Spatiotemporal profiling of the bovine oviduct fluid proteome around the time of ovulation.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 03 2022
09 03 2022
Historique:
received:
15
10
2021
accepted:
24
02
2022
entrez:
10
3
2022
pubmed:
11
3
2022
medline:
27
4
2022
Statut:
epublish
Résumé
Understanding the composition of the oviduct fluid (OF) is crucial to better comprehend the microenvironment in which sperm capacitation, fertilization and early embryo development take place. Therefore, our aim was to determine the spatiotemporal changes in the OF proteome according to the anatomical region of the oviduct (ampulla vs. isthmus), the proximity of the ovulating ovary (ipsilateral vs. contralateral side) and the peri-ovulatory stage (pre-ovulatory or Pre-ov vs. post-ovulatory or Post-ov). Oviducts from adult cyclic cows were collected at a local slaughterhouse and pools of OF were analyzed by nanoLC-MS/MS and label-free protein quantification (n = 32 OF pools for all region × stage × side conditions). A total of 3760 proteins were identified in the OF, of which 65% were predicted to be potentially secreted. The oviduct region was the major source of variation in protein abundance, followed by the proximity of the ovulating ovary and finally the peri-ovulatory stage. Differentially abundant proteins between regions, stages and sides were involved in a broad variety of biological functions, including protein binding, response to stress, cell-to-cell adhesion, calcium homeostasis and the immune system. This work highlights the dynamic regulation of oviduct secretions and provides new protein candidates for interactions between the maternal environment, the gametes and the early embryo.
Identifiants
pubmed: 35264682
doi: 10.1038/s41598-022-07929-3
pii: 10.1038/s41598-022-07929-3
pmc: PMC8907256
doi:
Substances chimiques
Proteome
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4135Informations de copyright
© 2022. The Author(s).
Références
Suarez, S. S. Mammalian sperm interactions with the female reproductive tract. Cell Tissue Res 363, 185–194 (2016).
pubmed: 26183721
doi: 10.1007/s00441-015-2244-2
Mahé, C. et al. Sperm migration, selection, survival, and fertilizing ability in the mammalian oviduct. Biol. Reprod. 105, 317–331 (2021).
pubmed: 34057175
pmcid: 8335357
doi: 10.1093/biolre/ioab105
Ded, L., Hwang, J. Y., Miki, K., Shi, H. F. & Chung, J.-J. 3D in situ imaging of the female reproductive tract reveals molecular signatures of fertilizing spermatozoa in mice. Elife 9, e62043 (2020).
pubmed: 33078708
pmcid: 7707823
doi: 10.7554/eLife.62043
Coy, P., García-Vázquez, F. A., Visconti, P. E. & Avilés, M. Roles of the oviduct in mammalian fertilization. Reproduction 144, 649–660 (2012).
pubmed: 23028122
pmcid: 4022750
doi: 10.1530/REP-12-0279
Li, S. & Winuthayanon, W. Oviduct: Roles in fertilization and early embryo development. J. Endocrinol. 232, R1–R26 (2017).
pubmed: 27875265
doi: 10.1530/JOE-16-0302
Saint-Dizier, M., Schoen, J., Chen, S., Banliat, C. & Mermillod, P. Composing the early embryonic microenvironment: Physiology and regulation of oviductal secretions. Int. J. Mol. Sci. 21, 223 (2020).
doi: 10.3390/ijms21010223
Lamy, J. et al. Steroid hormones in bovine oviductal fluid during the estrous cycle. Theriogenology 86, 1409–1420 (2016).
pubmed: 27262884
doi: 10.1016/j.theriogenology.2016.04.086
Lamy, J. et al. Metabolomic profiling of bovine oviductal fluid across the oestrous cycle using proton nuclear magnetic resonance spectroscopy. Reprod. Fertil. Dev. 30, 1021 (2018).
pubmed: 29301092
doi: 10.1071/RD17389
Lamy, J. et al. Regulation of the bovine oviductal fluid proteome. Reproduction 152, 629–644 (2016).
pubmed: 27601716
doi: 10.1530/REP-16-0397
Saint-Dizier, M., Sandra, O., Ployart, S., Chebrout, M. & Constant, F. Expression of nuclear progesterone receptor and progesterone receptor membrane components 1 and 2 in the oviduct of cyclic and pregnant cows during the post-ovulation period. Reprod. Biol. Endocrinol. 10, 76 (2012).
pubmed: 22958265
pmcid: 3447726
doi: 10.1186/1477-7827-10-76
Cerny, K. L., Garrett, E., Walton, A. J., Anderson, L. H. & Bridges, P. J. A transcriptomal analysis of bovine oviductal epithelial cells collected during the follicular phase versus the luteal phase of the estrous cycle. Reprod. Biol. Endocrinol. 13, 84 (2015).
pubmed: 26242217
pmcid: 4524109
doi: 10.1186/s12958-015-0077-1
Gonella-Diaza, A. M. et al. Size of the ovulatory follicle dictates spatial differences in the oviductal transcriptome in cattle. PLoS ONE 10, e0145321 (2015).
pubmed: 26699362
pmcid: 4689418
doi: 10.1371/journal.pone.0145321
Maillo, V. et al. Spatial differences in gene expression in the bovine oviduct. Reproduction 152, 37–46 (2016).
pubmed: 27069007
doi: 10.1530/REP-16-0074
Rodríguez-Alonso, B. et al. Spatial and pregnancy-related changes in the protein, amino acid, and carbohydrate composition of bovine oviduct fluid. IJMS 21, 1681 (2020).
pmcid: 7084926
doi: 10.3390/ijms21051681
Franchi, A., Moreno-Irusta, A., Domínguez, E. M., Adre, A. J. & Giojalas, L. C. Extracellular vesicles from oviductal isthmus and ampulla stimulate the induced acrosome reaction and signaling events associated with capacitation in bovine spermatozoa. J. Cell Biochem. 121, 2877–2888 (2020).
pubmed: 31692037
doi: 10.1002/jcb.29522
Kumaresan, A., Ansari, M. R. & Garg, A. Modulation of post-thaw sperm functions with oviductal proteins in buffaloes. Anim. Reprod. Sci. 90, 73–84 (2005).
pubmed: 15950408
doi: 10.1016/j.anireprosci.2005.01.009
Lopera-Vasquez, R. et al. Effect of bovine oviductal fluid on development and quality of bovine embryos produced in vitro. Reprod. Fertil. Dev. 29, 621 (2017).
pubmed: 26462440
doi: 10.1071/RD15238
Dashti, S., Zare Shahneh, A., Kohram, H., Zhandi, M. & Dadashpour Davachi, N. Differential influence of ovine oviduct ampullary and isthmic derived epithelial cells on in vitro early embryo development and kinetic. Small Ruminant Res. 136, 197–201 (2016).
doi: 10.1016/j.smallrumres.2016.02.007
Almiñana, C. et al. Oviduct extracellular vesicles protein content and their role during oviduct–embryo cross-talk. Reproduction 154, 253–268 (2017).
doi: 10.1530/REP-17-0054
Ferraz, M. D. A. M. M., Carothers, A., Dahal, R., Noonan, M. J. & Songsasen, N. Oviductal extracellular vesicles interact with the spermatozoon’s head and mid-piece and improves its motility and fertilizing ability in the domestic cat. Sci. Rep. 9, 9484 (2019).
pubmed: 31263184
pmcid: 6603010
doi: 10.1038/s41598-019-45857-x
Laezer, I. et al. Dynamic profile of EVs in porcine oviductal fluid during the periovulatory period. Reproduction 159, 371–382 (2020).
pubmed: 31990667
doi: 10.1530/REP-19-0219
Zhou, Y. et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun. 10, 1523 (2019).
pubmed: 30944313
pmcid: 6447622
doi: 10.1038/s41467-019-09234-6
Leese, H. J. et al. Female reproductive tract fluids: Composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod. Fertil. Dev. 20, 1 (2008).
pubmed: 18154692
doi: 10.1071/RD07153
Roblero, L., Biggers, J. D. & Lechene, C. P. Electron probe analysis of the elemental microenvironment of oviducal mouse embryos. Reproduction 46, 431–434 (1976).
doi: 10.1530/jrf.0.0460431
Borland, R. M., Hazra, S., Biggers, J. D. & Lechene, C. P. The elemental composition of the environments of the gametes and preimplantation embryo during the initiation of pregnancy. Biol. Reprod. 16, 147–157 (1977).
pubmed: 831844
doi: 10.1095/biolreprod16.2.147
Kavanaugh, J. F. & Killian, G. J. Bovine oviductal cannulations. J. Investig. Surg. 1, 201–208 (1988).
doi: 10.3109/08941938809141106
Gerena, R. L. & Killian, G. J. Electrophoretic characterization of proteins in oviduct fluid of cows during the estrous cycle. J. Exp. Zool. 256, 113–120 (1990).
pubmed: 2401882
doi: 10.1002/jez.1402560114
Hugentobler, S. A. et al. Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Mol. Reprod. Dev. 74, 445–454 (2007).
pubmed: 16998855
doi: 10.1002/mrd.20607
Tay, J. I. et al. Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum. Reprod. 12, 2451–2456 (1997).
pubmed: 9436683
doi: 10.1093/humrep/12.11.2451
Leese, H. J. & Gray, S. M. Vascular perfusion: A novel means of studying oviduct function. Am. J. Physiol. Endocrinol. Metab. 248, E624–E632 (1985).
doi: 10.1152/ajpendo.1985.248.5.E624
Elhassan, Y. M. et al. Amino acid concentrations in fluids from the bovine oviduct and uterus and in ksom-based culture media. Theriogenology 55, 1907–1918 (2001).
pubmed: 11414495
doi: 10.1016/S0093-691X(01)00532-5
Banliat, C. et al. Identification of 56 proteins involved in embryo-maternal interactions in the bovine oviduct. Int. J. Mol. Sci. 21, 466 (2020).
pmcid: 7013689
doi: 10.3390/ijms21020466
Papp, S. M. et al. A novel approach to study the bovine oviductal fluid proteome using transvaginal endoscopy. Theriogenology 132, 53–61 (2019).
pubmed: 30991169
doi: 10.1016/j.theriogenology.2019.04.009
Pillai, V. V., Weber, D. M., Phinney, B. S. & Selvaraj, V. Profiling of proteins secreted in the bovine oviduct reveals diverse functions of this luminal microenvironment. PLoS ONE 12, e0188105 (2017).
pubmed: 29155854
pmcid: 5695823
doi: 10.1371/journal.pone.0188105
Gegenfurtner, K. et al. Influence of metabolic status and genetic merit for fertility on proteomic composition of bovine oviduct fluid. Biol. Reprod. 101, 893–905 (2019).
pubmed: 31347661
doi: 10.1093/biolre/ioz142
Fernández-Hernández, P. et al. The proteome of equine oviductal fluid varies before and after ovulation: A comparative study. Front. Vet. Sci. 8, 694247 (2021).
pubmed: 34422946
pmcid: 8375304
doi: 10.3389/fvets.2021.694247
Soleilhavoup, C. et al. Proteomes of the female genital tract during the oestrous cycle. Mol. Cell Proteomics 15, 93–108 (2016).
pubmed: 26518761
doi: 10.1074/mcp.M115.052332
Ghosh, A., Syed, S. M. & Tanwar, P. S. In vivo genetic cell lineage tracing reveals that oviductal secretory cells self-renew and give rise to ciliated cells. Development 144, 3031–3041 (2017).
pubmed: 28743800
Ito, S., Kobayashi, Y., Yamamoto, Y., Kimura, K. & Okuda, K. Remodeling of bovine oviductal epithelium by mitosis of secretory cells. Cell Tissue Res. 366, 403–410 (2016).
pubmed: 27256395
doi: 10.1007/s00441-016-2432-8
Popa, S. J., Stewart, S. E. & Moreau, K. Unconventional secretion of annexins and galectins. Semin. Cell Dev. Biol. 83, 42–50 (2018).
pubmed: 29501720
pmcid: 6565930
doi: 10.1016/j.semcdb.2018.02.022
Yu, H. et al. Identification of rabbit oviductal fluid proteins involved in pre-fertilization processes by quantitative proteomics. Proteomics 19, 1800319 (2019).
doi: 10.1002/pmic.201800319
Gutiérrez, H. A., Latorre, R., MartÍnez BagÁn, E., Sánchez Margallo, F. M. & López Albors, O. Quantitative evaluation of the vasculature supplying the oviduct in pre-pubertal and sexually mature sows: Quantitative evaluation of the vasculature. Anat. Rec. 298, 1978–1983 (2015).
doi: 10.1002/ar.23269
Buhi, W. C., Ashworth, C. J., Bazer, F. W. & Alvarez, I. M. In vitro synthesis of oviductal secretory proteins by estrogen-treated ovariectomized gilts. J. Exp. Zool. 262, 426–435 (1992).
pubmed: 1624914
doi: 10.1002/jez.1402620409
Holt, W. V. & Fazeli, A. Sperm storage in the female reproductive tract. Annu. Rev. Anim. Biosci. 4, 291–310 (2016).
pubmed: 26526545
doi: 10.1146/annurev-animal-021815-111350
Lamy, J. et al. Identification by proteomics of oviductal sperm-interacting proteins. Reproduction 155, 457–466 (2018).
pubmed: 29540510
doi: 10.1530/REP-17-0712
Wong, C.-W. et al. The roles of protein disulphide isomerase family A, member 3 (ERp57) and surface thiol/disulphide exchange in human spermatozoa–zona pellucida binding. Hum. Reprod. 32, 733–742 (2017).
pubmed: 28175305
doi: 10.1093/humrep/dex007
Marín-Briggiler, C. I. et al. Glucose-regulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm–zona pellucida binding. Fertil. Steril. 93, 1574–1584 (2010).
pubmed: 19296942
doi: 10.1016/j.fertnstert.2008.12.132
Mondéjar, I., Martínez-Martínez, I., Avilés, M. & Coy, P. Identification of potential oviductal factors responsible for zona pellucida hardening and monospermy during fertilization in mammals. Biol. Reprod. 89, 67–1 (2013).
doi: 10.1095/biolreprod.113.111385
Lachance, C., Bailey, J. L. & Leclerc, P. Expression of Hsp60 and Grp78 in the human endometrium and oviduct, and their effect on sperm functions. Hum. Reprod. 22, 2606–2614 (2007).
pubmed: 17670764
doi: 10.1093/humrep/dem242
Tokuhiro, K. et al. Calreticulin is required for development of the cumulus oocyte complex and female fertility. Sci. Rep. 5, 14254 (2015).
pubmed: 26388295
pmcid: 4585710
doi: 10.1038/srep14254
Saavedra, M. D. et al. Calreticulin from suboolemmal vesicles affects membrane regulation of polyspermy. Reproduction 147, 369–378 (2014).
pubmed: 24398873
doi: 10.1530/REP-13-0454
Bernecic, N. C., Gadella, B. M., Leahy, T. & de Graaf, S. P. Novel methods to detect capacitation-related changes in spermatozoa. Theriogenology 137, 56–66 (2019).
pubmed: 31230703
doi: 10.1016/j.theriogenology.2019.05.038
Kotwica, G. et al. The concentrations of catecholamines and oxytocin receptors in the oviduct and its contractile activity in cows during the estrous cycle. Theriogenology 60, 953–964 (2003).
pubmed: 12935872
doi: 10.1016/S0093-691X(03)00086-4
Coy, P. et al. Hardening of the zona pellucida of unfertilized eggs can reduce polyspermic fertilization in the pig and cow. Reproduction 135, 19–27 (2008).
pubmed: 18159080
doi: 10.1530/REP-07-0280
Algarra, B. et al. The C-terminal region of OVGP1 remodels the zona pellucida and modifies fertility parameters. Sci. Rep. 6, 1–12 (2016).
doi: 10.1038/srep32556
Yang, X., Zhao, Y., Yang, X. & Kan, F. W. K. Recombinant hamster oviductin is biologically active and exerts positive effects on sperm functions and sperm-oocyte binding. PLoS ONE 10, e0123003 (2015).
pubmed: 25849110
pmcid: 4388664
doi: 10.1371/journal.pone.0123003
Zhao, Y. & Kan, F. W. K. Human OVGP1 enhances tyrosine phosphorylation of proteins in the fibrous sheath involving AKAP3 and increases sperm-zona binding. J. Assist. Reprod. Genet. 36, 1363–1377 (2019).
pubmed: 31254143
pmcid: 6642236
doi: 10.1007/s10815-019-01502-0
Choudhary, S. et al. Effect of recombinant and native buffalo OVGP1 on sperm functions and in vitro embryo development: A comparative study. J. Anim. Sci. Biotechnol. 8, 1–12 (2017).
doi: 10.1186/s40104-017-0201-5
Sakaue, T. et al. Factor H in porcine seminal plasma protects sperm against complement attack in genital tracts. J. Biol. Chem. 285, 2184–2192 (2010).
pubmed: 19920146
doi: 10.1074/jbc.M109.063495
Lee, K.-F. et al. Phospholipid transfer protein (PLTP) mRNA expression is stimulated by developing embryos in the oviduct. J. Cell. Biochem. 95, 740–749 (2005).
pubmed: 15832314
doi: 10.1002/jcb.20444
Smits, K. et al. Proteome of equine oviducal fluid: effects of ovulation and pregnancy. Reprod. Fertil. Dev. 29, 1085 (2017).
pubmed: 27120206
doi: 10.1071/RD15481
Locatelli, Y. et al. Relative effects of location relative to the corpus luteum and lactation on the transcriptome of the bovine oviduct epithelium. BMC Genomics 20, 233 (2019).
pubmed: 30898106
pmcid: 6427878
doi: 10.1186/s12864-019-5616-2
Sostaric, E. et al. Sperm binding properties and secretory activity of the bovine oviduct immediately before and after ovulation. Mol. Reprod. Dev. 75, 60–74 (2008).
pubmed: 17546595
doi: 10.1002/mrd.20766
Wijayagunawardane, M. P. et al. Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow. Theriogenology 49, 607–618 (1998).
pubmed: 10732039
doi: 10.1016/S0093-691X(98)00011-9
Kölle, S. et al. Ciliary transport, gamete interaction, and effects of the early embryo in the oviduct: Ex vivo analyses using a new digital videomicroscopic system in the cow. Biol. Reprod. 81, 267–274 (2009).
pubmed: 19299315
doi: 10.1095/biolreprod.108.073874
Lee, S. H., Oh, H. J., Kim, M. J. & Lee, B. C. Exosomes derived from oviduct cells mediate the EGFR/MAPK signaling pathway in cumulus cells. J. Cell Physiol. 235, 1386–1404 (2020).
pubmed: 31338842
doi: 10.1002/jcp.29058
Acosta-Martínez, M. PI3K: An attractive candidate for the central integration of metabolism and reproduction. Front. Endocrinol. 2, 110 (2012).
doi: 10.3389/fendo.2011.00110
Álvarez-Rodríguez, M., Martinez, C. A., Wright, D. & Rodríguez-Martinez, H. The role of semen and seminal plasma in inducing large-scale genomic changes in the female porcine peri-ovulatory tract. Sci. Rep. 10, 5061 (2020).
pubmed: 32193402
pmcid: 7081221
doi: 10.1038/s41598-020-60810-z
Bauersachs, S. et al. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. J. Mol. Endocrinol. 32, 449–466 (2004).
pubmed: 15072551
doi: 10.1677/jme.0.0320449
Ireland, J. J., Murphee, R. L. & Coulson, P. B. Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J. Dairy Sci. 63, 155–160 (1980).
pubmed: 7372895
doi: 10.3168/jds.S0022-0302(80)82901-8
Adib, A. et al. Progesterone improves the maturation of male-induced preovulatory follicles in anoestrous ewes. Reproduction 148, 403–416 (2014).
pubmed: 25062803
doi: 10.1530/REP-14-0263
Rico, C. et al. Regulation of anti-müllerian hormone production in the cow: A multiscale study at endocrine, ovarian, follicular, and granulosa cell levels1. Biol. Reprod. 84, 560–571 (2011).
pubmed: 21076084
doi: 10.1095/biolreprod.110.088187
Keller, A., Nesvizhskii, A. I., Kolker, E. & Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383–5392 (2002).
pubmed: 12403597
doi: 10.1021/ac025747h
Nesvizhskii, A. I., Keller, A., Kolker, E. & Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646–4658 (2003).
pubmed: 14632076
doi: 10.1021/ac0341261