Identification of small extracellular vesicle subtypes in follicular fluid: Insights into the function and miRNA profiles.
follicular fluid
microRNA
small extracellular vesicles
subtype
Journal
Journal of cellular physiology
ISSN: 1097-4652
Titre abrégé: J Cell Physiol
Pays: United States
ID NLM: 0050222
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
02
12
2020
received:
02
11
2020
accepted:
18
12
2020
pubmed:
13
2
2021
medline:
21
10
2021
entrez:
12
2
2021
Statut:
ppublish
Résumé
The study of small extracellular vesicles (sEVs) heterogeneity is one of the main problems that must be solved, and the different sEV subtypes in follicular fluid are still unclear, limiting our understanding of their function. This study first separated sEV subtypes from follicular fluid using differential ultracentrifugation combined with iodixanol density gradient flotation and then evaluated their miRNA profile and effects on the proliferation and apoptosis of granulosa cells (GCs). We also performed Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis of potential target genes of differentially expressed miRNAs (DEMs) and KEGG analysis of potential target genes of non-DEMs. Low-density sEVs (sEV_F6) were enriched in TSG101, while high-density sEVs (sEV_F8) were enriched in CD63. The miRNA profiles of sEV_F6 and sEV_F8 were heterogeneous, and the differential signaling pathways were mainly related to the adhesion and hypoxic stress pathways, while the same signaling pathways were mainly related to cell proliferation, apoptosis, cell cycle, and autophagy pathways. In addition, the highly expressed miRNAs in both subtypes were mainly related to cell proliferation and apoptosis. Both subtypes transferred their miRNAs into GCs and promoted the proliferation ability of the GCs and inhibited their apoptosis. The results showed for the first time that there are different subtypes of sEVs in follicular fluid and that the miRNA profiles of subtypes are heterogeneous.
Substances chimiques
MicroRNAs
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5633-5645Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Böing, A. N., van der Pol, E., Grootemaat, A. E., Coumans, F. A., Sturk, A., & Nieuwland, R. (2014). Single-step isolation of extracellular vesicles by size-exclusion chromatography. Journal of Extracellular Vesicles, 3, 3. https://doi.org/10.3402/jev.v3.23430
Bobrie, A., Colombo, M., Krumeich, S., Raposo, G., & Théry, C. (2012). Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. Journal of Extracellular Vesicles, 1, 1. https://doi.org/10.3402/jev.v1i0.18397
Cheruvanky, A., Zhou, H., Pisitkun, T., Kopp, J. B., Knepper, M. A., Yuen, P. S., & Star, R. A. (2007). Rapid isolation of urinary exosomal biomarkers using a nanomembrane ultrafiltration concentrator. American Journal of Physiology. Renal Physiology, 292(5), F1657-1661. https://doi.org/10.1152/ajprenal.00434.2006
da Silveira, J. C., Carnevale, E. M., Winger, Q. A., & Bouma, G. J. (2014). Regulation of ACVR1 and ID2 by cell-secreted exosomes during follicle maturation in the mare. Reproductive Biology and Endocrinology, 12, 44. https://doi.org/10.1186/1477-7827-12-44
da Silveira, J. C., Veeramachaneni, D. N., Winger, Q. A., Carnevale, E. M., & 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. Biology of Reproduction, 86(3), 71. https://doi.org/10.1095/biolreprod.111.093252
Giacomini, E., Makieva, S., Murdica, V., Vago, R., & Viganó, P. (2020). Extracellular vesicles as a potential diagnostic tool in assisted reproduction. Current Opinion in Obstetrics and Gynecology, 32(3), 179-184. https://doi.org/10.1097/gco.0000000000000621
Gurunathan, S., Kang, M. H., Jeyaraj, M., Qasim, M., & Kim, J. H. (2019). Review of the isolation, characterization, biological function, and multifarious therapeutic approaches of exosomes. Cells, 8(4), 307. https://doi.org/10.3390/cells8040307
Hung, W. T., Hong, X., Christenson, L. K., & McGinnis, L. K. (2015). Extracellular vesicles from bovine follicular fluid support cumulus expansion. Biology of Reproduction, 93(5), 117. https://doi.org/10.1095/biolreprod.115.132977
Hung, W. T., Navakanitworakul, R., Khan, T., Zhang, P., Davis, J. S., McGinnis, L. K., & Christenson, L. K. (2017). Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation. Biology of Reproduction, 97(4), 644-655. https://doi.org/10.1093/biolre/iox106
Jaśkiewicz, A., Pająk, B., & Orzechowski, A. (2018). The many faces of Rap1 GTPase. International Journal of Molecular Sciences, 19(10), 2848. https://doi.org/10.3390/ijms19102848
Jeppesen, D. K., Fenix, A. M., Franklin, J. L., Higginbotham, J. N., Zhang, Q., Zimmerman, L. J., Liebler, D. C., Ping, J., Liu, Q., Evans, R., Fissell, W. H., Patton, J. G., Rome, L. H., Burnette, D. T., & Coffey, R. J. (2019). Reassessment of exosome composition. Cell, 177(2), 428-445 e418. https://doi.org/10.1016/j.cell.2019.02.029
Kanada, M., Bachmann, M. H., Hardy, J. W., Frimannson, D. O., Bronsart, L., Wang, A., Sylvester, M. D., Schmidt, T. L., Kaspar, R. L., Butte, M. J., Matin, A. C., & Contag, C. H. (2015). Differential fates of biomolecules delivered to target cells via extracellular vesicles. Proceedings of the National Academy of Sciences of the United States of America, 112(12), E1433-1442. https://doi.org/10.1073/pnas.1418401112
Kowal, J., Arras, G., Colombo, M., Jouve, M., Morath, J. P., Primdal-Bengtson, B., Dingli, F., Loew, D., Tkach, M., & Théry, C. (2016). Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proceedings of the National Academy of Sciences of the United States of America, 113(8), E968-977. https://doi.org/10.1073/pnas.1521230113
Lötvall, J., Hill, A. F., Hochberg, F., Buzás, E. I., Di Vizio, D., Gardiner, C., Gho, Y. S., Kurochkin, I. V., Mathivanan, S., Quesenberry, P., Sahoo, S., Tahara, H., Wauben, M. H., Witwer, K. W., & Théry, C. (2014). Minimal experimental requirements for definition of extracellular vesicles and their functions: A position statement from the International Society for Extracellular Vesicles. Journal of Extracellular Vesicles, 3, 26913. https://doi.org/10.3402/jev.v3.26913
Lake, D., Corrêa, S. A., & Müller, J. (2016). Negative feedback regulation of the ERK1/2 MAPK pathway. Cellular and Molecular Life Science, 73(23), 4397-4413. https://doi.org/10.1007/s00018-016-2297-8
Lee, K., Shao, H., Weissleder, R., & Lee, H. (2015). Acoustic purification of extracellular microvesicles. ACS Nano, 9(3), 2321-2327. https://doi.org/10.1021/nn506538f
Lee, Y., El Andaloussi, S., & Wood, M. J. (2012). Exosomes and microvesicles: Extracellular vesicles for genetic information transfer and gene therapy. Human Molecular Genetics, 21(R1), R125-134. https://doi.org/10.1093/hmg/dds317
Li, K., Wong, D. K., Hong, K. Y., & Raffai, R. L. (2018). Cushioned-Density Gradient Ultracentrifugation (C-DGUC): A refined and high performance method for the isolation, characterization, and use of exosomes. Methods in Molecular Biology, 1740, 69-83. https://doi.org/10.1007/978-1-4939-7652-2_7
Li, P., Kaslan, M., Lee, S. H., Yao, J., & Gao, Z. (2017). Progress in exosome isolation techniques. Theranostics, 7(3), 789-804. https://doi.org/10.7150/thno.18133
Lin, F., Li, R., Pan, Z., Zhou, B., Yu, D., Wang, X., Ma, X., Han, J., Shen, M., & Liu, H. (2012). miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary. PLOS One, 7(6), e38640. https://doi.org/10.1371/journal.pone.0038640
Liu, J., Yao, W., Yao, Y., Du, X., Zhou, J., Ma, B., Liu, H., Li, Q., & Pan, Z. (2014). MiR-92a inhibits porcine ovarian granulosa cell apoptosis by targeting Smad7 gene. FEBS Letters, 588(23), 4497-4503. https://doi.org/10.1016/j.febslet.2014.10.021
Liu, Z., Gan, L., Zhang, T., Ren, Q., & Sun, C. (2018). Melatonin alleviates adipose inflammation through elevating α-ketoglutarate and diverting adipose-derived exosomes to macrophages in mice. Journal of Pineal Research, 64(1), e12455. https://doi.org/10.1111/jpi.12455
Lobb, R. J., Becker, M., Wen, S. W., Wong, C. S., Wiegmans, A. P., Leimgruber, A., & Möller, A. (2015). Optimized exosome isolation protocol for cell culture supernatant and human plasma. Journal of Extracellular Vesicles, 4, 27031. https://doi.org/10.3402/jev.v4.27031
Maalouf, S. W., Liu, W. S., & Pate, J. L. (2016). MicroRNA in ovarian function. Cell and Tissue Research, 363(1), 7-18. https://doi.org/10.1007/s00441-015-2307-4
Martins, R., Lithgow, G. J., & Link, W. (2016). Long live FOXO: Unraveling the role of FOXO proteins in aging and longevity. Aging cell, 15(2), 196-207. https://doi.org/10.1111/acel.12427
Matsuno, Y., Onuma, A., Fujioka, Y. A., Yasuhara, K., Fujii, W., Naito, K., & Sugiura, K. (2017). Effects of exosome-like vesicles on cumulus expansion in pigs in vitro. Journal of Reproduction and Development, 63(1), 51-58. https://doi.org/10.1262/jrd.2016-124
Mihaylova, M. M., & Shaw, R. J. (2011). The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nature Cell Biology, 13(9), 1016-1023. https://doi.org/10.1038/ncb2329
Miranda, K. C., Bond, D. T., Levin, J. Z., Adiconis, X., Sivachenko, A., Russ, C., Brown, D., Nusbaum, C., & Russo, L. M. (2014). Massively parallel sequencing of human urinary exosome/microvesicle RNA reveals a predominance of non-coding RNA. PLOS One, 9(5), e96094. https://doi.org/10.1371/journal.pone.0096094
Navakanitworakul, R., Hung, W. T., Gunewardena, S., Davis, J. S., Chotigeat, W., & Christenson, L. K. (2016). Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles. Scientific Reports, 6, 25486. https://doi.org/10.1038/srep25486
Sanchez-Soria, P., & Camenisch, T. D. (2010). ErbB signaling in cardiac development and disease. Seminars in Cell and Developmental Biology, 21(9), 929-935. https://doi.org/10.1016/j.semcdb.2010.09.011
Sedlik, C., Vigneron, J., Torrieri-Dramard, L., Pitoiset, F., Denizeau, J., Chesneau, C., de la Rochere, P., Lantz, O., Thery, C., & Bellier, B. (2014). Different immunogenicity but similar antitumor efficacy of two DNA vaccines coding for an antigen secreted in different membrane vesicle-associated forms. Journal of Extracellular Vesicles, 3, 3. https://doi.org/10.3402/jev.v3.24646
Semenza, G. L. (2001). HIF-1 and mechanisms of hypoxia sensing. Current Opinion in Cell Biology, 13(2), 167-171. https://doi.org/10.1016/s0955-0674(00)00194-0
Sen, A., Prizant, H., Light, A., Biswas, A., Hayes, E., Lee, H. J., Barad, D., Gleicher, N., & Hammes, S. R. (2014). Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proceedings of the National Academy of Sciences of the United States of America, 111(8), 3008-3013. https://doi.org/10.1073/pnas.1318978111
Shao, H., & Im, H. (2018). New technologies for analysis of extracellular vesicles. New Technologies for Analysis of Extracellular Vesicles, 118(4), 1917-1950. https://doi.org/10.1021/acs.chemrev.7b00534
Théry, C., Amigorena, S., Raposo, G., & Clayton, A. (2006). Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current Protocols in Cell Biology, Chapter 3, Unit 3, 22. https://doi.org/10.1002/0471143030.cb0322s30
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin-Smith, G. K., Ayre, D. C., Bach, J. M., Bachurski, D., Baharvand, H., Balaj, L., Baldacchino, S., Bauer, N. N., Baxter, A. A., Bebawy, M., … Jovanovic-Talisman, T. (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. Journal of Extracellular Vesicles, 7(1), 1535750. https://doi.org/10.1080/20013078.2018.1535750
Tkach, M., Kowal, J., Zucchetti, A. E., Enserink, L., Jouve, M., Lankar, D., Saitakis, M., Martin-Jaular, L., & Théry, C. (2017). Qualitative differences in T-cell activation by dendritic cell-derived extracellular vesicle subtypes. EMBO Journal, 36(20), 3012-3028. https://doi.org/10.15252/embj.201696003
Vagner, T., Spinelli, C., Minciacchi, V. R., Balaj, L., Zandian, M., Conley, A., Zijlstra, A., Freeman, M. R., Demichelis, F., De, S., Posadas, E. M., Tanaka, H., & Di Vizio, D. (2018). Large extracellular vesicles carry most of the tumour DNA circulating in prostate cancer patient plasma. Journal of Extracellular Vesicles, 7(1), 1505403. https://doi.org/10.1080/20013078.2018.1505403
Wang, Q., & Lu, Q. (2017). Plasma membrane-derived extracellular microvesicles mediate non-canonical intercellular NOTCH signaling. Nature Communications, 8(1), 709. https://doi.org/10.1038/s41467-017-00767-2
Wang, X., Meng, K., He, Y., Wang, H., Zhang, Y., & Quan, F. (2019). Melatonin stimulates STAR expression and progesterone production via activation of the PI3K/AKT pathway in bovine theca cells. International Journal of Biological Sciences, 15(2), 404-415. https://doi.org/10.7150/ijbs.27912
Willms, E., Cabañas, C., Mäger, I., Wood, M. J. A., & Vader, P. (2018). Extracellular vesicle heterogeneity: Subpopulations, isolation techniques, and diverse functions in cancer progression. Frontiers in Immunology, 9, 738. https://doi.org/10.3389/fimmu.2018.00738
Zarovni, N., Corrado, A., Guazzi, P., Zocco, D., Lari, E., Radano, G., Muhhina, J., Fondelli, C., Gavrilova, J., & Chiesi, A. (2015). Integrated isolation and quantitative analysis of exosome shuttled proteins and nucleic acids using immunocapture approaches. Methods, 87, 46-58. https://doi.org/10.1016/j.ymeth.2015.05.028
Zeringer, E., Barta, T., Li, M., & Vlassov, A. V. (2015). Strategies for isolation of exosomes. Cold Spring Harb Protocols, 2015(4), 319-323. https://doi.org/10.1101/pdb.top074476