, Brooks KE, O’Neil EV et al (2018) Progesterone effects on extracellular vesicles in the sheep uterus. Biol Reprod 98(5):612–622. https://doi.org/10.1093/biolre/ioy011
Caballero J, Frenette G, Sullivan R (2010) Post testicular sperm maturational changes in the bull: important role of the epididymosomes and prostasomes. Vet Med Int 2011:757194. https://doi.org/10.4061/2011/757194
Chae JI, Kim J, Lee SG et al (2011) Proteomic analysis of pregnancy-related proteins from pig uterus endometrium during pregnancy. Proteome Sci 9(41). https://doi.org/10.1186/1477-5956-9-4
Chatuphonprasert W, Jarukamjorn K, Ellinger I (2018) Physiology and pathophysiology of steroid biosynthesis, transport and metabolism in the human placenta. Front Pharmacol 9:1027. https://doi.org/10.3389/fphar.2018.01027
Cortes VA, Busso D, Maiz A et al (2014) Physiological and pathological implications of cholesterol. Front Biosci (landmark Ed) 19(3):416–428. https://doi.org/10.2741/4216
DesCôteaux L, Gnemmi G, Colloton J (2009) Ultrasonography of the bovine female genital tract. Vet Clin North Am Food Anim Pract 25(3):733–52, Table of Contents. https://doi.org/10.1016/j.cvfa.2009.07.009
Dissanayake K, Midekessa G, Lättekivi F, Fazeli A (2021a) Measurement of the Size and concentration and zeta potential of extracellular vesicles using nanoparticle tracking analyzer. Methods Mol Biol 2273:207–218. https://doi.org/10.1007/978-1-0716-1246-0_15
Dissanayake K, Nõmm M, Lättekivi F et al (2021b) Oviduct as a sensor of embryo quality: deciphering the extracellular vesicle (EV)-mediated embryo-maternal dialogue. J Mol Med (berl) 99(5):685–697. https://doi.org/10.1007/s00109-021-02042-w
Es-Haghi M, Godakumara K, Häling A et al (2019) Specific trophoblast transcripts transferred by extracellular vesicles affect gene expression in endometrial epithelial cells and may have a role in embryo-maternal crosstalk. Cell Commun Signal 17(1):146. https://doi.org/10.1186/s12964-019-0448-x
ExoCarta: List of top 100 proteins that are often identified in exosomes. http://exocarta.org/exosome_markers_new. Accessed 3 Feb 2022
Faulkner S, Elia G, O’Boyle P et al (2013) Composition of the bovine uterine proteome is associated with stage of cycle and concentration of systemic progesterone. Proteomics 13(22):3333–53. https://doi.org/10.1002/pmic.201300204
Forde N, Beltman ME, Lonergan P et al (2011) Oestrous cycles in Bos taurus cattle. Anim Reprod Sci 124(3–4):163–169. https://doi.org/10.1016/j.anireprosci.2010.08.025
Fröhlich E (2012) The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomed 7:5577–5591. https://doi.org/10.2147/IJN.S36111
Giacomini E, Scotti GM, Vanni VS et al (2021) Global transcriptomic changes occur in uterine fluid-derived extracellular vesicles during the endometrial window for embryo implantation. Hum Reprod 36(8):2249–2274. https://doi.org/10.1093/humrep/deab123
Hamdi M, Cañon-Beltrán K, Mazzarella R et al (2021) Characterization and profiling analysis of bovine oviduct and uterine extracellular vesicles and their miRNA cargo through the estrous cycle. FASEB J 35(12):e22000. https://doi.org/10.1096/fj.202101023R
Hartjes TA, Mytnyk S, Jenster GW et al (2019) Extracellular vesicle quantification and characterization: common methods and emerging approaches. Bioengineering (Basel) 6(1):7. https://doi.org/10.3390/bioengineering6010007
Hasan MM, Reshi QUA, Lättekivi F et al (2021) Bovine follicular fluid derived extracellular vesicles modulate the viability, capacitation and acrosome reaction of bull spermatozoa. Biology (Basel) 10(11):1154. https://doi.org/10.3390/biology10111154
Herrero C, de la Fuente A, Casas-Arozamena C et al (2019) Extracellular vesicles-based biomarkers represent a promising liquid biopsy in endometrial cancer. Cancers (Basel) 11(12):2000. https://doi.org/10.3390/cancers11122000
Huang DW, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37(1):1–13. https://doi.org/10.1093/nar/gkn923
Huang DW, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc 4(1):44–57. https://doi.org/10.1038/nprot.2008.211
Just J, Yan Y, Farup J et al (2020) Blood flow-restricted resistance exercise alters the surface profile, miRNA cargo and functional impact of circulating extracellular vesicles. Sci Rep 10:5835. https://doi.org/10.1038/s41598-020-62456-3
Kusama K, Nakamura K, Bai R et al (2018) Intrauterine exosomes are required for bovine conceptus implantation. Biochem Biophys Res Commun 495(1):1370–1375. https://doi.org/10.1016/j.bbrc.2017.11.176
Lange-Consiglio A, Lazzari B, Pizzi F et al (2020) Amniotic microvesicles impact hatching and pregnancy percentages of in vitro bovine embryos and blastocyst microRNA expression versus in vivo controls. Sci Rep 10(1):501. https://doi.org/10.1038/s41598-019-57060-z
Liu C, Yao W, Yao J, Li L et al (2020) Endometrial extracellular vesicles from women with recurrent implantation failure attenuate the growth and invasion of embryos. Fertil Steril 114(2):416–425. https://doi.org/10.1016/j.fertnstert.2020.04.005
Marcu IC, Eberhard N, Yerly A et al (2020) Isolation of human small extracellular vesicles and tracking of their uptake by retinal pigment epithelial cells in vitro. Int J Mol Sci 21(11):3799. https://doi.org/10.3390/ijms21113799
Martins T, Pugliesi G, Sponchiado M et al (2018) Perturbations in the uterine luminal fluid composition are detrimental to pregnancy establishment in cattle. J Anim Sci Biotechnol 9:70. https://doi.org/10.1186/s40104-018-0285-6
Méndez-Tepepa M, Zepeda-Pérez D, Nicolás-Toledo L et al (2020) Inferring lanosterol functions in the female rabbit reproductive tract based on the immunolocalization of lanosterol 14-demethylase and farnesoid beta-receptor. Acta Histochem 122(2):151472. https://doi.org/10.1016/j.acthis.2019.151472
Midekessa G, Godakumara K, Dissanayake K et al (2021) Characterization of extracellular vesicles labelled with a lipophilic dye using fluorescence nanoparticle tracking analysis. Membranes (Basel) 11(10):779. https://doi.org/10.3390/membranes11100779
Nakamura K, Kusama K, Ideta A et al (2019) Effects of miR-98 in intrauterine extracellular vesicles on maternal immune regulation during the peri-implantation period in cattle. Sci Rep 9:20330. https://doi.org/10.1038/s41598-019-56879-w
O’Neil EV, Spencer TE (2021) Insights into the lipidome and primary metabolome of the uterus from day 14 cyclic and pregnant sheep. Bio Reprod 105(1):87–99. https://doi.org/10.1093/biolre/ioab053
Perez-Riverol Y, Bai J, Bandla C, Hewapathirana S et al (2022) The PRIDE database resources in 2022: A Hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res 50(D1):D543–D552
Pioltine EM, Machado MF, da Silveira JC et al (2020) Can extracellular vesicles from bovine ovarian follicular fluid modulate the in-vitro oocyte meiosis progression similarly to the CNP-NPR2 system? Theriogenology 157:210–217. https://doi.org/10.1016/j.theriogenology.2020.06.031
Rai A, Poh QH, Fatmous M et al (2021) Proteomic profiling of human uterine extracellular vesicles reveal dynamic regulation of key players of embryo implantation and fertility during menstrual cycle. Proteomics 21(13–14):e2000211. https://doi.org/10.1002/pmic.202000211
Reese ST, Franco GA, Poole RK et al (2020) Pregnancy loss in beef cattle: A meta-analysis. Anim Reprod Sci 212:106251. https://doi.org/10.1016/j.anireprosci.2019.106251
Reshi QUA, Hasan MM, Dissanayake K, Fazeli A (2021) Isolation of extracellular vesicles (EVs) using benchtop size exclusion chromatography (SEC) columns. Methods Mol Biol 2273:201–206. https://doi.org/10.1007/978-1-0716-1246-0_14
Ruiz-González I, Xu J, Wang X et al (2015) Exosomes, endogenous retroviruses and toll-like receptors: pregnancy recognition in ewes. Reproduction 149(3):281–291. https://doi.org/10.1530/REP-14-0538
Sato N, Kawamura K, Fukuda J et al (2003) Expression of LDL receptor and uptake of LDL in mouse preimplantation embryos. Mol Cell Endocrinol 202(1–2):191–194. https://doi.org/10.1016/s0303-7207(03)00082-0
Schobers G, Koeck R, Pellaers D et al (2021) Liquid biopsy: state of reproductive medicine and beyond. Hum Reprod 36(11):2824–2839. https://doi.org/10.1093/humrep/deab206
Seli E, Babayev E, Collins SC et al (2014) Minireview: Metabolism of female reproduction: regulatory mechanisms and clinical implications. Mol Endocrinol 28(6):790–804. https://doi.org/10.1210/me.2013-1413
Shehu A, Mao J, Gibori GB et al (2008) Prolactin receptor-associated protein/17beta-hydroxysteroid dehydrogenase type 7 gene (Hsd17b7) plays a crucial role in embryonic development and fetal survival. Mol Endocrinol 22(10):2268–2277. https://doi.org/10.1210/me.2008-0165
Shpacovitch V, Hergenröder R (2018) Optical and surface plasmonic approaches to characterize extracellular vesicles. A Review Anal Chim Acta 1005:1–15. https://doi.org/10.1016/j.aca.2017.11.066
Simintiras CA, Forde N (2017) Understanding the uterine environment in early pregnancy in cattle: How have the omics enhanced our knowledge? Anim Reprod 14(3):583–646. https://doi.org/10.21451/1984-3143-AR997
Simintiras CA, Sánchez JM, McDonald M, Lonergan P (2019) The biochemistry surrounding bovine conceptus elongation†. Biol Reprod 101(2):328–337. https://doi.org/10.1093/biolre/ioz101
Simon C, Greening DW, Bolumar D et al (2018) Extracellular vesicles in human reproduction in health and disease. Endocr Rev 39(3):292–332. https://doi.org/10.1210/er.2017-00229
Spencer TE (2014) Biological roles of uterine glands in pregnancy. Semin Reprod Med 32(5):346–357. https://doi.org/10.1055/s-0034-1376354
Sponchiado M, Gomes NS, Fontes PK et al (2017) Pre-hatching embryo-dependent and -independent programming of endometrial function in cattle. PLoS ONE 12(4):e0175954. https://doi.org/10.1371/journal.pone.0175954
Su YQ, Sugiura K, Eppig JJ (2009) Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 27(1):32–42. https://doi.org/10.1055/s-0028-1108008
Sullivan R, Saez F, Girouard J, Frenette G (2005) Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis 35(1):1–10. https://doi.org/10.1016/j.bcmd.2005.03.005
Tannetta D, Dragovic R, Alyahyaei Z, Southcombe J (2014) Extracellular vesicles and reproduction-promotion of successful pregnancy. Cell Mol Immunol 11(6):548–563. https://doi.org/10.1038/cmi.2014.42
Tavares Pereira M, Papa P, Reichler IM et al (2022) Luteal expression of factors involved in the metabolism and sensitivity to oestrogens in the dog during pregnancy and in non-pregnant cycle. Reprod Domest Anim 57(1):86–97. https://doi.org/10.1111/rda.14032
Théry C, Witwer KW, Aikawa E et al (2018) Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 7(1):1535750. https://doi.org/10.1080/20013078.2018.1535750
Tóth EÁ, Turiák L, Visnovitz T et al (2021) Formation of a protein corona on the surface of extracellular vesicles in blood plasma. J Extracell Vesicles 10(11):e12140. https://doi.org/10.1002/jev2.12140
Valdmann M, Kurykin J, Kaart T et al (2018) Relationships between plasma insulin-like growth factor-1 and insulin concentrations in multiparous dairy cows with cytological endometritis. Vet Rec 183(4):126. https://doi.org/10.1136/vr.104640
Vilella F, Moreno-Moya JM, Balaguer N et al (2015) Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome. Development 142(18):3210–3221. https://doi.org/10.1242/dev.124289
Waldmann A, Raud A (2016) Comparison of a lateral flow milk progesterone test with enzyme immunoassay as an aid for reproductive status determination in cows. Vet Rec 178(11):260. https://doi.org/10.1136/vr.103605
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. ISBN 978–3–319–24277–4. https://ggplot2.tidyverse.org
Wu T, Hu E, Xu M et al (2021) clusterProfiler, 4.0: A universal enrichment tool for interpreting omics data. Innovation (N Y) 2(3):100141. https://doi.org/10.1016/j.xinn.2021.100141
Zhang X, Smits A, van Tilburg G et al (2018) Proteome-wide identification of ubiquitin interactions using UbIA-MS. Nat Protoc 13:530–550. https://doi.org/10.1038/nprot.2017.147