Follicular fluid exosomes act on the bovine oocyte to improve oocyte competence to support development and survival to heat shock
Thais A. Rodrigues
A , Kubra M. Tuna B , Abdel A. Alli B , P. Tribulo C , P. J. Hansen C , Jin Koh D and F. F. Paula-Lopes A E
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, Federal University of São Paulo, 275 Professor Arthur Riedel Street, 09972-270, Diadema, Sao Paulo, Brazil.
B Department of Physiology and Functional Genomics, University of Florida, Gainesville, FL 32611-0910, USA.
C Department of Animal Sciences, University of Florida, Gainesville, FL 32611-0910, USA.
D Proteomics and Mass Spectrometry Laboratory, Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL 32611-0910, USA.
E Corresponding author. Email: ffpaulalopes@gmail.com
Reproduction, Fertility and Development 31(5) 888-897 https://doi.org/10.1071/RD18450
Submitted: 23 June 2018 Accepted: 5 December 2018 Published: 14 February 2019
Abstract
Addition of follicular fluid to oocyte maturation medium can affect cumulus cell function, increase competence of the oocytes to be fertilised and develop to the blastocyst stage and protect the oocyte from heat shock. Here, it was tested whether exosomes in follicular fluid are responsible for the effects of follicular fluid on the function of the cumulus–oocyte complex (COC). This was accomplished by culturing COCs during oocyte maturation at 38.5°C (body temperature of the cow) or 41°C (heat shock) with follicular fluid or exosomes derived from follicular fluid and evaluating various aspects of function of the oocyte and the embryo derived from it. Negative effects of heat shock on cleavage and blastocyst development, but not cumulus expansion, were reduced by follicular fluid and exosomes. The results support the idea that exosomes in follicular fluid play important roles during oocyte maturation to enhance oocyte function and protect it from stress.
Additional keywords: cumulus cells, electronic microscopy, embryo, oocyte maturation, proteomics.
References
Ascari, I. J., Alves, N. G., Jasmin, J., Lima, R. R., Quintão, C. C. R., Oberlender, G., Moraes, E. A., and Camargo, L. S. A. (2017). Addition of insulin-like growth factor I to the maturation medium of bovine oocytes subjected to heat shock: effects on the production of reactive oxygen species, mitochondrial activity and oocyte competence. Domest. Anim. Endocrinol. 60, 50–60.| Addition of insulin-like growth factor I to the maturation medium of bovine oocytes subjected to heat shock: effects on the production of reactive oxygen species, mitochondrial activity and oocyte competence.Crossref | GoogleScholarGoogle Scholar | 28445838PubMed |
Barraud-Lange, V., Chalas Boissonnas, C., Serres, C., Auer, J., Schmitt, A., Lefèvre, B., Wolf, J. P., and Ziyyat, A. (2012). Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of CD9-deleted oocytes. Reproduction 144, 53–66.
| Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilising ability of CD9-deleted oocytes.Crossref | GoogleScholarGoogle Scholar | 22554680PubMed |
Benammar, A., Ziyyat, A., Lefèvre, B., and Wolf, J. P. (2017). Tetraspanins and mouse oocyte microvilli related to fertilizing ability. Reprod. Sci. 24, 1062–1069.
| Tetraspanins and mouse oocyte microvilli related to fertilizing ability.Crossref | GoogleScholarGoogle Scholar | 27879451PubMed |
Bertolin, K., Meinsohn, M. C., Suzuki, J., Gossen, J., Schoonjans, K., Duggavathi, R., and Murphy, B. D. (2017). Ovary-specific depletion of the nuclear receptor Nr5a2 compromises expansion of the cumulus oophorus but not fertilization by intracytoplasmic sperm injection. Biol. Reprod. 96, 1231–1243.
| Ovary-specific depletion of the nuclear receptor Nr5a2 compromises expansion of the cumulus oophorus but not fertilization by intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 28520915PubMed |
Carper, S. W., Rocheleau, T. A., Cimino, D., and Storm, F. K. (1997). Heat shock protein 27 stimulates recovery of RNA and protein synthesis following a heat shock. J. Cell. Biochem. 66, 153–164.
| Heat shock protein 27 stimulates recovery of RNA and protein synthesis following a heat shock.Crossref | GoogleScholarGoogle Scholar | 9213217PubMed |
Choi, D. S., Kim, D. K., Kim, Y. K., and Gho, Y. S. (2013). Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 13, 1554–1571.
| Proteomics, transcriptomics and lipidomics of exosomes and ectosomes.Crossref | GoogleScholarGoogle Scholar | 23401200PubMed |
Ciavarra, R. P., Goldman, C., Wen, K. K., Tedeschi, B., and Castora, F. J. (1994). Heat stress induces hsc70/nuclear topoisomerase I complex formation in vivo: evidence for hsc70-mediated, ATP-independent reactivation in vitro. Proc. Natl. Acad. Sci. USA 91, 1751–1755.
| Heat stress induces hsc70/nuclear topoisomerase I complex formation in vivo: evidence for hsc70-mediated, ATP-independent reactivation in vitro.Crossref | GoogleScholarGoogle Scholar | 8127877PubMed |
Conde-Vancells, J., Rodriguez-Suarez, E., Embade, N., Gil, D., Matthiesen, R., Valle, M., Elortza, F., Lu, S. C., Mato, J. M., and Falcon-Perez, J. M. (2008). Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J. Proteome Res. 7, 5157–5166.
| Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes.Crossref | GoogleScholarGoogle Scholar | 19367702PubMed |
da Silveira, J. C., Veeramachaneni, D. N., Winger, Q. A., Carnevale, E. M., and Bouma, G. J. (2012). 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. 86, 71.
| Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 22116803PubMed |
da Silveira, J. C., Andrade, G. M., Del Collado, M., Sampaio, R. V., Sangalli, J. R., Silva, L. A., Pinaffi, F. V. L., Jardim, I. B., Cesar, M. C., Nogueira, M. F. G., Cesar, A. S. M., Coutinho, L. L., Pereira, R. W., Perecin, F., and Meirelles, F. V. (2017). Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development. PLoS One 12, e0179451.
| Supplementation with small-extracellular vesicles from ovarian follicular fluid during in vitro production modulates bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 28922408PubMed |
Dalenezi, F. M., and Ferreira, J. C. P. (2016). Gene expression of in vitro maturated oocytes can be modulated by follicle exosomes from cows kept under thermo-neutral or heat- stress condition. Vet. Zootech. 23, 54.
Dang, V. D., Jella, K. K., Ragheb, R. R. T., Denslow, N. D., and Alli, A. A. (2017). Lipidomic and proteomic analysis of exosomes from mouse cortical collecting duct cells. FASEB J. 31, 5399–5408.
| Lipidomic and proteomic analysis of exosomes from mouse cortical collecting duct cells.Crossref | GoogleScholarGoogle Scholar | 28821634PubMed |
de Castro e Paula, L. A., and Hansen, P. J. (2007). Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation. Theriogenology 68, 763–770.
| Interactions between oxygen tension and glucose concentration that modulate actions of heat shock on bovine oocytes during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 17643482PubMed |
de S. Torres-Júnior, J. R., de F A Pires, M., de Sá, W. F., de M Ferreira, A., Viana, J. H., Camargo, L. S., Ramos, A. A., Folhadella, I. M., Polisseni, J., de Freitas, C., Clemente, C. A., de Sá Filho, M. F., Paula-Lopes, F. F., and Baruselli, P. S. (2008). Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology 69, 155–166.
| Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle.Crossref | GoogleScholarGoogle Scholar | 17953981PubMed |
Di Pietro, C. (2016). Exosome-mediated communication in the ovarian follicle. J. Assist. Reprod. Genet. 33, 303–311.
| Exosome-mediated communication in the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 26814471PubMed |
Doerwald, L., Onnekink, C., van Genesen, S. T., de Jong, W. W., and Lubsen, N. H. (2003). Translational thermotolerance provided by small heat shock proteins is limited to cap-dependent initiation and inhibited by 2-aminopurine. J. Biol. Chem. 278, 49743–49750.
| Translational thermotolerance provided by small heat shock proteins is limited to cap-dependent initiation and inhibited by 2-aminopurine.Crossref | GoogleScholarGoogle Scholar | 14523008PubMed |
Fair, T., Hulshof, S. C., Hyttel, P., Greve, T., and Boland, M. (1997). Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat. Embryol. (Berl.) 195, 327–336.
| Oocyte ultrastructure in bovine primordial to early tertiary follicles.Crossref | GoogleScholarGoogle Scholar | 9108198PubMed |
Flamenbaum, I., and Galon, N. (2010). Management of heat stress to improve fertility in dairy cows in Israel. J. Reprod. Dev. 56, S36–S41.
| 20629215PubMed |
Fleshner, M., and Crane, C. R. (2017). Exosomes, DAMPs and miRNA: features of stress physiology and immune homeostasis. Trends Immunol. 38, 768–776.
| Exosomes, DAMPs and miRNA: features of stress physiology and immune homeostasis.Crossref | GoogleScholarGoogle Scholar | 28838855PubMed |
Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A., and Peelman, L. J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5, 27.
| Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 16324220PubMed |
Grupen, C. G., and Armstrong, D. T. (2010). Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM. Reprod. Fertil. Dev. 22, 1100–1109.
| Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM.Crossref | GoogleScholarGoogle Scholar | 20797348PubMed |
Guay, C., and Regazzi, R. (2017). Exosomes as new players in metabolic organ cross-talk. Diabetes Obes. Metab. 19, 137–146.
| Exosomes as new players in metabolic organ cross-talk.Crossref | GoogleScholarGoogle Scholar | 28880477PubMed |
Hansen, P. J. (2009). Effects of heat stress on mammalian reproduction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3341–3350.
| Effects of heat stress on mammalian reproduction.Crossref | GoogleScholarGoogle Scholar | 19833646PubMed |
Hegmans, J. P., Bard, M. P., Hemmes, A., Luider, T. M., Kleijmeer, M. J., Prins, J. B., Zitvogel, L., Burgers, S. A., Hoogsteden, H. C., and Lambrecht, B. N. (2004). Proteomic analysis of exosomes secreted by human mesothelioma cells. Am. J. Pathol. 164, 1807–1815.
| Proteomic analysis of exosomes secreted by human mesothelioma cells.Crossref | GoogleScholarGoogle Scholar | 15111327PubMed |
Hung, W. T., Hong, X., Christenson, L. K., and McGinnis, L. K. (2015). Extracellular vesicles from bovine follicular fluid support cumulus expansion. Biol. Reprod. 93, 117.
| Extracellular vesicles from bovine follicular fluid support cumulus expansion.Crossref | GoogleScholarGoogle Scholar | 26423123PubMed |
Hung, W. T., Navakanitworakul, R., Khan, T., Davis, J. S., McGinnis, L. K., and Christenson, L. K. (2017). Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation. Biol. Reprod. 97, 644–655.
| Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation.Crossref | GoogleScholarGoogle Scholar | 29025042PubMed |
Ispada, J., Rodrigues, T. A., Risolia, P. H. B., Lima, R. S., Gonçalves, D. R., Rettori, D., Nichi, M., Feitosa, W. B., and Paula-Lopes, F. F. (2018). Astaxanthin counteracts the effects of heat shock on the maturation of bovine oocytes. Reprod. Fertil. Dev. 30, 1169–1179.
| Astaxanthin counteracts the effects of heat shock on the maturation of bovine oocytes.Crossref | GoogleScholarGoogle Scholar |
Jella, K. K., Yu, L., Yue, Q., Friedman, D., Duke, B. J., and Alli, A. A. (2016). Exosomal GAPDH from proximal tubule cells regulate ENaC activity. PLoS One 11, e0165763.
| Exosomal GAPDH from proximal tubule cells regulate ENaC activity.Crossref | GoogleScholarGoogle Scholar | 27802315PubMed |
Kannampuzha-Francis, J., Tribulo, P., and Hansen, P. J. (2017). Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on the development of the bovine preimplantation embryo. Reprod. Fertil. Dev. 29, 1329–1339.
| Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on the development of the bovine preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 27185102PubMed |
LaVoie, H. A. (2017). Transcriptional control of genes mediating ovarian follicular growth, differentiation, and steroidogenesis in pigs. Mol. Reprod. Dev. 84, 788–801.
| Transcriptional control of genes mediating ovarian follicular growth, differentiation, and steroidogenesis in pigs.Crossref | GoogleScholarGoogle Scholar | 28467682PubMed |
Lima, R. S., Risolia, P. H., Ispada, J., Assumpção, M. E., Visintin, J. A., Orlandi, C., and Paula-Lopes, F. F. (2017). Role of insulin-like growth factor 1 on cross-bred Bos indicus cattle germinal vesicle oocytes exposed to heat shock. Reprod. Fertil. Dev. 29, 1405–1414.
| Role of insulin-like growth factor 1 on cross-bred Bos indicus cattle germinal vesicle oocytes exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 27619511PubMed |
Matsuno, Y., Onuma, A., Fujioka, Y. A., Yasuhara, K., Fujii, W., Naito, K., and Sugiura, K. (2017). Effects of exosome-like vesicles on cumulus expansion in pigs in vitro. J. Reprod. Dev. 63, 51–58.
| Effects of exosome-like vesicles on cumulus expansion in pigs in vitro.Crossref | GoogleScholarGoogle Scholar | 28163264PubMed |
Mehlmann, L. M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–799.
| Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 16322539PubMed |
Monniaux, D. (2016). Driving folliculogenesis by the oocyte-somatic cell dialog: lessons from genetic models. Theriogenology 86, 41–53.
| Driving folliculogenesis by the oocyte-somatic cell dialog: lessons from genetic models.Crossref | GoogleScholarGoogle Scholar | 27155734PubMed |
Mulcahy, L. A., Pink, R. C., and Carter, D. R. (2014). Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles 3, 24641.
| Routes and mechanisms of extracellular vesicle uptake.Crossref | GoogleScholarGoogle Scholar |
Nabenishi, H., Ohta, H., Nishimoto, T., Morita, T., Ashizawa, K., and Tsuzuki, Y. (2012). The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote 20, 249–259.
| The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress.Crossref | GoogleScholarGoogle Scholar | 21729376PubMed |
Navakanitworakul, R., Hung, W. T., Gunewardena, S., Davis, J. S., Chotigeat, W., and Christenson, L. K. (2016). Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles. Sci. Rep. 6, 25486.
| Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles.Crossref | GoogleScholarGoogle Scholar | 27158133PubMed |
Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646–4658.
| A statistical model for identifying proteins by tandem mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 14632076PubMed |
Ortega, M. S., Wohlgemuth, S., Tribulo, P., Siqueira, L. G., Null, D. J., Cole, J. B., Da Silva, M. V., and Hansen, P. J. (2017). A single nucleotide polymorphism in COQ9 affects mitochondrial and ovarian function and fertility in Holstein cows. Biol. Reprod. 96, 652–663.
| A single nucleotide polymorphism in COQ9 affects mitochondrial and ovarian function and fertility in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 28339599PubMed |
Ozawa, M., Sakatani, M., Hankowski, K. E., Terada, N., Dobbs, K. B., and Hansen, P. J. (2012). Importance of culture conditions during the morula-to-blastocyst period on capacity of inner cell-mass cells of bovine blastocysts for establishment of self-renewing pluripotent cells. Theriogenology 78, 1243–1251.e2.
| Importance of culture conditions during the morula-to-blastocyst period on capacity of inner cell-mass cells of bovine blastocysts for establishment of self-renewing pluripotent cells.Crossref | GoogleScholarGoogle Scholar | 22898023PubMed |
Ploutarchou, P., Melo, P., Day, A. J., Milner, C. M., and Williams, S. A. (2015). Molecular analysis of the cumulus matrix: insights from mice with O-glycan-deficient oocytes. Reproduction 149, 533–543.
| Molecular analysis of the cumulus matrix: insights from mice with O-glycan-deficient oocytes.Crossref | GoogleScholarGoogle Scholar | 25855670PubMed |
Putney, D. J., Drost, M., and Thatcher, W. W. (1988). Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination. Theriogenology 30, 195–209.
| Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between the onset of estrus and insemination.Crossref | GoogleScholarGoogle Scholar | 16726462PubMed |
Rodrigues, T. A., Orlandi, C. M. B., Gonçalves, D. R., Silva, D. F., and Paula-Lopes, F. F. (2015). Follicular fluid thermoprotective role during in vitro maturation of bovine oocytes subjected to heat shock. Anim. Reprod. 12, 776.
Rodrigues, T. A., Ispada, J., Risolia, P. H., Rodrigues, M. T., Lima, R. S., Assumpção, M. E., Visintin, J. A., and Paula-Lopes, F. F. (2016). Thermoprotective effect of insulin-like growth factor 1 on in vitro matured bovine oocyte exposed to heat shock. Theriogenology 86, 2028–2039.
| Thermoprotective effect of insulin-like growth factor 1 on in vitro matured bovine oocyte exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 27545516PubMed |
Roth, Z., and Hansen, P. J. (2004a). Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol. Reprod. 71, 1898–1906.
| Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 15306551PubMed |
Roth, Z., and Hansen, P. J. (2004b). Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation. Biol. Reprod. 71, 2072–2078.
| Sphingosine 1-phosphate protects bovine oocytes from heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 15317688PubMed |
Roth, Z., and Hansen, P. J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–244.
| Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation.Crossref | GoogleScholarGoogle Scholar | 15695618PubMed |
Russell, D. L., Gilchrist, R. B., Brown, H. M., and Thompson, J. G. (2016). Bidirectional communication between cumulus cells and the oocyte: old hands and new players? Theriogenology 86, 62–68.
| Bidirectional communication between cumulus cells and the oocyte: old hands and new players?Crossref | GoogleScholarGoogle Scholar | 27160446PubMed |
Saeed-Zidane, M., Linden, L., Salilew-Wondim, D., Held, E., Neuhoff, C., Tholen, E., Hoelker, M., Schellander, K., and Tesfaye, D. (2017). Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress. PLoS One 12, e0187569.
| Cellular and exosome mediated molecular defense mechanism in bovine granulosa cells exposed to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 29117219PubMed |
Santonocito, M., Vento, M., Guglielmino, M. R., Battaglia, R., Wahlgren, J., Ragusa, M., Barbagallo, D., Borzì, P., Rizzari, S., Maugeri, M., Scollo, P., Tatone, C., Valadi, H., Purrello, M., and Di Pietro, C. (2014). Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil. Steril. 102, 1751–1761.e1.
| Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation.Crossref | GoogleScholarGoogle Scholar | 25241362PubMed |
Shi, Y., Nishida, K., Campigli Di Giammartino, D., and Manley, J. L. (2011). Heat shock-induced SRSF10 dephosphorylation displays thermotolerance mediated by Hsp27. Mol. Cell. Biol. 31, 458–465.
| Heat shock-induced SRSF10 dephosphorylation displays thermotolerance mediated by Hsp27.Crossref | GoogleScholarGoogle Scholar | 21135127PubMed |
Sohel, M. M., Hoelker, M., Noferesti, S. S., Salilew-Wondim, D., Tholen, E., Looft, C., Rings, F., Uddin, M. J., Spencer, T. E., Schellander, K., and Tesfaye, D. (2013). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One 8, e78505.
| Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 24223816PubMed |
Somfai, T., Inaba, Y., Watanabe, S., Geshi, M., and Nagai, T. (2012). Follicular fluid supplementation during in vitro maturation promotes sperm penetration in bovine oocytes by enhancing cumulus expansion and increasing mitochondrial activity in oocytes. Reprod. Fertil. Dev. 24, 743–752.
| Follicular fluid supplementation during in vitro maturation promotes sperm penetration in bovine oocytes by enhancing cumulus expansion and increasing mitochondrial activity in oocytes.Crossref | GoogleScholarGoogle Scholar | 22697124PubMed |
Swaney, D. L., McAlister, G. C., and Coon, J. J. (2008). Decision tree-driven tandem mass spectrometry for shotgun proteomics. Nat. Methods 5, 959–964.
| Decision tree-driven tandem mass spectrometry for shotgun proteomics.Crossref | GoogleScholarGoogle Scholar | 18931669PubMed |
UniProt Consortium (2017). UniProt: the universal protein knowledgebase. Nucleic Acids Res. 45, D158–D169.
| UniProt: the universal protein knowledgebase.Crossref | GoogleScholarGoogle Scholar | 27899622PubMed |
Urbanelli, L., Magini, A., Buratta, S., Brozzi, A., Sagini, K., Polchi, A., Tancini, B., and Emiliani, C. (2013). Signaling pathways in exosomes biogenesis, secretion and fate. Genes (Basel) 4, 152–170.
| Signaling pathways in exosomes biogenesis, secretion and fate.Crossref | GoogleScholarGoogle Scholar | 24705158PubMed |
Vashisht, M., Rani, P., Sunita, , Onteru, S. K., and Singh, D. (2018). Curcumin primed exosomes reverses LPS-induced pro-inflammatory gene expression in buffalo granulosa cells. J. Cell. Biochem. 119, 1488–1500.
| Curcumin primed exosomes reverses LPS-induced pro-inflammatory gene expression in buffalo granulosa cells.Crossref | GoogleScholarGoogle Scholar | 28771796PubMed |
