Promoter hypermethylation of PIWI/piRNA pathway genes associated with diminished pachytene piRNA production in bovine hybrid male sterility

References

• Civetta A. Misregulation of gene expression and sterility in interspecies hybrids: causal links and alternative hypotheses. J Mol Evol. 2016 May;82(4–5):176–182.
   PubMed Web of Science ®Google Scholar
• Mallet J. Hybrid speciation. Nature. 2007 Mar 15;446(7133):279–283.
   PubMed Web of Science ®Google Scholar
• Maheshwari S, Barbash DA. The genetics of hybrid incompatibilities. Annu Rev Genet. 2011;45:331–355.
   PubMed Web of Science ®Google Scholar
• Qiu Q, Zhang G, Ma T, et al. The yak genome and adaptation to life at high altitude. Nat Genet. 2012 Jul 1;44(8):946–949.
   PubMed Web of Science ®Google Scholar
• Lou YN, Liu WJ, Wang CL, et al. Histological evaluation and PRDM9 expression level in the testis of sterile male cattle-yaks. Livestock Sci. 2014;160:208–213.
   Web of Science ®Google Scholar
• Yan P, Xiang L, Guo X, et al. The low expression of Dmrt7 is associated with spermatogenic arrest in cattle-yak. Mol Biol Rep. 2014 Nov;41(11):7255–7263.
   PubMed Web of Science ®Google Scholar
• Zhang GW, Wu Y, Luo Z, et al. Comparison of Y-chromosome-linked TSPY, TSPY2, and PRAMEY genes in Taurus cattle, yaks, and interspecific hybrid bulls. J Dairy Sci. 2019 May 15;102(7):6263–6275.
   PubMed Web of Science ®Google Scholar
• Cai X, Yu S, Mipam T, et al. Comparative analysis of testis transcriptomes associated with male infertility in cattleyak. Theriogenology. 2017 Jan;15(88):28–42.
   Google Scholar
• Yu S, Cai X, Sun L, et al. Comparative iTRAQ proteomics revealed proteins associated with spermatogenic arrest of cattleyak. J Proteomics. 2016 Jun;16(142):102–113.
   Google Scholar
• Michalak P. Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity (Edinb). 2009 Jan;102(1):45–50.
   PubMed Web of Science ®Google Scholar
• Stewart KR, Veselovska L, Kelsey G. Establishment and functions of DNA methylation in the germline. Epigenomics. 2016 Oct;8(10):1399–1413.
   PubMed Web of Science ®Google Scholar
• Rajender S, Avery K, Agarwal A. Epigenetics, spermatogenesis and male infertility. Mutat Res. 2011 May-Jun;727(3):62–71.
   PubMed Web of Science ®Google Scholar
• Iwasaki YW, Siomi MC, Siomi H. PIWI-interacting RNA: its biogenesis and functions. Annu Rev Biochem. 2015;84:405–433.
   PubMed Web of Science ®Google Scholar
• Chen T, Li E. Structure and function of eukaryotic DNA methyltransferases. Curr Top Dev Biol. 2004;60:55–89.
   PubMed Web of Science ®Google Scholar
• Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001 Aug 10;293(5532):1068–1070.
   PubMed Web of Science ®Google Scholar
• Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012 May 29;13(7):484–492.
   PubMed Web of Science ®Google Scholar
• Khazamipour N, Noruzinia M, Fatehmanesh P, et al. MTHFR promoter hypermethylation in testicular biopsies of patients with non-obstructive azoospermia: the role of epigenetics in male infertility. Hum Reprod. 2009 Sep;24(9):2361–2364.
   PubMed Web of Science ®Google Scholar
• Xu A, Hua Y, Zhang J, et al. Abnormal hypermethylation of the VDAC2 promoter is a potential cause of idiopathic asthenospermia in men. Sci Rep. 2016 Nov 28;6:37836.
   PubMed Web of Science ®Google Scholar
• Liu Z, Li Q, Pan Z, et al. Comparative analysis on mRNA expression level and methylation status of DAZL gene between cattle-yaks and their parents. Anim Reprod Sci. 2011 Jul;126(3–4):258–264.
   PubMed Web of Science ®Google Scholar
• Wang S, Pan Z, Zhang Q, et al. Differential mRNA expression and promoter methylation status of SYCP3 gene in testes of yaks and cattle-yaks. Reprod Domest Anim. 2012 Jun;47(3):455–462.
   PubMed Web of Science ®Google Scholar
• Gu Y, Li Q, Pan Z, et al. Molecular cloning, gene expression and methylation status analysis of PIWIL1 in cattle-yaks and the parental generation. Anim Reprod Sci. 2013 Aug;140(3–4):131–137.
   PubMed Web of Science ®Google Scholar
• Luo H, Zhou Y, Li Y, et al. Splice variants and promoter methylation status of the Bovine Vasa Homology (Bvh) gene may be involved in bull spermatogenesis. BMC Genet. 2013 Jul;1(14):58.
   Google Scholar
• Li B, Luo H, Weng Q, et al. Differential DNA methylation of the meiosis-specific gene FKBP6 in testes of yak and cattle-yak hybrids. Reprod Domest Anim. 2016 Dec;51(6):1030–1038.
   PubMed Web of Science ®Google Scholar
• Heyn H, Ferreira HJ, Bassas L, et al. Epigenetic disruption of the PIWI pathway in human spermatogenic disorders. PloS One. 2012;7(10):e47892.
   PubMed Web of Science ®Google Scholar
• Ferreira HJ, Heyn H, Garcia Del Muro X, et al. Epigenetic loss of the PIWI/piRNA machinery in human testicular tumorigenesis. Epigenetics. 2014 Jan;9(1):113–118.
   PubMed Web of Science ®Google Scholar
• Aravin A, Gaidatzis D, Pfeffer S, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature. 2006 Jul 13;442(7099):203–207.
   PubMed Web of Science ®Google Scholar
• Girard A, Sachidanandam R, Hannon GJ, et al. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature. 2006 Jul 13;442(7099):199–202.
   PubMed Web of Science ®Google Scholar
• Lau NC, Seto AG, Kim J, et al. Characterization of the piRNA complex from rat testes. Science. 2006 Jul 21;313(5785):363–367.
   PubMed Web of Science ®Google Scholar
• de Mateo S, Sassone-Corsi P. Regulation of spermatogenesis by small non-coding RNAs: role of the germ granule. Semin Cell Dev Biol. 2014 May;29:84–92.
   PubMed Web of Science ®Google Scholar
• Kim VN. Small RNAs just got bigger: piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev. 2006 Aug 1;20(15):1993–1997.
   PubMed Web of Science ®Google Scholar
• Li XZ, Roy CK, Dong X, et al. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol Cell. 2013 Apr 11;50(1):67–81.
   PubMed Web of Science ®Google Scholar
• Aravin AA, Sachidanandam R, Bourc’his D, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell. 2008 Sep 26;31(6):785–799.
   PubMed Web of Science ®Google Scholar
• Reuter M, Berninger P, Chuma S, et al. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature. 2011 Nov 27;480(7376):264–267.
   PubMed Web of Science ®Google Scholar
• Zhang P, Kang JY, Gou LT, et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 2015 Feb;25(2):193–207.
   PubMed Web of Science ®Google Scholar
• Pezic D, Manakov SA, Sachidanandam R, et al. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev. 2014 Jul 1;28(13):1410–1428.
   PubMed Web of Science ®Google Scholar
• Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008 Apr 1;22(7):908–917.
   PubMed Web of Science ®Google Scholar
• Di Giacomo M, Comazzetto S, Saini H, et al. Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol Cell. 2013 May 23;50(4):601–608.
   PubMed Web of Science ®Google Scholar
• Goh WS, Falciatori I, Tam OH, et al. piRNA-directed cleavage of meiotic transcripts regulates spermatogenesis. Genes Dev. 2015 May 15;29(10):1032–1044.
   PubMed Web of Science ®Google Scholar
• Gou LT, Dai P, Yang JH, et al. Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis. Cell Res. 2014 Jun;24(6):680–700.
   PubMed Web of Science ®Google Scholar
• Ozata DM, Gainetdinov I, Zoch A, et al. PIWI-interacting RNAs: small RNAs with big functions. Nat Rev Genet. 2019 Feb;20(2):89–108.
   PubMed Web of Science ®Google Scholar
• da Cruz I, Rodriguez-Casuriaga R, Santinaque FF, et al. Transcriptome analysis of highly purified mouse spermatogenic cell populations: gene expression signatures switch from meiotic-to postmeiotic-related processes at pachytene stage. BMC Genomics. 2016 Apr;19(17):294.
   Google Scholar
• Zhang Y, Wang X, Kang L. A k-mer scheme to predict piRNAs and characterize locust piRNAs. Bioinformatics. 2011 Mar 15;27(6):771–776.
   PubMed Web of Science ®Google Scholar
• Brennecke J, Aravin AA, Stark A, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007 Mar 23;128(6):1089–1103.
   PubMed Web of Science ®Google Scholar
• Robine N, Lau NC, Balla S, et al. A broadly conserved pathway generates 3ʹUTR-directed primary piRNAs. Curr Biol. 2009 Dec 29;19(24):2066–2076.
   PubMed Web of Science ®Google Scholar
• Li XZ, Roy CK, Moore MJ, et al. Defining piRNA primary transcripts. Cell Cycle. 2013 Jun 1;12(11):1657–1658.
   PubMed Web of Science ®Google Scholar
• Gan H, Lin X, Zhang Z, et al. piRNA profiling during specific stages of mouse spermatogenesis. Rna. 2011 Jul;17(7):1191–1203.
   PubMed Web of Science ®Google Scholar
• O’Donnell KA, Boeke JD. Mighty Piwis defend the germline against genome intruders. Cell. 2007 Apr 6;129(1):37–44.
   PubMed Web of Science ®Google Scholar
• Aravin AA, Sachidanandam R, Girard A, et al. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science. 2007 May 4;316(5825):744–747.
   PubMed Web of Science ®Google Scholar
• Gainetdinov I, Skvortsova Y, Kondratieva S, et al. Two modes of targeting transposable elements by piRNA pathway in human testis. Rna. 2017 Nov;23(11):1614–1625.
   PubMed Web of Science ®Google Scholar
• Michalak P, Noor MA. Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol. 2003 Jul;20(7):1070–1076.
   PubMed Web of Science ®Google Scholar
• Michalak P, Noor MA. Association of misexpression with sterility in hybrids of Drosophila simulansand D. mauritiana. J Mol Evol. 2004 Aug;59(2):277–282.
   PubMed Web of Science ®Google Scholar
• Wenda JM, Homolka D, Yang Z, et al. Distinct roles of RNA helicases MVH and TDRD9 in PIWI slicing-triggered mammalian piRNA biogenesis and function. Dev Cell. 2017 Jun 19;41(6):623–637 e9.
   PubMed Web of Science ®Google Scholar
• Kuramochi-Miyagawa S, Watanabe T, Gotoh K, et al. MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev. 2010 May;24(9):887–892.
   PubMed Web of Science ®Google Scholar
• Castaneda J, Genzor P, van der Heijden GW, et al. Reduced pachytene piRNAs and translation underlie spermiogenic arrest in Maelstrom mutant mice. Embo J. 2014 Sep 17;33(18):1999–2019.
   PubMed Web of Science ®Google Scholar
• Gao Q, Frohman MA. Roles for the lipid-signaling enzyme MitoPLD in mitochondrial dynamics, piRNA biogenesis, and spermatogenesis. BMB Rep. 2012 Jan;45(1):7–13.
   PubMed Web of Science ®Google Scholar
• Wang J, Saxe JP, Tanaka T, et al. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr Biol. 2009 Apr 28;19(8):640–644.
   PubMed Web of Science ®Google Scholar
• Reuter M, Chuma S, Tanaka T, et al. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat Struct Mol Biol. 2009 Jun;16(6):639–646.
   PubMed Web of Science ®Google Scholar
• Ding D, Liu J, Midic U, et al. TDRD5 binds piRNA precursors and selectively enhances pachytene piRNA processing in mice. Nat Commun. 2018 Jan 9;9(1):127.
   PubMedGoogle Scholar
• Wasik KA, Tam OH, Knott SR, et al. RNF17 blocks promiscuous activity of PIWI proteins in mouse testes. Genes Dev. 2015 Jul 1;29(13):1403–1415.
   PubMed Web of Science ®Google Scholar
• Xiol J, Cora E, Koglgruber R, et al. A role for Fkbp6 and the chaperone machinery in piRNA amplification and transposon silencing. Mol Cell. 2012 Sep 28;47(6):970–979.
   PubMed Web of Science ®Google Scholar
• Zheng K, Xiol J, Reuter M, et al. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11841–11846.
   PubMed Web of Science ®Google Scholar
• Vourekas A, Zheng K, Fu Q, et al. The RNA helicase MOV10L1 binds piRNA precursors to initiate piRNA processing. Genes Dev. 2015 Mar 15;29(6):617–629.
   PubMed Web of Science ®Google Scholar
• Zhou L, Canagarajah B, Zhao Y, et al. BTBD18 regulates a subset of piRNA-generating loci through transcription elongation in mice. Dev Cell. 2017 Mar 13;40(5):453–466 e5.
   PubMed Web of Science ®Google Scholar
• Ding D, Liu J, Dong K, et al. Mitochondrial membrane-based initial separation of MIWI and MILI functions during pachytene piRNA biogenesis. Nucleic Acids Res. 2019 Mar 18;47(5):2594–2608.
   PubMed Web of Science ®Google Scholar
• Pandey RR, Homolka D, Olotu O, et al. Exonuclease domain-containing 1 enhances MIWI2 piRNA biogenesis via its interaction with TDRD12. Cell Rep. 2018 Sep 25;24(13):3423–3432 e4.
   PubMed Web of Science ®Google Scholar
• Carmell MA, Girard A, van de Kant HJ, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell. 2007 Apr;12(4):503–514.
   PubMed Web of Science ®Google Scholar
• Pandey RR, Tokuzawa Y, Yang Z, et al. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice. Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16492–16497.
   PubMed Web of Science ®Google Scholar
• Manakov SA, Pezic D, Marinov GK, et al. MIWI2 and MILI have differential effects on piRNA biogenesis and DNA methylation. Cell Rep. 2015 Aug 25;12(8):1234–1243.
   PubMed Web of Science ®Google Scholar
• Ding D, Liu J, Dong K, et al. PNLDC1 is essential for piRNA 3ʹ end trimming and transposon silencing during spermatogenesis in mice. Nat Commun. 2017 Oct 10;8(1):819.
   PubMedGoogle Scholar
• Lim SL, Qu ZP, Kortschak RD, et al. HENMT1 and piRNA stability are required for adult male germ cell transposon repression and to define the spermatogenic program in the mouse. PLoS Genet. 2015 Oct;11(10):e1005620.
   PubMed Web of Science ®Google Scholar
• Wang M, Liu X, Chang G, et al. Single-cell RNA sequencing analysis reveals sequential cell fate transition during human spermatogenesis. Cell Stem Cell. 2018 Oct 4;23(4):599–614 e4.
   PubMed Web of Science ®Google Scholar
• Mihola O, Trachtulec Z, Vlcek C, et al. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 2009 Jan 16;323(5912):373–375.
   PubMed Web of Science ®Google Scholar
• Davies B, Hatton E, Altemose N, et al. Re-engineering the zinc fingers of PRDM9 reverses hybrid sterility in mice. Nature. 2016 Feb 11;530(7589):171–176.
   PubMed Web of Science ®Google Scholar
• Hedges DJ, Deininger PL. Inviting instability: transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat Res. 2007 Mar 1;616(1–2):46–59.
   PubMed Web of Science ®Google Scholar
• Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012 Nov 1;26(21):2361–2373.
   PubMed Web of Science ®Google Scholar
• Vourekas A, Zheng Q, Alexiou P, et al. Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol. 2012 Aug;19(8):773–781.
   PubMed Web of Science ®Google Scholar
• Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell. 2002 Jun;2(6):819–830.
   PubMed Web of Science ®Google Scholar
• Kuramochi-Miyagawa S, Kimura T, Ijiri TW, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development. 2004 Feb;131(4):839–849.
   PubMed Web of Science ®Google Scholar
• Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011 Jun 1;27(11):1571–1572.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012 Mar 4;9(4):357–359.
   PubMed Web of Science ®Google Scholar
• Feng H, Conneely KN, Wu H. A Bayesian hierarchical model to detect differentially methylated loci from single nucleotide resolution sequencing data. Nucleic Acids Res. 2014 Apr;42(8):e69.
   PubMed Web of Science ®Google Scholar
• Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57.
   PubMed Web of Science ®Google Scholar
• Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
   PubMed Web of Science ®Google Scholar
• Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
   PubMed Web of Science ®Google Scholar
• Wang J, Zhang P, Lu Y, et al. piRBase: a comprehensive database of piRNA sequences. Nucleic Acids Res. 2019 Jan 8;47(D1):D175–D180.
   PubMed Web of Science ®Google Scholar
• Wu Y, Zhang WX, Zuo F, et al. Comparison of mRNA expression from Y-chromosome X-degenerate region genes in taurine cattle, yaks and interspecific hybrid bulls. Animal genetics. 2019 Dec;50(6):740-743.
   Google Scholar