Extracellular vesicles of bovine small follicular fluid promote ovarian cortical stromal cell proliferation and steroidogenesis.

Publisher: Paul Parey Scientific Publishers Country of Publication: Germany NLM ID: 9015668 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1439-0531 (Electronic) Linking ISSN: 09366768 NLM ISO Abbreviation: Reprod Domest Anim Subsets: MEDLINE

Original Publication: Berlin ; Hamburg : Paul Parey Scientific Publishers, c1990-

Extracellular Vesicles* ; Follicular Fluid*; Stromal Cells/*physiology; Androstenedione/metabolism ; Animals ; Cattle ; Cell Communication ; Cell Proliferation ; Female ; Ovary/cytology ; Progesterone/metabolism ; Stromal Cells/metabolism

The aim of this study was to investigate the effects of extracellular vesicles (EVs) on the proliferation and steroid hormone synthesis of bovine ovarian cortical stromal cells in vitro. The release and uptake of EVs are the new mechanisms of cell-to-cell communication. Using reverse transcriptase polymerase chain reaction, enzyme-linked immunosorbent assay, TUNEL and other experiments, we found that EVs in bovine follicular fluid can promote the proliferation and synthesis of androstenedione and progesterone in ovarian cortical stromal cells. Moreover, 100 μg/ml EVs caused the most significant effect. We conclude that EVs at 100 μg/ml can significantly promote the proliferation and synthesis of androstenedione and progesterone in ovarian cortical stromal cells. This research is of great significance for further elucidating the regulatory role of follicular fluid EVs in follicular development and atresia and for research on the interaction of ovarian stromal cells, granulosa cells and oocytes.
(© 2021 Wiley-VCH GmbH.)

Abraham, A., & Natarajagounder, S. J. E. R. (1997). Control of differentiation, transformation, and apoptosis in granulosa cells by oncogenes, oncoviruses, and tumor suppressor genes. Endocrine reviews. 18(4), 435-461.
Al-Dossary, A. A., Strehler, E. E., & Martin-Deleon, P. A. (2013). Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: Association with oviductal exosomes and uptake in sperm. PLoS One, 8(11), e80181. https://doi.org/10.1371/journal.pone.0080181.
Andrade, G. M., Meirelles, F. V., Perecin, F., & da Silveira, J. C. (2017). Cellular and extracellular vesicular origins of miRNAs within the bovine ovarian follicle. Reproduction in Domestic Animals, 52(6), 1036-1045. https://doi.org/10.1111/rda.13021.
Camussi, G., Deregibus, M. C., & Tetta, C. (2010). Paracrine/endocrine mechanism of stem cells on kidney repair: Role of microvesicle-mediated transfer of genetic information. Current Opinion in Nephrology and Hypertension, 19(1), 7-12. https://doi.org/10.1097/MNH.0b013e328332fb6f.
Candelaria, N. R., Padmanabhan, A., Stossi, F., Ljungberg, M. C., Shelly, K. E., Pew, B. K., Solis, M., Rossano, A. M., McAllister, J. M., Wu, S., & Richards, J. A. S. (2019). VCAM1 is induced in ovarian theca and stromal cells in a mouse model of androgen excess. Endocrinology, 160(6), 1377-1393. https://doi.org/10.1210/en.2018-00731.
Carletti, M. Z., Fiedler, S. D., & Christenson, L. K. (2010). MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biology of Reproduction, 83(2), 286-295. https://doi.org/10.1095/biolreprod.109.081448.
Chen, S., Zhu, X., & Huang, S. (2020). Clinical applications of extracellular vesicle long RNAs. Critical Reviews in Clinical Laboratory Sciences, 57(8), 508-521. https://doi.org/10.1080/10408363.2020.1751584.
Colombo, M., Raposo, G., & Thery, C. (2014). Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annual Review of Cell and Developmental Biology, 30, 255-289. https://doi.org/10.1146/annurev-cellbio-101512-122326.
Fabbiano, F., Corsi, J., Gurrieri, E., Trevisan, C., Notarangelo, M., & D'Agostino, V. G. (2020). RNA packaging into extracellular vesicles: An orchestra of RNA-binding proteins? Journal of Extracellular Vesicles, 10(2), e12043. https://doi.org/10.1002/jev2.12043.
Hua, W., Kazumichi, A., Haruo, H., Liu, X., Nobumasa, K., Yumiko, A., & Hideki, M. J. E. (2001). Effect of adrenal and ovarian androgens on type 4 follicles unresponsive to FSH in immature mice, Endocrinology, 11, 4930-4936.
Huang, Z., & Wells, D. (2010). The human oocyte and cumulus cells relationship: New insights from the cumulus cell transcriptome. MHR: Basic Science of Reproductive Medicine, 16(10), 715-725. https://doi.org/10.1093/molehr/gaq031.
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.
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.
Kim, K. M., Abdelmohsen, K., Mustapic, M., Kapogiannis, D., & Gorospe, M. (2017). RNA in extracellular vesicles. Wiley Interdisciplinary Reviews: RNA, 8(4), e1413. https://doi.org/10.1002/wrna.1413.
Li, Z., Jie, G., & Sheng, C. (2017). miR-21 Is involved in norepinephrine-mediated rat granulosa cell apoptosis by targeting SMAD7. Journal of molecular endocrinology, 58(4), 199-210.
Liu, S., Zhan, Y., Luo, J., Feng, J., Lu, J., Zheng, H., Wen, Q., & Fan, S. (2019). Roles of exosomes in the carcinogenesis and clinical therapy of non-small cell lung cancer. Biomedicine & Pharmacotherapy, 111, 338-346. https://doi.org/10.1016/j.biopha.2018.12.088.
Liu, T., Zhang, Q., Zhang, J., Li, C., Miao, Y. R., Lei, Q., Li, Q., & Guo, A. Y. (2019). EVmiRNA: A database of miRNA profiling in extracellular vesicles. Nucleic Acids Research, 47(D1), D89-D93. https://doi.org/10.1093/nar/gky985.
Lo Cicero, A., Stahl, P. D., & Raposo, G. (2015). Extracellular vesicles shuffling intercellular messages: For good or for bad. Current Opinion in Cell Biology, 35, 69-77. https://doi.org/10.1016/j.ceb.2015.04.013.
Lv, M. M., Zhu, X. Y., Chen, W. X., Zhong, S. L., Hu, Q., Ma, T. F., Zhang, J., Chen, L., Tang, J. H., & Zhao, J. H. (2014). Exosomes mediate drug resistance transfer in MCF-7 breast cancer cells and a probable mechanism is delivery of. P-glycoprotein, Tumour Biology: The Journal Of The International Society for Oncodevelopmental Biology and Medicine, 35(11), 10773-10779. https://doi.org/10.1007/s13277-014-2377-z.
Mantel, P. Y., & Marti, M. (2014). The role of extracellular vesicles in Plasmodium and other protozoan parasites. Cellular Microbiology, 16(3), 344-354. https://doi.org/10.1111/cmi.12259.
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.
Oliveira, D. L., Nakayasu, E. S., Joffe, L. S., Guimarães, A. J., Sobreira, T. J. P., Nosanchuk, J. D., Cordero, R. J. B., Frases, S., Casadevall, A., Almeida, I. C., Nimrichter, L., & Rodrigues, M. L. (2010). Characterization of yeast extracellular vesicles: Evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One, 5(6), e11113. https://doi.org/10.1371/journal.pone.0011113.
Orisaka, M., Tajima, K., Mizutani, T., Tsang, B. K., Fukuda, S., Yoshida, Y., Kotsuji, F. (2006). Granulosa cells promote differentiation of cortical stromal cells into theca cells in the bovine ovary. Biology of Reproduction, 75(5), 734-740.
Orisaka, M., Tajima, K., Tsang, B. K., & Kotsuji, F. (2009). Oocyte-granulosa-theca cell interactions during preantral follicular development. Journal of Ovarian Research, 2(1), 9. https://doi.org/10.1186/1757-2215-2-9.
Palma, G. A., Argañaraz, M. E., Barrera, A. D., Rodler, D., Mutto, A. Á., & Sinowatz, F. (2012). Biology and biotechnology of follicle development. The Scientific World Journal, 2012(5), 938138. https://doi.org/10.1100/2012/938138.
Qiu, M. N., Han, C. Q., Yang, Z. C., Liu, J., Quan, F. S., Zhang, Y. J. C. J. O. A., & Ences, V. (2013). Effect of ovarian stromal cells on co-cultured small antral follicles in the Goat. Chinese Journal of Animal and Veterinary Science, 44(7), 1043-1050.
Qiu, M., Liu, J., Han, C., Wu, B., Yang, Z., Su, F., & Zhang, Y. (2014). The influence of ovarian stromal/theca cells during in vitro culture on steroidogenesis, proliferation and apoptosis of granulosa cells derived from the goat ovary. Reproduction in Domestic Animals, 49(1), 170-176. https://doi.org/10.1111/rda.12256.
Raposo, G., & Stoorvogel, W. (2013). Extracellular vesicles: Exosomes, microvesicles, and friends. Journal of Cell Biology, 200(4), 373-383. https://doi.org/10.1083/jcb.201211138.
Record, M., Subra, C., Silvente-Poirot, S., & Poirot, M. (2011). Exosomes as intercellular signalosomes and pharmacological effectors. Biochemical Pharmacology, 81(10), 1171-1182. https://doi.org/10.1016/j.bcp.2011.02.011.
Saez, F., Frenette, G., & Sullivan, R. (2003). Epididymosomes and prostasomes: Their roles in posttesticular maturation of the sperm cells. Journal of Andrology, 24(2), 149-154. https://doi.org/10.1002/j.1939-4640.2003.tb02653.x.
Sinha, A, Alfaro, J, & Kislinger, T. (2017). Characterization of protein content present in exosomes isolated from conditioned media and urine. Current Protocols in Protein Science, 87(1), 21-24. https://doi.org/10.1002/cpps.23.
Sohel, M. M. H., Hoelker, M., Noferesti, S. S., Salilew-Wondim, D., Tholen, E., Looft, C., Rings, F., Uddin, M. J., Spencer, T. E., Schellander, K., & Tesfaye, D. (2013). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: Implications for bovine oocyte developmental competence. PLoS One, 8(11), e78505. https://doi.org/10.1371/journal.pone.0078505.
Sun, B., Ma, Y., Wang, F., Hu, L., & Sun, Y. (2019). miR-644-5p carried by bone mesenchymal stem cell-derived exosomes targets regulation of p53 to inhibit ovarian granulosa cell apoptosis. Stem Cell Research & Therapy, 10(1), 360. https://doi.org/10.1186/s13287-019-1442-3.
Sun, L., Li, D., Song, K., Wei, J., Yao, S., Li, Z., Su, X., Ju, X., Chao, L., Deng, X., Kong, B., & Li, L. I. (2017). Exosomes derived from human umbilical cord mesenchymal stem cells protect against cisplatin-induced ovarian granulosa cell stress and apoptosis in vitro. Scientific Reports, 7(1), 2552. https://doi.org/10.1038/s41598-017-02786-x.
Tajima, K., Orisaka, M., Mori, T., & Kotsuji, F. (2007). Ovarian theca cells in follicular function. Reproductive BioMedicine Online, 15(5), 591-609. https://doi.org/10.1016/S1472-6483(10)60392-6.
Théry C., Ostrowski M., Segura E. (2009). Membrane vesicles as conveyors of immune responses. Nature Reviews Immunology, 9(8):581-593.
Tsatsaronis, J. A., Franch-Arroyo, S., Resch, U., & Charpentier, E. J. T. I. M. (2018). Extracellular vesicle RNA: A universal mediator of microbial communication? Trends in Microbiology, 26(5), 401-410. https://doi.org/10.1016/j.tim.2018.02.009.
Urbanelli, L., Magini, A., Buratta, S., Brozzi, A., Sagini, K., Polchi, A., Tancini, B., & Emiliani, C. (2013). Signaling pathways in exosomes biogenesis, secretion and fate. Genes (Basel), 4(2), 152-170. https://doi.org/10.3390/genes4020152.
Wei-Ting, H., Raphatphorn, N., Tarique, K., 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.
Willms, E., Cabanas, C., Mager, 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.
Xu, L., Sun, H., Zhang, M., Jiang, Y., Zhang, C., Zhou, J., & Yan, G. (2017). MicroRNA-145 protects follicular granulosa cells against oxidative stress-induced apoptosis by targeting Kruppel-like factor 4. Molecular and Cellular Endocrinology, 452, 138-147. https://doi.org/10.1016/j.mce.2017.05.030.
Yan, G., Zhang, L., Fang, T., Zhang, Q., Wu, S., Jiang, Y., Sun, H., & Hu, Y. (2012). MicroRNA-145 suppresses mouse granulosa cell proliferation by targeting activin receptor IB. FEBS Letters, 586(19), 3263-3270. https://doi.org/10.1016/j.febslet.2012.06.048.
Zhang, J., Yin, H., Jiang, H., Du, X., & Yang, Z. (2020). The protective effects of human umbilical cord mesenchymal stem cell-derived extracellular vesicles on cisplatin-damaged granulosa cells. Taiwanese Journal of Obstetrics and Gynecology, 59(4), 527-533. https://doi.org/10.1016/j.tjog.2020.05.010.

2016ZX08007-002 National major special project; 2020NY-019 Shaanxi Province's key research and development plan

Keywords: bovine; cell proliferation; follicular fluid EVs; ovarian cortical stromal cells; steroid hormones

409J2J96VR (Androstenedione)
4G7DS2Q64Y (Progesterone)

Date Created: 20210817 Date Completed: 20211209 Latest Revision: 20211214

20240829

10.1111/rda.14007

34402549