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Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Endo-siRNA deficiency results in oocyte maturation failure and apoptosis in porcine oocytes

Wanxin Liu A , Qi Zhao A , Shanhua Piao A , Chunsheng Wang A , Qingran Kong B C and Tiezhu An A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Animal Developmental Biology, College of Life Science, Northeast Forestry University, Harbin, Heilongjiang Province 150040, China.

B Laboratory of Embryo Biotechnology, College of Life Science, Northeast Agricultural University, Harbin, Heilongjiang Province 150030, China.

C Corresponding authors. Emails: kqr721726@163.com; antiezhu@qq.com

Reproduction, Fertility and Development 29(11) 2168-2174 https://doi.org/10.1071/RD16498
Submitted: 29 August 2016  Accepted: 31 January 2017   Published: 12 April 2017

Journal Compilation © CSIRO 2017 Open Access CC BY-NC-ND

Abstract

Both microRNAs (miRNAs) and endogenous small interfering RNAs (endo-siRNAs) play key regulatory roles in gene expression. Some studies have demonstrated that the function of miRNA is suppressed in mouse oocytes, suggesting that endo-siRNA, not miRNA, is essential for female meiosis. This finding has yet to be confirmed in other species. In this study, by knockdown of DICER1, DROSHA and its cofactor DiGeorge syndrome critical region 8 (DGCR8) in porcine oocytes, we found that the proportion of oocytes with DICER1 deficiency that developed to meiosis II (MII) stage was significantly lower than oocytes with DROSHA and DGCR8 deficiency (39.23 versus 68.71 and 71.25% respectively; P < 0.05). Oocytes lacking DROSHA and DGCR8 formed a barrel-shaped metaphase I spindle, with chromosomes tightly aligned at the metaphase plate whereas most oocytes (87%) lacking DICER1 showed spindle abnormalities during oocyte in vitro maturation. Furthermore, DICER1 deficiency also resulted in oocyte apoptosis. These results indicate that endo-siRNAs are essential for oocyte maturation in pigs.

Additional keywords: gene regulation, in vitro maturation, livestock.


References

Ambros, V., Lee, R. C., Lavanway, A., Williams, P. T., and Jewell, D. (2003). MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr. Biol. 13, 807–818.
MicroRNAs and other tiny endogenous RNAs in C. elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFamsbs%3D&md5=96bf56bbce987562ee4ca55a18b90e9aCAS |

Andree, H. A., Reutelingsperger, C. P., Hauptmann, R., Hemker, H. C., Hermens, W. T., and Willems, G. M. (1990). Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J. Biol. Chem. 265, 4923–4928.
| 1:CAS:528:DyaK3cXhvFCjtbw%3D&md5=67f3b944f935048c5779b7bf11bc0333CAS |

Bagasra, O., and Prilliman, K. R. (2004). RNA interference: the molecular immune system. J. Mol. Histol. 35, 545–553.
| 1:CAS:528:DC%2BD2cXhtFWqsbvJ&md5=bb83b1dd7f6fdef45aacc3e88b91dc93CAS |

Banisch, T. U., Goudarzi, M., and Raz, E. (2012). Small RNAs in germ cell development. Curr. Top. Dev. Biol. 99, 79–113.
Small RNAs in germ cell development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmslClur0%3D&md5=c0299cc00ce1d5d2b45c36eb2461ae59CAS |

Bernstein, E., Caudy, A. A., Hammond, S. M., and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363–366.
Role for a bidentate ribonuclease in the initiation step of RNA interference.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXms12ksA%3D%3D&md5=9aa7ce0f3f150af438e925b4602badd8CAS |

Carthew, R. W., and Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642–655.
Origins and mechanisms of miRNAs and siRNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvFGksb0%3D&md5=928572bba7e96f65e21366f1f8e71465CAS |

Castel, S. E., and Martienssen, R. A. (2013). RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14, 100–112.
RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptlOrtQ%3D%3D&md5=a3c26290a9a4ca12765bb3092dca6aa0CAS |

Claycomb, J. M. (2014). Ancient endo-siRNA pathways reveal new tricks. Curr. Biol. 24, R703–R715.
Ancient endo-siRNA pathways reveal new tricks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlSqtrrJ&md5=d0910e31e394a11b0ea8557569efeaf9CAS |

Coticchio, G., Dal Canto, M., Mignini Renzini, M., Guglielmo, M. C., Brambillasca, F., Turchi, D., Novara, P. V., and Fadini, R. (2015). Oocyte maturation: gamete–somatic cell interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum. Reprod. Update 21, 427–454.
Oocyte maturation: gamete–somatic cell interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization.Crossref | GoogleScholarGoogle Scholar |

Czech, B., and Hannon, G. J. (2011). Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12, 19–31.
Small RNA sorting: matchmaking for Argonautes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFOiu7rE&md5=88be7b84a756225a01ed2319b77338d8CAS |

Ekwall, K. (2007). Epigenetic control of centromere behavior. Annu. Rev. Genet. 41, 63–81.
Epigenetic control of centromere behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1Sjsg%3D%3D&md5=23d2f8d35abb41684c29ed41385758a7CAS |

Ene, A. C., Park, S., Edelmann, W., and Taketo, T. (2013). Caspase 9 is constitutively activated in mouse oocytes and plays a key role in oocyte elimination during meiotic prophase progression. Dev. Biol. 377, 213–223.
Caspase 9 is constitutively activated in mouse oocytes and plays a key role in oocyte elimination during meiotic prophase progression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtl2jsLg%3D&md5=17080a649bf510fa5d2925c708092ab0CAS |

Evans, J. P., and Robinson, D. N. (2011). The spatial and mechanical challenges of female meiosis. Mol. Reprod. Dev. 78, 769–777.
The spatial and mechanical challenges of female meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7vF&md5=98324720abb82cb9614b48477f443c2eCAS |

Fukagawa, T., and Earnshaw, W. C. (2014). The centromere: chromatin foundation for the kinetochore machinery. Dev. Cell 30, 496–508.
The centromere: chromatin foundation for the kinetochore machinery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFagsbfF&md5=72ccdf824ecad0a65d5acc8622803d7aCAS |

García-López, J., Hourcade Jde, D., Alonso, L., Cardenas, D. B., and del Mazo, J. (2014). Global characterization and target identification of piRNAs and endo-siRNAs in mouse gametes and zygotes. Biochim. Biophys. Acta 1839, 463–475.
Global characterization and target identification of piRNAs and endo-siRNAs in mouse gametes and zygotes.Crossref | GoogleScholarGoogle Scholar |

Ghildiyal, M., and Zamore, P. D. (2009). Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94–108.
Small silencing RNAs: an expanding universe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFChtA%3D%3D&md5=ec8c290c42b6f7fb65dff44f1be15800CAS |

Hamilton, A., Voinnet, O., Chappell, L., and Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. EMBO J. 21, 4671–4679.
Two classes of short interfering RNA in RNA silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xms1KmsrY%3D&md5=edba38d4bcefe9ad2983f46594306fc5CAS |

Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514–521.
Oocyte-secreted factors enhance oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2gsb4%3D&md5=02562f698c762d378021f5cb17dd2107CAS |

Jolly, P., Estrela, P., and Ladomery, M. (2016). Oligonucleotide-based systems: DNA, microRNAs, DNA/RNA aptamers. Essays Biochem. 60, 27–35.
Oligonucleotide-based systems: DNA, microRNAs, DNA/RNA aptamers.Crossref | GoogleScholarGoogle Scholar |

Kaneda, M., Tang, F., O’Carroll, D., Lao, K., and Surani, M. A. (2009). Essential role for Argonaute2 protein in mouse oogenesis. Epigenetics Chromatin 2, 9.
Essential role for Argonaute2 protein in mouse oogenesis.Crossref | GoogleScholarGoogle Scholar |

Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., Livingston, D. M., and Rajewsky, K. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489–501.
Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1OhsL4%3D&md5=efceee864c451a5a56a2981e78dc8c75CAS |

Kanwar, J. R., Roy, K., Maremanda, N. G., Subramanian, K., Veedu, R. N., Bawa, R., and Kanwar, R. K. (2015). Nucleic acid-based aptamers: applications, development and clinical trials. Curr. Med. Chem. 22, 2539–2557.
Nucleic acid-based aptamers: applications, development and clinical trials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFWms7%2FN&md5=d13a84fe285c88563e829cb3c160d670CAS |

Kim, V. N., Han, J., and Siomi, M. C. (2009). Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126–139.
Biogenesis of small RNAs in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVCitA%3D%3D&md5=07527daad2b4c416a50d9c8f0719380bCAS |

Kong, Q., Xie, B., Li, J., Huan, Y., Huang, T., Wei, R., Lv, J., Liu, S., and Liu, Z. (2014). Identification and characterization of an oocyte factor required for porcine nuclear reprogramming. J. Biol. Chem. 289, 6960–6968.
Identification and characterization of an oocyte factor required for porcine nuclear reprogramming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjvV2jur8%3D&md5=7cf5a1e90dc594e3033c010bfe0107feCAS |

Li, L. C. (2014). Chromatin remodeling by the small RNA machinery in mammalian cells. Epigenetics 9, 45–52.
Chromatin remodeling by the small RNA machinery in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVyiurvM&md5=f3036118ea960b10de4bc11ec6d54c72CAS |

Ma, J., Flemr, M., Stein, P., Berninger, P., Malik, R., Zavolan, M., Svoboda, P., and Schultz, R. M. (2010). MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 20, 265–270.
MicroRNA activity is suppressed in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslSmurY%3D&md5=70bc0bb8228680522216090e03880864CAS |

Murchison, E. P., Stein, P., Xuan, Z., Pan, H., Zhang, M. Q., Schultz, R. M., and Hannon, G. J. (2007). Critical roles for Dicer in the female germline. Genes Dev. 21, 682–693.
Critical roles for Dicer in the female germline.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1WqsbY%3D&md5=ec0372ecbcf37f287602c5f47ff61073CAS |

Nejepinska, J., Malik, R., Filkowski, J., Flemr, M., Filipowicz, W., and Svoboda, P. (2012). dsRNA expression in the mouse elicits RNAi in oocytes and low adenosine deamination in somatic cells. Nucleic Acids Res. 40, 399–413.
dsRNA expression in the mouse elicits RNAi in oocytes and low adenosine deamination in somatic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Ggsg%3D%3D&md5=fd0174bc6c1aa7eb85e4a0bb981b3e95CAS |

Pratt, S. L., Sherrer, E. S., Reeves, D. E., and Stice, S. L. (2006). Factors influencing the commercialisation of cloning in the pork industry. Soc. Reprod. Fertil. Suppl. 62, 303–315.
| 1:STN:280:DC%2BD28vktlamsA%3D%3D&md5=c501a5031d50b4086cc4afa2342689abCAS |

Reuter, M., Berninger, P., Chuma, S., Shah, H., Hosokawa, M., Funaya, C., Antony, C., Sachidanandam, R., and Pillai, R. S. (2011). Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480, 264–267.
Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFWqtb7P&md5=1a36f171104637d354f1a18626868eecCAS |

Saito, K., and Siomi, M. C. (2010). Small RNA-mediated quiescence of transposable elements in animals. Dev. Cell 19, 687–697.
Small RNA-mediated quiescence of transposable elements in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsValsLnM&md5=c77f154215847e9658aa81b9bc772f69CAS |

Schmerler, S., and Wessel, G. M. (2011). Polar bodies – more a lack of understanding than a lack of respect. Mol. Reprod. Dev. 78, 3–8.
Polar bodies – more a lack of understanding than a lack of respect.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvV2lug%3D%3D&md5=94cff0daf98d766d1f0ec0a8baf57ec8CAS |

Stein, P., Rozhkov, N. V., Li, F., Cardenas, F. L., Davydenko, O., Vandivier, L. E., Gregory, B. D., Hannon, G. J., and Schultz, R. M. (2015). Essential role for endogenous siRNAs during meiosis in mouse oocytes. PLoS Genet. 11, e1005013.
Essential role for endogenous siRNAs during meiosis in mouse oocytes.Crossref | GoogleScholarGoogle Scholar |

Suh, N., Baehner, L., Moltzahn, F., Melton, C., Shenoy, A., Chen, J., and Blelloch, R. (2010). MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 20, 271–277.
MicroRNA function is globally suppressed in mouse oocytes and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslSmurc%3D&md5=4843abb563228780190d10aa72ddacfaCAS |

Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R. M., and Hannon, G. J. (2008). Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534–538.
Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1OrtLg%3D&md5=4ae7a8d452793f79982827a4b37e760dCAS |

Tang, F., Kaneda, M., O’Carroll, D., Hajkova, P., Barton, S. C., Sun, Y. A., Lee, C., Tarakhovsky, A., Lao, K., and Surani, M. A. (2007). Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 21, 644–648.
Maternal microRNAs are essential for mouse zygotic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjs1Wqsbo%3D&md5=e57024560755971541c04da28becd6bfCAS |

Tripathi, A., and Chaube, S. K. (2015). Roscovitine inhibits extrusion of second polar body and induces apoptosis in rat eggs cultured in vitro. Pharmacol. Rep. 67, 866–874.
Roscovitine inhibits extrusion of second polar body and induces apoptosis in rat eggs cultured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xitlyjtb8%3D&md5=3bdaf05149317ae458c9283fe881dbc3CAS |

van Engeland, M., Nieland, L. J., Ramaekers, F. C., Schutte, B., and Reutelingsperger, C. P. (1998). Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1–9.
Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtVGruw%3D%3D&md5=06db8efe35053c6b6ab2066289719becCAS |

Watanabe, T., Takeda, A., Tsukiyama, T., Mise, K., Okuno, T., Sasaki, H., Minami, N., and Imai, H. (2006). Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 20, 1732–1743.
Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvV2ksLs%3D&md5=6b1683f26919055c0fe643d5e64eb881CAS |

Wei, Y., Huan, Y., Shi, Y., Liu, Z., Bou, G., Luo, Y., Zhang, L., Yang, C., Kong, Q., Tian, J., Xia, P., Sun, Q. Y., and Liu, Z. (2011). Unfaithful maintenance of methylation imprints due to loss of maternal nuclear Dnmt1 during somatic cell nuclear transfer. PLoS One 6, e20154.
Unfaithful maintenance of methylation imprints due to loss of maternal nuclear Dnmt1 during somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXms1Kmurg%3D&md5=78c26b5b436f33ab0217fdc7ccfef241CAS |

Whyte, J. J., and Prather, R. S. (2011). Genetic modifications of pigs for medicine and agriculture. Mol. Reprod. Dev. 78, 879–891.
Genetic modifications of pigs for medicine and agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7rK&md5=5f707bd4ee0269ee9e232a17fda0cc4bCAS |

Xu, B. Z., Li, M., Xiong, B., Lin, S. L., Zhu, J. Q., Hou, Y., Chen, D. Y., and Sun, Q. Y. (2009). Involvement of calcium/calmodulin-dependent protein kinase kinase in meiotic maturation of pig oocytes. Anim. Reprod. Sci. 111, 17–30.
Involvement of calcium/calmodulin-dependent protein kinase kinase in meiotic maturation of pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCgs7%2FL&md5=87dac586b8946d6b4a789e26367641dcCAS |

Yuan, S., Ortogero, N., Wu, Q., Zheng, H., and Yan, W. (2014). Murine follicular development requires oocyte DICER, but not DROSHA. Biol. Reprod. 91, 39.
Murine follicular development requires oocyte DICER, but not DROSHA.Crossref | GoogleScholarGoogle Scholar |