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Home / Equine Research Bank / Sci Rep / Identification of piRNAs and piRNA clusters in the testes of...
Scientific reports2019; 9(1); 5022; doi: 10.1038/s41598-019-41475-9

Identification of piRNAs and piRNA clusters in the testes of the Mongolian horse.

Abstract: P-element induced wimpy testis-interacting RNAs (piRNAs) are essential for testicular development and spermatogenesis in mammals. Comparative analyses of the molecular mechanisms of spermatogenesis among different organisms are therefore dependent on accurate characterizations of piRNAs. At present, little is known of piRNAs in non-model organisms. Here, we characterize piRNAs in the Mongolian horse, a hardy breed that reproduces under extreme circumstances. A thorough understanding of spermatogenesis and reproduction in this breed may provide insights for the improvement of fecundity and reproductive success in other breeds. We identified 4,936,717 piRNAs and 7,890 piRNA clusters across both testicular developmental stages. Of these, 2,236,377 putative piRNAs were expressed in the mature samples only, and 2,391,271 putative piRNAs were expressed in the immature samples only. Approximately 3,016 piRNA clusters were upregulated in the mature testes as compared to the immature testes, and 4,874 piRNA clusters were downregulated. Functional and pathway analyses indicated that the candidate generating genes of the predicted piRNAs were likely involved in testicular development and spermatogenesis. Our results thus provide information about differential expression patterns in genes associated with testicular development and spermatogenesis in a non-model animal.
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Publication Date: 2019-03-22 PubMed ID: 30903011PubMed Central: PMC6430771DOI: 10.1038/s41598-019-41475-9Google Scholar: Lookup
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  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research explores the presence and role of P-element induced wimpy testis-interacting RNAs (piRNAs) in the testicular development and spermatogenesis of the Mongolian horse. Researchers identified almost 5 million piRNAs and close to 8,000 piRNA clusters, revealing a correlation between these components and the process of testicular maturation and sperm production.

Understanding piRNAs and Their Roles

  • PiRNAs, or P-element induced wimpy testis-interacting RNAs, play critical roles in mammalian reproduction, specifically in the context of testicular development and spermatogenesis (the production of sperm).
  • Despite their importance, the presence and character of piRNAs in non-model organisms, like the Mongolian horse studied in this research, are not well understood.
  • There is an evident need for more widespread and comparative analyses of piRNA roles in sperm production across different species to better understand their functional importance and intricacies.

Study of Mongolian Horse

  • The Mongolian horse was the focal point of this research primarily because of its cultivation in extreme environmental conditions, which presents a unique opportunity to study aspects of hardiness in reproduction.
  • By studying piRNAs in the Mongolian horse, the researchers aimed to advance the general understanding of spermatogenesis and other reproductive traits and use this knowledge to improve reproductive success in other animal breeds.

Findings and Implications

  • Researchers discovered, in total, close to 5 million piRNAs and about 8,000 piRNA clusters across different testicular development stages.
  • They also found a differential expression of certain piRNAs between mature and immature testicular samples, indicating that these RNAs are actively involved in the maturation and development process of the testes.
  • Similarly, the upregulation of approximately 3,000 piRNA clusters in mature testes, compared to immature ones, indicated the active involvement of piRNAs in the maturation process.
  • The downregulation of about 4,874 piRNA clusters also suggests their active role in the fading of processes as the testes mature.
  • Through functional and pathway analyses, the research established that the genes generating these predicted piRNAs are probably involved in from testicular development and spermatogenesis, hence confirming their crucial role in these processes.
  • The differential expression pattern of genes associated with testicular development and spermatogenesis in this non-model organism can provide valuable information for continued research in this field.

Cite This Article

APA
Li B, He X, Zhao Y, Bai D, Bou G, Zhang X, Su S, Dao L, Liu R, Wang Y, Manglai D. (2019). Identification of piRNAs and piRNA clusters in the testes of the Mongolian horse. Sci Rep, 9(1), 5022. https://doi.org/10.1038/s41598-019-41475-9

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 5022

Researcher Affiliations

Li, Bei
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
He, Xiaolong
  • Inner Mongolia Academy of Agricultural and Animal Husbandry Sciences, Hohhot, 010031, P. R. China.
Zhao, Yiping
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Bai, Dongyi
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Bou, Gerelchimeg
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Zhang, Xinzhuang
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Su, Shaofeng
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Dao, Leng
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Liu, Rui
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Wang, Yuejiao
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China.
Manglai, Dugarjaviin
  • College of animal science, Inner Mongolia Key Laboratory of Equine Genetics, Breeding and Reproduction, Scientific Observing and Experimental Station of Equine Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Equine Research Center, Inner Mongolia Agricultural University, Hohhot, 010018, China. dmanglai@163.com.

MeSH Terms

  • Animals
  • Breeding
  • China
  • Fertility / genetics
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Developmental
  • Gene Ontology
  • Horses / genetics
  • Horses / growth & development
  • Male
  • Multigene Family
  • RNA, Small Interfering / genetics
  • Signal Transduction / genetics
  • Spermatogenesis / genetics
  • Testis / growth & development
  • Testis / metabolism

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 72 references
  1. Aravin A. A novel class of small RNAs bind to MILI protein in mouse testes.. Nature 2006;442:203–207.
    doi: 10.1038/nature04916pubmed: 16751777google scholar: lookup
  2. Girard ASR, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins.. Nature 2006;442:199–202.
    doi: 10.1038/nature04917pubmed: 16751776google scholar: lookup
  3. Grivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells.. Genes & Development 2006;20:1709–1714.
    doi: 10.1101/gad.1434406pmc: PMC1522066pubmed: 16766680google scholar: lookup
  4. Lau NC. Characterization of the piRNA complex from rat testes.. Science 2006;313:363–367.
    doi: 10.1126/science.1130164pubmed: 16778019google scholar: lookup
  5. Rosenkranz DZH. proTRAC - a software for probabilistic piRNA cluster detection, visualization and analysis.. Bmc Bioinformatics 2012;13:5.
    doi: 10.1186/1471-2105-13-5pmc: PMC3293768pubmed: 22233380google scholar: lookup
  6. David R. piRNA cluster database: a web resource for piRNA producing loci.. Nucleic Acids Res 2016;44:D223–230.
    doi: 10.1093/nar/gkw011pmc: PMC4702893pubmed: 26582915google scholar: lookup
  7. Kim VN. Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes.. Genes & Development 2006;20:1993–1997.
    doi: 10.1101/gad.1456106pubmed: 16882976google scholar: lookup
  8. Watanabe T. 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 & Development 2006;20:1732–1743.
    doi: 10.1101/gad.1425706pmc: PMC1522070pubmed: 16766679google scholar: lookup
  9. Gou LT. Ubiquitination-Deficient Mutations in Human Piwi Cause Male Infertility by Impairing Histone-to-Protamine Exchange during Spermiogenesis.. Cell 2017;169:1090–1104.
    doi: 10.1016/j.cell.2017.04.034pmc: PMC5985145pubmed: 28552346google scholar: lookup
  10. Gou LT. Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis.. Cell Res 2014;24:680–700.
    doi: 10.1038/cr.2014.41pmc: PMC4042167pubmed: 24787618google scholar: lookup
  11. Deng W. Miwi, a Murine Homolog of piwi, Encodes a Cytoplasmic Protein Essential for Spermatogenesis.. Dev Cell 2002;2:819–830.
    doi: 10.1016/S1534-5807(02)00165-Xpubmed: 12062093google scholar: lookup
  12. Kotaja N. The chromatoid body: a germ-cell-specific RNA-processing centre.. Nat Rev Mol Cell Biol 2007;8:85–90.
    doi: 10.1038/nrm2081pubmed: 17183363google scholar: lookup
  13. Onohara YFT, Yasukochi T, Himeno M, Yokota S. Localization of mouse vasa homolog protein in chromatoid body and related nuage structures of mammalian spermatogenic cells during spermatogenesis.. Histochem Cell Biol 2010;133:627–639.
    doi: 10.1007/s00418-010-0699-5pubmed: 20401665google scholar: lookup
  14. Siomi MC, Sato K, Pezic D, Aravin AA. PIWI-interacting small RNAs: the vanguard of genome defence.. Nat Rev Mol Cell Biol 2011;12:246–258.
    doi: 10.1038/nrm3089pubmed: 21427766google scholar: lookup
  15. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally Regulated piRNA Clusters Implicate MILI in Transposon Control.. Science 2007;316:744–747.
    doi: 10.1126/science.1142612pubmed: 17446352google scholar: lookup
  16. Aravin AA, Hannon GJ. Small RNA Silencing Pathways in Germ and Stem Cells.. Cold Spring Harbor Symposia on Quantitative Biology 2009;73:283–290.
    doi: 10.1101/sqb.2008.73.058pubmed: 19270082google scholar: lookup
  17. Bjørnstad G, Nilsen NØ, Røed KH. Genetic relationship between Mongolian and Norwegian horses?. Anim Genet 2003;34:55–58.
    doi: 10.1046/j.1365-2052.2003.00922.xpubmed: 12580788google scholar: lookup
  18. Huang JZY. Analysis of horse genomes provides insight into the diversification and adaptive evolution of karyotype.. Sci Rep 2014;4:4958.
    doi: 10.1038/srep04958pmc: PMC4021364pubmed: 24828444google scholar: lookup
  19. Kefena EM. Discordances between morphological systematics and molecular taxonomy in the stem line of equids: A review of the case of taxonomy of genus Equus.. Livestock Science 2012;143:105–115.
    doi: 10.1016/j.livsci.2011.09.017google scholar: lookup
  20. Johnson L, Varner DD, Jr TD. Effect of age and season on the establishment of spermatogenesis in the horse.. Journal of Reproduction & Fertility Supplement 1991;44:87.
    pubmed: 1795306
  21. Naden J, Amann RP, Squires EL. Testicular growth, hormone concentrations, seminal characteristics and sexual behaviour in stallions.. Journal of Reproduction & Fertility 1990;88:167.
    doi: 10.1530/jrf.0.0880167pubmed: 2107299google scholar: lookup
  22. Sai Lakshmi S, Agrawal S. piRNABank: a web resource on classified and clustered Piwi-interacting RNAs.. Nucleic Acids Research 2008;36:D173–D177.
    doi: 10.1093/nar/gkm696pmc: PMC2238943pubmed: 17881367google scholar: lookup
  23. Zhang Y, Wang X, Kang L. A k-mer scheme to predict piRNAs and characterize locust piRNAs.. Bioinformatics 2011;27:771–776.
    doi: 10.1093/bioinformatics/btr016pmc: PMC3051322pubmed: 21224287google scholar: lookup
  24. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.. Genome Biology 2009;10:R25.
    doi: 10.1186/gb-2009-10-3-r25pmc: PMC2690996pubmed: 19261174google scholar: lookup
  25. Young MD, Wakefield MJ, Smyth GK, Oshlack. goseq: Gene Ontology testing for RNA-seq datasets.. Research Gate 2010;1–21.
  26. Kanehisa M. KEGG for linking genomes to life and the environment.. Nucleic Acids Res 2008;36.
    pmc: PMC2238879pubmed: 18077471
  27. Anders S. Differential expression analysis for sequence count data.. Genome Biology 2010;11:R106.
    doi: 10.1186/gb-2010-11-10-r106pmc: PMC3218662pubmed: 20979621google scholar: lookup
  28. Anders S H W. Differential expression of RNA-Seq data at the gene level.. EMBL 2013.
  29. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data.. Bioinformatics 2010;26:136–138.
    doi: 10.1093/bioinformatics/btp612pubmed: 19855105google scholar: lookup
  30. Xiang M. U6 is not a suitable endogenous control for the quantification of circulating microRNAs.. Biochem Biophys Res Commun 2014;454:210–214.
    doi: 10.1016/j.bbrc.2014.10.064pubmed: 25450382google scholar: lookup
  31. Livak KJ. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.. Methods 2001;25:402–408.
    doi: 10.1006/meth.2001.1262pubmed: 11846609google scholar: lookup
  32. Aravin AA. The Small RNA Profile during Drosophila melanogaster Development.. Developmental Cell 2003;5:337–350.
    doi: 10.1016/S1534-5807(03)00228-4pubmed: 12919683google scholar: lookup
  33. Brennecke J. Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila.. Cell 2007;128:1089–1103.
    doi: 10.1016/j.cell.2007.01.043pubmed: 17346786google scholar: lookup
  34. Gunawardane LS. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila.. Science 2007;315:1587–1590.
    doi: 10.1126/science.1140494pubmed: 17322028google scholar: lookup
  35. Houwing S. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish.. Cell 2007;129:69–82.
    doi: 10.1016/j.cell.2007.03.026pubmed: 17418787google scholar: lookup
  36. Mi Shijun CT. Sorting of Small RNAs into Arabidopsis Argonaute Complexes Is Directed by the 5′ Terminal Nucleotide.. Cell 2005;133:116–127.
    pmc: PMC2981139pubmed: 18342361
  37. Carmell MA, Xuan Z, Zhang MQ, Hannon GJ. The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis.. Genes Dev 2002;16:2733–2742.
    doi: 10.1101/gad.1026102pubmed: 12414724google scholar: lookup
  38. Klattenhoff C, Theurkauf W. Biogenesis and germline functions of piRNAs.. Development 2007;135:3–9.
    doi: 10.1242/dev.006486pubmed: 18032451google scholar: lookup
  39. Frank FSN, Nagar B. Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2.. Nature 2010;465:818–822.
    doi: 10.1038/nature09039pubmed: 20505670google scholar: lookup
  40. Chu CY. Small RNAs: regulators and guardians of the genome.. Journal of Cellular Physiology 2010;213:412–419.
    doi: 10.1002/jcp.21230pubmed: 17674365google scholar: lookup
  41. Lazaros L. The association of aromatase (CYP19) gene variants with sperm concentration and motility.. Asian J Androl 2011;13:292–297.
    doi: 10.1038/aja.2010.144pmc: PMC3739188pubmed: 21217768google scholar: lookup
  42. Yang Qingling. MicroRNA and piRNA Profiles in Normal Human Testis Detected by Next Generation Sequencing.. PLoS ONE 2013;8:e66809.
    doi: 10.1371/journal.pone.0066809pmc: PMC3691314pubmed: 23826142google scholar: lookup
  43. Schmid R. The splicing landscape is globally reprogrammed during male meiosis.. Nucleic Acids Res 2013;41:10170–10184.
    doi: 10.1093/nar/gkt811pmc: PMC3905889pubmed: 24038356google scholar: lookup
  44. Flannigan R. Large scale miRNA and piRNA sequencing analysis of testis biopsies from fertile an infertile men reveals differences between miRNA and piRNA expression during spermatogenesis cycle.. Fertility and Sterility 2017;108:e312.
  45. Meister G. Identification of novel argonaute-associated proteins.. Curr Biol 2005;15:2149–2155.
    doi: 10.1016/j.cub.2005.10.048pubmed: 16289642google scholar: lookup
  46. Janowski BA. Involvement of AGO1 and AGO2 in mammalian transcriptional silencing.. Nature Structural & Molecular Biology 2006;13(9):787–792.
    pubmed: 16936728
  47. Wu Ligang, Fan Jihua, Belasco Joel G. Importance of Translation and Nonnucleolytic Ago Proteins for On-Target RNA Interference.. Current Biology 2008;18:1327–1332.
    doi: 10.1016/j.cub.2008.07.072pmc: PMC3690557pubmed: 18771919google scholar: lookup
  48. Stry MV. Enhanced Susceptibility of Ago1/3 Double-Null Mice to Influenza A Virus Infection.. Journal of Virology 2012;86(8):4151–4157.
    pmc: PMC3318639pubmed: 22318144
  49. Russell SJ. Identification of PIWIL1 Isoforms and Their Expression in Bovine Testes, Oocytes, and Early Embryos.. Biol Reprod 2016;94:75.
    doi: 10.1095/biolreprod.115.136721pubmed: 26911426google scholar: lookup
  50. Xu L. Piwil1 mediates meiosis during spermatogenesis in chicken.. Anim Reprod Sci 2016;166.
    pubmed: 26811260
  51. Chang G. DNA methylation and NF-Y regulate Piwil1 expression during chicken spermatogenesis.. Anim Reprod Sci 2015;162:95–103.
    doi: 10.1016/j.anireprosci.2015.09.016pubmed: 26471838google scholar: lookup
  52. Kuramochi-Miyagawa S. Two mouse piwi-related genes: miwi and mili.. Mech Dev 2001;108:121–133.
    doi: 10.1016/S0925-4773(01)00499-3pubmed: 11578866google scholar: lookup
  53. Thomson T, Lin H. The Biogenesis and Function of PIWI Proteins and piRNAs: Progress and Prospect.. Annual Review of Cell and Developmental Biology 2009;25:355–376.
    doi: 10.1146/annurev.cellbio.24.110707.175327pmc: PMC2780330pubmed: 19575643google scholar: lookup
  54. Gomes Fernandes M. Human-specific subcellular compartmentalization of P-element induced wimpy testis-like (PIWIL) granules during germ cell development and spermatogenesis.. Hum Reprod 2018;33:258–269.
    doi: 10.1093/humrep/dex365pmc: PMC5850288pubmed: 29237021google scholar: lookup
  55. Lee JH, Engel W, Nayernia K. Stem cell protein Piwil2 modulates expression of murine spermatogonial stem cell expressed genes.. Mol Reprod Dev 2006;73:173–179.
    doi: 10.1002/mrd.20391pubmed: 16261612google scholar: lookup
  56. Aravin AA. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice.. Mol Cell 2008;31:785–799.
    doi: 10.1016/j.molcel.2008.09.003pmc: PMC2730041pubmed: 18922463google scholar: lookup
  57. Unhavaithaya Y. H. MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation.. J Biol Chem 2009;284:6507–6519.
    doi: 10.1074/jbc.M809104200pmc: PMC2649106pubmed: 19114715google scholar: lookup
  58. Yang Z. PIWI Slicing and EXD1 Drive Biogenesis of Nuclear piRNAs from Cytosolic Targets of the Mouse piRNA Pathway.. Mol Cell 2016;61:138–152.
    doi: 10.1016/j.molcel.2015.11.009pmc: PMC4712191pubmed: 26669262google scholar: lookup
  59. Sato KIY, Siomi H, Siomi MC. Tudor-domain containing proteins act to make the piRNA pathways more robust in Drosophila.. Fly (Austin) 2015;9:86–90.
    doi: 10.1080/19336934.2015.1128599pmc: PMC4826119pubmed: 26647059google scholar: lookup
  60. Pandey RR. Tudor domain containing 12 (TDRD12) is essential for secondary PIWI interacting RNA biogenesis in mice.. Proc Natl Acad Sci USA 2013;110:16492–16497.
    doi: 10.1073/pnas.1316316110pmc: PMC3799322pubmed: 24067652google scholar: lookup
  61. Ishizuka M. Abnormal spermatogenesis and male infertility in testicular zinc finger protein Zfp318-knockout mice.. Dev Growth Differ 2016;58:600–608.
    doi: 10.1111/dgd.12301pmc: PMC11520953pubmed: 27385512google scholar: lookup
  62. Katayama KYH, Tochigi Y, Suzuki H. The microtubule-associated protein astrin transgenesis rescues spermatogenesis and renal function in hypogonadic (hgn/hgn) rats.. Andrology 2013;1:301–307.
    doi: 10.1111/j.2047-2927.2012.00032.xpubmed: 23413142google scholar: lookup
  63. Huo S, Du W, Shi P, Si Y, Zhao S. The role of spermatogenesis-associated protein 6 in testicular germ cell tumors.. Int J Clin Exp Pathol 2015;8:9119–9125.
    pmc: PMC4583887pubmed: 26464655
  64. Wu H. Sperm associated antigen 8 (SPAG8), a novel regulator of activator of CREM in testis during spermatogenesis.. FEBS Lett 2010;584:2807–2815.
    doi: 10.1016/j.febslet.2010.05.016pubmed: 20488182google scholar: lookup
  65. Kirino Y. Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability.. Nature Cell Biology 2009;11:652–658.
    doi: 10.1038/ncb1872pmc: PMC2746449pubmed: 19377467google scholar: lookup
  66. Kawaoka S. A role for transcription from a piRNA cluster in de novo piRNA production.. Rna 2011;18:265–273.
    doi: 10.1261/rna.029777.111pmc: PMC3264913pubmed: 22194309google scholar: lookup
  67. Vagin VV. A Distinct Small RNA Pathway Silences Selfish Genetic Elements in the Germline.. Science 2006;313:320–324.
    doi: 10.1126/science.1129333pubmed: 16809489google scholar: lookup
  68. Pantano L. The small RNA content of human sperm reveals pseudogene-derived piRNAs complementary to protein-coding genes.. Rna 2015;21:1085–1095.
    doi: 10.1261/rna.046482.114pmc: PMC4436662pubmed: 25904136google scholar: lookup
  69. Antoniewski C, Gebert D, Ketting RF, Zischler H, Rosenkranz D. piRNAs from Pig Testis Provide Evidence for a Conserved Role of the Piwi Pathway in Post-Transcriptional Gene Regulation in Mammals.. Plos One 2015;10:e0124860.
    doi: 10.1371/journal.pone.0124860pmc: PMC4423968pubmed: 25950437google scholar: lookup
  70. Kirino Y, Mourelatos Z. Mouse Piwi-interacting RNAs are 2′-O-methylated at their 3′ termini.. Nature Structural & Molecular Biology 2007;14:347–348.
    doi: 10.1038/nsmb1218pubmed: 17384647google scholar: lookup
  71. Srayko M, Buster DW, Bazirgan OA, McNally FJ, Mains PE. MEI-1/MEI-2katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis.. Genes Dev 2000;14:1072–1084.
    pmc: PMC316576pubmed: 10809666
  72. Yang HY, McNally K, McNally FJ. MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C elegans.. Dev Biol 2003;260:245–259.
    doi: 10.1016/S0012-1606(03)00216-1pubmed: 12885567google scholar: lookup
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