Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Expression and Preliminary Functional Profiling of the let-7 Family during Porcine Ovary Follicle Atresia

  • Cao, Rui (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Wu, Wang Jun (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Zhou, Xiao Long (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Xiao, Peng (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Wang, Yi (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Liu, Hong Lin (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University)
  • Received : 2014.05.12
  • Accepted : 2015.01.19
  • Published : 2015.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Most follicles in the mammalian ovary undergo atresia. Granulosa cell apoptosis is a hallmark of follicle atresia. Our previous study using a microRNA (miRNA) microarray showed that the let-7 microRNA family was differentially expressed during follicular atresia. However, whether the let-7 miRNA family members are related to porcine (Sus scrofa) ovary follicular apoptosis is unclear. In the current study, real-time quantitative polymerase chain reaction showed that the expression levels of let-7 family members in follicles and granulosa cells were similar to our microarray data, in which miRNAs let-7a, let-7b, let-7c, and let-7i were significantly decreased in early atretic and progressively atretic porcine ovary follicles compared with healthy follicles, while let-7g was highly expressed during follicle atresia. Furthermore, flow cytometric analysis and Hoechst33342 staining demonstrated that let-7g increased the apoptotic rate of cultured granulosa cells. In addition, let-7 target genes were predicted and annotated by TargetScan, PicTar, gene ontology and Kyoto encyclopedia of genes and genomes pathways. Our data provide new insight into the association between the let-7 miRNA family in granulosa cell programmed death.

Keywords

References

  1. Bortul, R., Tazzari, P.L., Cappellini, A., Tabellini, G., Billi, A.M., Bareggi, R., Manzoli, L., Cocco, L., and Martelli, A.M. (2003). Constitutively active Akt1 protects HL60 leukemia cells from TRAIL-induced apoptosis through a mechanism involving NF-kappaB activation and cFLIP(L) up-regulation. Leukemia 17, 379-389. https://doi.org/10.1038/sj.leu.2402793
  2. Carletti, M.Z., Fiedler, S.D., and Christenson, L.K. (2010). MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol. Reprod. 83, 286-295. https://doi.org/10.1095/biolreprod.109.081448
  3. Carson, R.S., Findlay, J.K., Burger, H.G., and Trounson, A.O. (1979). Gonadotropin receptors of the ovine ovarian follicle during follicular growth and atresia. Biol. Reprod. 21, 75-87. https://doi.org/10.1095/biolreprod21.1.75
  4. Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., Barbisin, M., Xu, N.L., Mahuvakar, V.R., and Andersen, M.R. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179. https://doi.org/10.1093/nar/gni178
  5. Cheng, Y., Maeda, A., Goto, Y., Matsuda, F., Miyano, T., Inoue, N., Sakamaki, K., and Manabe, N. (2008). Changes in expression and localization of X-linked inhibitor of apoptosis protein (XIAP) in follicular granulosa cells during atresia in porcine ovaries. J. Reprod. Dev. 54, 454-459. https://doi.org/10.1262/jrd.20088
  6. Chun, S.Y., Eisenhauer, K.M., Minami, S., Billig, H., Perlas, E., and Hsueh, A.J. (1996). Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor. Endocrinology 137, 1447-1456. https://doi.org/10.1210/endo.137.4.8625923
  7. Craig, J., Orisaka, M., Wang, H., Orisaka, S., Thompson, W., Zhu, C., Kotsuji, F., and Tsang, B.K. (2007). Gonadotropin and intraovarian signals regulating follicle development and atresia: the delicate balance between life and death. Front. Biosci. 12, 3628-3639. https://doi.org/10.2741/2339
  8. Dai, L., Tsai-Morris, C.H., Sato, H., Villar, J., Kang, J.H., Zhang, J., and Dufau, M.L. (2011). Testis-specific miRNA-469 up-regulated in gonadotropin-regulated testicular RNA helicase (GRTH/DDX25)-null mice silences transition protein 2 and protamine 2 messages at sites within coding region: implications of its role in germ cell development. J. Biol. Chem. 286, 44306-44318. https://doi.org/10.1074/jbc.M111.282756
  9. Diskin, M.G., Mackey, D.R., Roche, J.F., and Sreenan, J.M. (2003). Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Anim. Reprod. Sci. 78, 345-370. https://doi.org/10.1016/S0378-4320(03)00099-X
  10. Eulalio, A., Huntzinger, E., Nishihara, T., Rehwinkel, J., Fauser, M., and Izaurralde, E. (2009). Deadenylation is a widespread effect of miRNA regulation. RNA 15, 21-32.
  11. Fu, T.Y., Lin, C.T., and Tang, P.C. (2011). Steroid hormoneregulated let-7b mediates cell proliferation and basigin expression in the mouse endometrium. J. Reprod. Dev. 57, 627-635. https://doi.org/10.1262/jrd.11-018E
  12. Guthrie, H.D., Cooper, B.S., Welch, G.R., Zakaria, A.D., and Johnson, L.A. (1995). Atresia in follicles grown after ovulation in the pig: measurement of increased apoptosis in granulosa cells and reduced follicular fluid estradiol-17 beta. Biol. Reprod. 52, 920-927. https://doi.org/10.1095/biolreprod52.4.920
  13. Hay, M.R., Cran, D.G., and Moor, R.M. (1976). Structural changes occurring during atresia in sheep ovarian follicles. Cell Tissue Res. 169, 515-529.
  14. Hillier, S.G., and Tetsuka, M. (1997). Role of androgens in follicle maturation and atresia. Baillieres Clin. Obstet. Gynaecol. 11, 249-260. https://doi.org/10.1016/S0950-3552(97)80036-3
  15. Hsueh, A.J., Billig, H., and Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr. Rev. 15, 707-724.
  16. Hughes, F.M., Jr., and Gorospe, W.C. (1991). Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129, 2415-2422. https://doi.org/10.1210/endo-129-5-2415
  17. Huntzinger, E., and Izaurralde, E. (2011). Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110. https://doi.org/10.1038/nrg2936
  18. Le, M.T., Shyh-Chang, N., Khaw, S.L., Chin, L., Teh, C., Tay, J., O'Day, E., Korzh, V., Yang, H., Lal, A., et al. (2011). Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miRNA-target gene pairs. PLoS Genet. 7, e1002242. https://doi.org/10.1371/journal.pgen.1002242
  19. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S., and Wang, X. (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489. https://doi.org/10.1016/S0092-8674(00)80434-1
  20. Li, M., Xia, Y., Gu, Y., Zhang, K., Lang, Q., Chen, L., Guan, J., Luo, Z., Chen, H., Li, Y., et al., (2010). MicroRNAome of porcine pre- and postnatal development. PLoS One 5, e11541. https://doi.org/10.1371/journal.pone.0011541
  21. Li, M., Liu, Y., Wang, T., Guan, J., Luo, Z., Chen, H., Wang, X., Chen, L., Ma, J., Mu, Z., et al. (2011). Repertoire of porcine microRNAs in adult ovary and testis by deep sequencing. Int. J. Biol. Sci. 7, 1045-1055. https://doi.org/10.7150/ijbs.7.1045
  22. Lian, C., Sun, B., Niu, S., Yang, R., Liu, B., Lu, C., Meng, J., Qiu, Z., Zhang, L., and Zhao, Z. (2012). A comparative profile of the microRNA transcriptome in immature and mature porcine testes using Solexa deep sequencing. FEBS J. 279, 964-975. https://doi.org/10.1111/j.1742-4658.2012.08480.x
  23. Lin, P.F., Hao, Y.B., Guo, H.L., Liu, H.L., and Rui, R. (2010). Role of Fas/FasL on apoptosis of porcine follicular granulosa cells derived from isolated follicles during culture in vitro. Dongwuxue Yanjiu 31, 268-274.
  24. Lin, F., Li, R., Pan, Z.X., Zhou, B., Yu de, B., Wang, X.G., Ma, X.S., Han, J., Shen, M., and Liu, H.L. (2012). miR-26b promotes granulosa cell apoptosis by targeting ATM during follicular atresia in porcine ovary. PLoS One 7, e38640. https://doi.org/10.1371/journal.pone.0038640
  25. Manabe, N., Imai, Y., Ohno, H., Takahagi, Y., Sugimoto, M., and Miyamoto, H. (1996). Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in pig ovaries. Experientia 52, 647-651. https://doi.org/10.1007/BF01925566
  26. Manabe, N., Goto, Y., Matsuda-Minehata, F., Inoue, N., Maeda, A., Sakamaki, K., and Miyano, T. (2004). Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J. Reprod. Dev. 50, 493-514. https://doi.org/10.1262/jrd.50.493
  27. Matsuda-Minehata, F., Inoue, N., Goto, Y., and Manabe, N. (2006). The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules. J. Reprod. Dev. 52, 695-705. https://doi.org/10.1262/jrd.18069
  28. Meng, F., Glaser, S.S., Francis, H., DeMorrow, S., Han, Y., Passarini, J.D., Stokes, A., Cleary, J.P., Liu, X., Venter, J., et al. (2012). Functional analysis of microRNAs in human hepatocellular cancer stem cells. J. Cell. Mol. Med. 16, 160-173. https://doi.org/10.1111/j.1582-4934.2011.01282.x
  29. Pasquinelli, A.E., Reinhart, B.J., Slack, F., Martindale, M.Q., Kuroda, M.I., Maller, B., Hayward, D.C., Ball, E.E., Degnan, B., Muller, P., et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89. https://doi.org/10.1038/35040556
  30. Qian, P., Zuo, Z., Wu, Z., Meng, X., Li, G., Wu, Z., Zhang, W., Tan, S., Pandey, V., Yao, Y., et al. (2011). Pivotal role of reduced let-7g expression in breast cancer invasion and metastasis. Cancer Res. 71, 6463-6474. https://doi.org/10.1158/0008-5472.CAN-11-1322
  31. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906. https://doi.org/10.1038/35002607
  32. Sasson, R., Winder, N., Kees, S., and Amsterdam, A. (2002). Induction of apoptosis in granulosa cells by TNF alpha and its attenuation by glucocorticoids involve modulation of Bcl-2. Biochem. Biophys. Res. Commun. 294, 51-59. https://doi.org/10.1016/S0006-291X(02)00431-X
  33. Shimizu, S., Takehara, T., Hikita, H., Kodama, T., Miyagi, T., Hosui, A., Tatsumi, T., Ishida, H., Noda, T., Nagano, H., et al. (2010). The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma. J. Hepatol. 52, 698-704. https://doi.org/10.1016/j.jhep.2009.12.024
  34. Sugimoto, M., Manabe, N., Kimura, Y., MYOUMOTO, A., IMAI, Y., OHNO, H. and MIYAMOTO, H. (1998). Ultrastructural changes in granulosa cells in porcine antral follicles undergoing atresia indicate apoptotic cell death. J. Reprod. Dev. 44, 7-14. https://doi.org/10.1262/jrd.44.7
  35. Tilly, J.L., Kowalski, K.I., Johnson, A.L., and Hsueh, A. (1991). Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129, 2799-2801. https://doi.org/10.1210/endo-129-5-2799
  36. Tilly, J.L., and Tilly, K.I. (1995). Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology 136, 242-252. https://doi.org/10.1210/endo.136.1.7828537
  37. Trang, P., Medina, P.P., Wiggins, J.F., Ruffino, L., Kelnar, K., Omotola, M., Homer, R., Brown, D., Bader, A.G., Weidhaas, J.B., et al. (2010). Regression of murine lung tumors by the let-7 microRNA. Oncogene 29, 1580-1587. https://doi.org/10.1038/onc.2009.445
  38. Tsang, W.P., and Kwok, T.T. (2008). Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis 13, 1215-1222. https://doi.org/10.1007/s10495-008-0256-z
  39. Wada, S., Manabe, N., Nakayama, M., Inou, N., Matsui, T., and Miyamoto, H. (2002). TRAIL-decoy receptor 1 plays inhibitory role in apoptosis of granulosa cells from pig ovarian follicles. J. Vet. Med. Sci. 64, 435-439. https://doi.org/10.1292/jvms.64.435
  40. Xie, S.S., Huang, T.H., Shen, Y., Li, X.Y., Zhang, X.X., Zhu, M.J., Qin, H.Y. and Zhao, S.H. (2010). Identification and characterization of microRNAs from porcine skeletal muscle. Anim. Genet. 41, 179-190. https://doi.org/10.1111/j.1365-2052.2009.01991.x
  41. Yamagata, K., Fujiyama, S., Ito, S., Ueda, T., Murata, T., Naitou, M., Takeyama, K., Minami, Y., O'Malley, B.W., et al. (2009). Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol. Cell. 36, 340-347. https://doi.org/10.1016/j.molcel.2009.08.017

Cited by

  1. Transcriptome profile of one-month-old lambs’ granulosa cells after superstimulation vol.30, pp.1, 2016, https://doi.org/10.5713/ajas.15.0999
  2. Let-7g induces granulosa cell apoptosis by targeting MAP3K1 in the porcine ovary vol.68, 2015, https://doi.org/10.1016/j.biocel.2015.08.011
  3. MicroRNA-144 is regulated by CP2 and decreases COX-2 expression and PGE2 production in mouse ovarian granulosa cells vol.8, pp.2, 2017, https://doi.org/10.1038/cddis.2017.24
  4. MicroRNA in ovarian function vol.363, pp.1, 2016, https://doi.org/10.1007/s00441-015-2307-4
  5. A syntenic locus on buffalo chromosome 20: novel genomic hotspot for miRNAs involved in follicular-luteal transition vol.17, pp.2-3, 2017, https://doi.org/10.1007/s10142-016-0535-7
  6. Circulating microRNAs in follicular fluid, powerful tools to explore in vitro fertilization process vol.6, pp.1, 2016, https://doi.org/10.1038/srep24976
  7. Comparative profiling of differentially expressed microRNAs between the follicular and luteal phases ovaries of goats vol.5, pp.1, 2016, https://doi.org/10.1186/s40064-016-2902-1
  8. MicroRNAs: New Insight in Modulating Follicular Atresia: A Review vol.18, pp.2, 2017, https://doi.org/10.3390/ijms18020333
  9. High-throughput sequencing reveals differential expression of miRNAs in prehierarchal follicles of laying and brooding geese vol.48, pp.7, 2016, https://doi.org/10.1152/physiolgenomics.00011.2016
  10. Identification and characterization of a specific 13-miRNA expression signature during follicle activation in the zebrafish ovary† vol.98, pp.1, 2017, https://doi.org/10.1093/biolre/iox160
  11. Characterization of the miRNA regulators of the human ovulatory cascade vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-33807-y
  12. Roles of microRNAs in mammalian reproduction: from the commitment of germ cells to peri-implantation embryos pp.14647931, 2019, https://doi.org/10.1111/brv.12459
  13. MicroRNAs: tiny molecules with a significant role in mammalian follicular and oocyte development vol.155, pp.3, 2018, https://doi.org/10.1530/REP-17-0428
  14. MicroRNAs in ovarian follicular atresia and granulosa cell apoptosis vol.17, pp.1, 2019, https://doi.org/10.1186/s12958-018-0450-y
  15. miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis vol.1861, pp.3, 2015, https://doi.org/10.1016/j.bbagrm.2018.01.009
  16. MicroRNA profiling and identification of let-7a as a target to prevent chemotherapy-induced primordial follicles apoptosis in mouse ovaries vol.9, pp.None, 2015, https://doi.org/10.1038/s41598-019-45642-w
  17. Grape Seed Procyanidin B2 Protects Porcine Ovarian Granulosa Cells against Oxidative Stress-Induced Apoptosis by Upregulating let-7a Expression vol.2019, pp.None, 2015, https://doi.org/10.1155/2019/1076512
  18. Expression of Transcripts in Marmoset Oocytes Retrieved during Follicle Isolation Without Gonadotropin Induction vol.20, pp.5, 2015, https://doi.org/10.3390/ijms20051133
  19. Comparative expression analysis of let-7 microRNAs during ovary development in Megalobrama amblycephala vol.45, pp.3, 2019, https://doi.org/10.1007/s10695-019-00624-7
  20. Answer to Controversy: miR-10a Replacement Approaches Do Not Offer Protection against Chemotherapy-Induced Gonadotoxicity in Mouse Model vol.20, pp.19, 2015, https://doi.org/10.3390/ijms20194958
  21. Phylogenetic Analysis to Explore the Association Between Anti-NMDA Receptor Encephalitis and Tumors Based on microRNA Biomarkers vol.9, pp.10, 2019, https://doi.org/10.3390/biom9100572
  22. MIR143 Inhibits Steroidogenesis and Induces Apoptosis Repressed by H3K27me3 in Granulosa Cells vol.8, pp.None, 2015, https://doi.org/10.3389/fcell.2020.565261
  23. Circular RNA expression profiling and bioinformatic analysis of cumulus cells in endometriosis infertility patients vol.12, pp.23, 2020, https://doi.org/10.2217/epi-2020-0291
  24. Integrative Proteomic and Phosphoproteomic Analyses of Granulosa Cells During Follicular Atresia in Porcine vol.8, pp.None, 2015, https://doi.org/10.3389/fcell.2020.624985
  25. Expression characteristics of pineal miRNAs at ovine different reproductive stages and the identification of miRNAs targeting the AANAT gene vol.22, pp.1, 2015, https://doi.org/10.1186/s12864-021-07536-y
  26. Small RNA sequencing reveals distinct nuclear microRNAs in pig granulosa cells during ovarian follicle growth vol.14, pp.1, 2021, https://doi.org/10.1186/s13048-021-00802-3
  27. Gene cascade analysis in human granulosa tumor cells (KGN) following exposure to high levels of free fatty acids and insulin vol.14, pp.1, 2015, https://doi.org/10.1186/s13048-021-00934-6