Correction to: HENMT1 and piRNA Stability Are Required for Adult Male Germ Cell Transposon Repression and to Define the Spermatogenic Program in the Mouse (PLoS Genet, 11, 10, e1005620, 10.1371/journal.pgen.1005620);HENMT1 and piRNA Stability Are Required for Adult Male Germ Cell Transposon Repression and to Define the Spermatogenic Program in the Mouse

PLoS Genetics

Volumn 11, Issue 10, 2015, Pages

  Lim, Shu Ly ^a   Qu, Zhi Peng ^b   Kortschak, R Daniel ^b   Lawrence, David M ^c   Geoghegan, Joel ^c   Hempfling, Anna Lena ^a,d   Bergmann, Martin ^d   Goodnow, Christopher C ^e   Ormandy, Christopher J ^f   Wong, Lee ^a   Mann, Jeff ^g   Scott, Hamish S ^b,c,h   Jamsai, Duangporn ^a   Adelson, David L ^b   O’Bryan, Moira K ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c Australian Dolphin Research Foundation   (Australia)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

^e Biology and Environment   (Australia)

^f GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g ROYAL CHILDREN'S HOSPITAL   (Australia)

^h CENTRE FOR CANCER BIOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PIWI INTERACTING RNA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CHROMATIN; HENMT1 PROTEIN, MOUSE; METHYLTRANSFERASE; NHLH1 PROTEIN, MOUSE; SMALL INTERFERING RNA; TRANSPOSON;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; GENE REPRESSION; GENETIC TRANSCRIPTION; GERM CELL; HAPLOIDY; HENMT1 GENE; MALE; MALE STERILITY; MOUSE; NONHUMAN; RNA SEQUENCE; RNA STABILITY; SPERM QUALITY; SPERMATOGENESIS; TRANSPOSON; ANIMAL; BIOSYNTHESIS; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALE INFERTILITY; PATHOLOGY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CHROMATIN; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; HUMANS; INFERTILITY, MALE; MALE; METHYLTRANSFERASES; MICE; RNA STABILITY; RNA, SMALL INTERFERING; SPERMATOGENESIS;

EID: 84946600989     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005782     Document Type: Erratum

References (79)

1. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, et al. (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522–535. doi: 10.1016/j.cell.2009.03.040 19395010
2. Kazazian HH, Jr. (2004) Mobile elements: drivers of genome evolution. Science 303: 1626–1632. 15016989
3. Kirino Y, Mourelatos Z, (2007) Mouse Piwi-interacting RNAs are 2'-O-methylated at their 3' termini. Nat Struct Mol Biol 14: 347–348. 17384647
4. Robine N, Lau NC, Balla S, Jin Z, Okamura K, et al. (2009) A broadly conserved pathway generates 3'UTR-directed primary piRNAs. Curr Biol 19: 2066–2076. doi: 10.1016/j.cub.2009.11.064 20022248
5. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203–207. 16751777
6. Girard A, Sachidanandam R, Hannon GJ, Carmell MA, (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199–202. 16751776
7. Siomi MC, Sato K, Pezic D, Aravin AA, (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246–258. doi: 10.1038/nrm3089 21427766
8. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ, (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744–747. 17446352
9. De Fazio S, Bartonicek N, Di Giacomo M, Abreu-Goodger C, Sankar A, et al. (2011) The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 480: 259–263. doi: 10.1038/nature10547 22020280
10. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, et al. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12: 503–514. 17395546
11. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, et al. (2011) Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480: 264–267. doi: 10.1038/nature10672 22121019
12. Beyret E, Lin H, (2011) Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. Dev Biol 355: 215–226. doi: 10.1016/j.ydbio.2011.04.021 21539824
13. Handler D, Meixner K, Pizka M, Lauss K, Schmied C, et al. (2013) The genetic makeup of the Drosophila piRNA pathway. Mol Cell 50: 762–777. doi: 10.1016/j.molcel.2013.04.031 23665231
14. Ipsaro JJ, Haase AD, Knott SR, Joshua-Tor L, Hannon GJ, (2012) The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 491: 279–283. doi: 10.1038/nature11502 23064227
15. Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, et al. (2012) Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491: 284–287. doi: 10.1038/nature11509 23064230
16. Watanabe T, Chuma S, Yamamoto Y, Kuramochi-Miyagawa S, Totoki Y, et al. (2011) MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev Cell 20: 364–375. doi: 10.1016/j.devcel.2011.01.005 21397847
17. Huang H, Gao Q, Peng X, Choi SY, Sarma K, et al. (2011) piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev Cell 20: 376–387. doi: 10.1016/j.devcel.2011.01.004 21397848
18. Billi AC, Alessi AF, Khivansara V, Han T, Freeberg M, et al. (2012) The Caenorhabditis elegans HEN1 ortholog, HENN-1, methylates and stabilizes select subclasses of germline small RNAs. PLoS Genet 8: e1002617. doi: 10.1371/journal.pgen.1002617 22548001
19. Huang RH, (2012) Unique 2'-O-methylation by Hen1 in eukaryotic RNA interference and bacterial RNA repair. Biochemistry 51: 4087–4095. doi: 10.1021/bi300497x 22564049
20. Ohara T, Sakaguchi Y, Suzuki T, Ueda H, Miyauchi K, et al. (2007) The 3' termini of mouse Piwi-interacting RNAs are 2'-O-methylated. Nat Struct Mol Biol 14: 349–350. 17384646
21. Kirino Y, Mourelatos Z, (2007) The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA 13: 1397–1401. 17652135
22. Horwich MD, Li C, Matranga C, Vagin V, Farley G, et al. (2007) The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 17: 1265–1272. 17604629
23. Saito K, Sakaguchi Y, Suzuki T, Suzuki T, Siomi H, et al. (2007) Pimet, the Drosophila homolog of HEN1, mediates 2'-O-methylation of Piwi- interacting RNAs at their 3' ends. Genes Dev 21: 1603–1608. 17606638
24. Kamminga LM, Luteijn MJ, den Broeder MJ, Redl S, Kaaij LJ, et al. (2010) Hen1 is required for oocyte development and piRNA stability in zebrafish. EMBO J 29: 3688–3700. doi: 10.1038/emboj.2010.233 20859253
25. Kirino Y, Mourelatos Z, (2007) 2'-O-methyl modification in mouse piRNAs and its methylase. Nucleic Acids Symp Ser (Oxf): 417–418.
26. Baker G, Barak S (2012) Clinical Management of Male Infertility. wwwENDOTEXTorg Chapter 7: MDTEXT.COM.Inc, South Dartmouth, MA, USA.
27. Kierszenbaum AL, Rivkin E, Tres LL, (2007) Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 65: 33–43. 17644953
28. Meikar O, Da Ros M, Korhonen H, Kotaja N, (2011) Chromatoid body and small RNAs in male germ cells. Reproduction 142: 195–209. doi: 10.1530/REP-11-0057 21652638
29. Alefelder S, Patel BK, Eckstein F, (1998) Incorporation of terminal phosphorothioates into oligonucleotides. Nucleic Acids Res 26: 4983–4988. 9776763
30. Martin M, (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17.
31. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168
32. Gan H, Lin X, Zhang Z, Zhang W, Liao S, et al. (2011) piRNA profiling during specific stages of mouse spermatogenesis. RNA 17: 1191–1203. doi: 10.1261/rna.2648411 21602304
33. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, et al. (2012) Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol 19: 773–781. doi: 10.1038/nsmb.2347 22842725
34. Axtell MJ, (2013) ShortStack: comprehensive annotation and quantification of small RNA genes. RNA 19: 740–751. doi: 10.1261/rna.035279.112 23610128
35. Antoniewski C, (2014) Computing siRNA and piRNA overlap signatures. Methods Mol Biol 1173: 135–146. doi: 10.1007/978-1-4939-0931-5_12 24920366
36. Zhang Z, Xu J, Koppetsch BS, Wang J, Tipping C, et al. (2011) Heterotypic piRNA Ping-Pong requires qin, a protein with both E3 ligase and Tudor domains. Mol Cell 44: 572–584. doi: 10.1016/j.molcel.2011.10.011 22099305
37. Weick EM, Miska EA, (2014) piRNAs: from biogenesis to function. Development 141: 3458–3471. doi: 10.1242/dev.094037 25183868
38. Ibrahim F, Rymarquis LA, Kim EJ, Becker J, Balassa E, et al. (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc Natl Acad Sci U S A 107: 3906–3911. doi: 10.1073/pnas.0912632107 20142471
39. Sement FM, Ferrier E, Zuber H, Merret R, Alioua M, et al. (2013) Uridylation prevents 3' trimming of oligoadenylated mRNAs. Nucleic Acids Res 41: 7115–7127. doi: 10.1093/nar/gkt465 23748567
40. Luteijn MJ, Ketting RF, (2013) PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat Rev Genet 14: 523–534. doi: 10.1038/nrg3495 23797853
41. Simon B, Kirkpatrick JP, Eckhardt S, Reuter M, Rocha EA, et al. (2011) Recognition of 2'-O-methylated 3'-end of piRNA by the PAZ domain of a Piwi protein. Structure 19: 172–180. doi: 10.1016/j.str.2010.11.015 21237665
42. Soper SF, van der Heijden GW, Hardiman TC, Goodheart M, Martin SL, et al. (2008) Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15: 285–297. doi: 10.1016/j.devcel.2008.05.015 18694567
43. Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, et al. (2010) 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 107: 11841–11846. doi: 10.1073/pnas.1003953107 20534472
44. Gasior SL, Wakeman TP, Xu B, Deininger PL, (2006) The human LINE-1 retrotransposon creates DNA double-strand breaks. J Mol Biol 357: 1383–1393. 16490214
45. Di Giacomo M, Comazzetto S, Saini H, De Fazio S, Carrieri C, et al. (2013) Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol Cell 50: 601–608. doi: 10.1016/j.molcel.2013.04.026 23706823
46. Sasaki H, Matsui Y, (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9: 129–140. doi: 10.1038/nrg2295 18197165
47. Zheng K, Wang PJ, (2012) Blockade of pachytene piRNA biogenesis reveals a novel requirement for maintaining post-meiotic germline genome integrity. PLoS Genet 8: e1003038. doi: 10.1371/journal.pgen.1003038 23166510
48. Gou LT, Dai P, Yang JH, Xue Y, Hu YP, et al. (2014) Pachytene piRNAs instruct massive mRNA elimination during late spermiogenesis. Cell Res 24: 680–700. doi: 10.1038/cr.2014.41 24787618
49. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308
50. Aleem M, Padwal V, Choudhari J, Balasinor N, Gill-Sharma MK, (2008) Sperm protamine levels as indicators of fertilising potential in sexually mature male rats. Andrologia 40: 29–37. doi: 10.1111/j.1439-0272.2008.00805.x 18211299
51. Shirley CR, Hayashi S, Mounsey S, Yanagimachi R, Meistrich ML, (2004) Abnormalities and reduced reproductive potential of sperm from Tnp1- and Tnp2-null double mutant mice. Biol Reprod 71: 1220–1229. 15189834
52. Steger K, Wilhelm J, Konrad L, Stalf T, Greb R, et al. (2008) Both protamine-1 to protamine-2 mRNA ratio and Bcl2 mRNA content in testicular spermatids and ejaculated spermatozoa discriminate between fertile and infertile men. Hum Reprod 23: 11–16. 18003625
53. Zheng H, Stratton CJ, Morozumi K, Jin J, Yanagimachi R, et al. (2007) Lack of Spem1 causes aberrant cytoplasm removal, sperm deformation, and male infertility. Proc Natl Acad Sci U S A 104: 6852–6857. 17426145
54. Fajardo MA, Haugen HS, Clegg CH, Braun RE, (1997) Separate elements in the 3' untranslated region of the mouse protamine 1 mRNA regulate translational repression and activation during murine spermatogenesis. Dev Biol 191: 42–52. 9356170
55. Steger K, (2001) Haploid spermatids exhibit translationally repressed mRNAs. Anat Embryol (Berl) 203: 323–334.
56. Aravin AA, Hannon GJ, Brennecke J, (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761–764. 17975059
57. Bourc'his D, Bestor TH, (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96–99. 15318244
58. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, et al. (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908–917. doi: 10.1101/gad.1640708 18381894
59. Webster KE, O'Bryan MK, Fletcher S, Crewther PE, Aapola U, et al. (2005) Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci U S A 102: 4068–4073. 15753313
60. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, et al. (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27: 390–399. doi: 10.1101/gad.209841.112 23392610
61. Deng W, Lin H, (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819–830. 12062093
62. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, et al. (2014) Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17: 667–669. doi: 10.1038/nn.3695 24728267
63. Jamsai D, O'Bryan MK, (2010) Genome-wide ENU mutagenesis for the discovery of novel male fertility regulators. Syst Biol Reprod Med 56: 246–259. doi: 10.3109/19396361003706424 20536324
64. O'Donnell L, Rhodes D, Smith SJ, Merriner DJ, Clark BJ, et al. (2012) An essential role for katanin p80 and microtubule severing in male gamete production. PLoS Genet 8: e1002698. doi: 10.1371/journal.pgen.1002698 22654669
65. Borg CL, Wolski KM, Gibbs GM, O'Bryan MK, (2010) Phenotyping male infertility in the mouse: how to get the most out of a 'non-performer'. Hum Reprod Update 16: 205–224. doi: 10.1093/humupd/dmp032 19758979
66. Cotton L, Gibbs GM, Sanchez-Partida LG, Morrison JR, de Kretser DM, et al. (2006) FGFR-1 [corrected] signaling is involved in spermiogenesis and sperm capacitation. J Cell Sci 119: 75–84. 16352663
67. Gibbs GM, Orta G, Reddy T, Koppers AJ, Martinez-Lopez P, et al. (2011) Cysteine-rich secretory protein 4 is an inhibitor of transient receptor potential M8 with a role in establishing sperm function. Proc Natl Acad Sci U S A 108: 7034–7039. doi: 10.1073/pnas.1015935108 21482758
68. Pesch S, Bergmann M, (2006) Structure of mammalian spermatozoa in respect to viability, fertility and cryopreservation. Micron 37: 597–612. 16621580
69. Romrell LJ, Bellve AR, Fawcett DW, (1976) Separation of mouse spermatogenic cells by sedimentation velocity. A morphological characterization. Dev Biol 49: 119–131. 176074
70. Dennis K, Fan T, Geiman T, Yan Q, Muegge K, (2001) Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev 15: 2940–2944. 11711429
71. Lim SL, Tsend-Ayush E, Kortschak RD, Jacob R, Ricciardelli C, et al. (2013) Conservation and Expression of piRNA Pathway Genes in Male and Female Adult Gonad of Amniotes. Biol Reprod.
72. Jamsai D, Bianco DM, Smith SJ, Merriner DJ, Ly-Huynh JD, et al. (2008) Characterization of gametogenetin 1 (GGN1) and its potential role in male fertility through the interaction with the ion channel regulator, cysteine-rich secretory protein 2 (CRISP2) in the sperm tail. Reproduction 135: 751–759. doi: 10.1530/REP-07-0485 18502891
73. Heidaran MA, Showman RM, Kistler WS, (1988) A cytochemical study of the transcriptional and translational regulation of nuclear transition protein 1 (TP1), a major chromosomal protein of mammalian spermatids. J Cell Biol 106: 1427–1433. 3372585
74. Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, et al. (2004) Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci U S A 101: 16501–16506. 15546993
75. O'Bryan MK, Clark BJ, McLaughlin EA, D'Sylva RJ, O'Donnell L, et al. (2013) RBM5 is a male germ cell splicing factor and is required for spermatid differentiation and male fertility. PLoS Genet 9: e1003628. doi: 10.1371/journal.pgen.1003628 23935508
76. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. 11846609
77. Yang Z, Vilkaitis G, Yu B, Klimasauskas S, Chen X, (2007) Approaches for studying microRNA and small interfering RNA methylation in vitro and in vivo. Methods Enzymol 427: 139–154. 17720483
78. Chang FT, McGhie JD, Chan FL, Tang MC, Anderson MA, et al. (2013) PML bodies provide an important platform for the maintenance of telomeric chromatin integrity in embryonic stem cells. Nucleic Acids Res 41: 4447–4458. doi: 10.1093/nar/gkt114 23444137
79. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36. doi: 10.1186/gb-2013-14-4-r36 23618408