Reduced pachytene piRNAs and translation underlie spermiogenic arrest in Maelstrom mutant mice

EMBO Journal

Volumn 33, Issue 18, 2014, Pages 1999-2019

  Castañeda, Julio ^a,b,c   Genzor, Pavol ^a,b   Van Der Heijden, Godfried W ^b   Sarkeshik, Ali ^c   Yates, John R ^c   Ingolia, Nicholas T ^b,d   Bortvin, Alex ^b,e  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

germ cell; maelstrom; mouse; piRNA; Piwi

Indexed keywords

MESSENGER RNA; PIWI INTERACTING RNA; PIWI PROTEIN; RNA PRECURSOR; DNA BINDING PROTEIN; MAELSTROM PROTEIN, MOUSE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ACROSOME; ADULT; ARTICLE; FLAGELLUM; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PACHYTENE; PHENOTYPE; POLYSOME; PROTEIN PROTEIN INTERACTION; RNA TRANSLATION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; ANIMAL; GENE EXPRESSION REGULATION; GERM CELL; KNOCKOUT MOUSE; MAELSTROM; METABOLISM; MUTATION; PHYSIOLOGY; PIWI; PROTEIN SYNTHESIS; TESTIS;

GERM CELL; MAELSTROM; MOUSE; PIRNA; PIWI;

ANIMALS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; MUTATION; PACHYTENE STAGE; PROTEIN BIOSYNTHESIS; RNA, SMALL INTERFERING; SPERMATIDS; SPERMATOGENESIS; TESTIS; TRANSCRIPTION FACTORS;

EID: 84908179136     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201386855     Document Type: Article

References (87)

1. Abe K, Noce T, (1997) A DEAD-family protein gene, Ddx4, encoding a murine homolog of Drosophila vasa maps to the distal end of mouse chromosome 13. Mamma Genome 8: 622-623
2. Akagi K, Li J, Stephens RM, Volfovsky N, Symer DE, (2008) Extensive variation between inbred mouse strains due to endogenous L1 retrotransposition. Genome Res 18: 869-880
3. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T, (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203-207
4. Aravin AA, Hannon GJ, Brennecke J, (2007a) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764
5. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ, (2007b) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747
6. Aravin AA, Bourc'his D, (2008) Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev 22: 970-975
7. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ, (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799
8. Aravin AA, van der Heijden GW, Castaneda J, Vagin VV, Hannon GJ, Bortvin A, (2009) Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet 5: e1000764
9. Bingham JB, King SJ, Schroer TA, (1998) Purification of dynactin and dynein from brain tissue. Methods Enzymol 298: 171-184
10. Blobel G, Sabatini D, (1971) Dissociation of mammalian polyribosomes into subunits by puromycin. Proc Natl Acad Sci USA 68: 390-394
11. Bourc'his D, Bestor TH, (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96-99
12. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, Hannon GJ, (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12: 503-514
13. Chuma S, Hiyoshi M, Yamamoto A, Hosokawa M, Takamune K, Nakatsuji N, (2003) Mouse Tudor repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech Dev 120: 979-990
14. Chuma S, Hosokawa M, Kitamura K, Kasai S, Fujioka M, Hiyoshi M, Takamune K, Noce T, Nakatsuji N, (2006) Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc Natl Acad Sci USA 103: 15894-15899
15. Clermont Y, Perey B, (1957) The stages of the cycle of the seminiferous epithelium of the rat: practical definitions in PA-Schiff-hematoxylin and hematoxylin-eosin stained sections. Rev Can Biol 16: 451-462
16. Costa Y, Speed RM, Gautier P, Semple CA, Maratou K, Turner JM, Cooke HJ, (2006) Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway? Hum Mol Genet 15: 2324-2334
17. Deng W, Lin H, (2002) Miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830
18. Di Giacomo M, Comazzetto S, Saini H, De Fazio S, Carrieri C, Morgan M, Vasiliauskaite L, Benes V, Enright AJ, O'Carroll D, (2013) Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol Cell 50: 601-608
19. Doetschman T, (2009) Influence of genetic background on genetically engineered mouse phenotypes. Methods Mol Biol 530: 423-433
20. Eaker S, Cobb J, Pyle A, Handel MA, (2002) Meiotic prophase abnormalities and metaphase cell death in MLH1-deficient mouse spermatocytes: insights into regulation of spermatogenic progress. Dev Biol 249: 85-95
21. Edgar R, Domrachev M, Lash AE, (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
22. Findley SD, Tamanaha M, Clegg NJ, Ruohola-Baker H, (2003) Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130: 859-871
23. Fourcroy P, Cuiller S, Largitte FC, Lambert C, (1981) Polyribosome analysis on sucrose gradients produced by the freeze-thaw method. J Biochem Biophys Methods 4: 243-246
24. Girard A, Sachidanandam R, Hannon GJ, Carmell MA, (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202
25. Grivna ST, Beyret E, Wang Z, Lin H, (2006a) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20: 1709-1714
26. Grivna ST, Pyhtila B, Lin H, (2006b) MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci USA 103: 13415-13420
27. van der Heijden GW, Derijck AA, Posfai E, Giele M, Pelczar P, Ramos L, Wansink DG, van der Vlag J, Peters AH, de Boer P, (2007) Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat Genet 39: 251-258
28. van der Heijden GW, Bortvin A, (2009a) Defending the genome in tudor style. Dev Cell 17: 745-746
29. van der Heijden GW, Bortvin A, (2009b) Transient relaxation of transposon silencing at the onset of mammalian meiosis. Epigenetics 4: 76-79
30. Hosokawa M, Shoji M, Kitamura K, Tanaka T, Noce T, Chuma S, Nakatsuji N, (2007) Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev Biol 301: 38-52
31. Huang H, Gao Q, Peng X, Choi SY, Sarma K, Ren H, Morris AJ, Frohman MA, (2011) piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev Cell 20: 376-387
32. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223
33. Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS, (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 7: 1534-1550
34. Ingolia NT, (2014) Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet 15: 205-213
35. 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
36. King SJ, Bonilla M, Rodgers ME, Schroer TA, (2002) Subunit organization in cytoplasmic dynein subcomplexes. Protein Sci 11: 1239-1250
37. Kirino Y, Vourekas A, Sayed N, de Lima Alves F, Thomson T, Lasko P, Rappsilber J, Jongens TA, Mourelatos Z, (2010) Arginine methylation of Aubergine mediates Tudor binding and germ plasm localization. RNA 16: 70-78
38. Kojima K, Kuramochi-Miyagawa S, Chuma S, Tanaka T, Nakatsuji N, Kimura T, Nakano T, (2009) Associations between PIWI proteins and TDRD1/MTR-1 are critical for integrated subcellular localization in murine male germ cells. Genes Cells 14: 1155-1165
39. Kotaja N, Lin H, Parvinen M, Sassone-Corsi P, (2006) Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. J Cell Sci 119: 2819-2825
40. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T, (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849
41. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, Hata K, Li E, Matsuda Y, Kimura T, Okabe M, Sakaki Y, Sasaki H, Nakano T, (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917
42. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S, Kojima-Kita K, Shiromoto Y, Asada N, Toyoda A, Fujiyama A, Totoki Y, Shibata T, Kimura T, Nakatsuji N, Noce T, Sasaki H, Nakano T, (2010) MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev 24: 887-892
43. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
44. Leblond CP, Clermont Y, (1952) Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat 90: 167-215
45. Lees-Murdock DJ, Walsh CP, (2008) DNA methylation reprogramming in the germ line. Epigenetics 3: 5-13
46. Lerner EA, Lerner MR, Janeway CA Jr, Steitz JA, (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci USA 78: 2737-2741
47. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J, Moore MJ, Schimenti JC, Weng Z, Zamore PD, (2013a) An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol Cell 50: 67-81
48. Li XZ, Roy CK, Moore MJ, Zamore PD, (2013b) Defining piRNA primary transcripts. Cell Cycle 12: 1657-1658
49. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, Morris DR, Garvik BM, Yates JR III, (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17: 676-682
50. Luthe DS, (1983) A simple technique for the preparation and storage of sucrose gradients. Anal Biochem 135: 230-232
51. Ma L, Buchold GM, Greenbaum MP, Roy A, Burns KH, Zhu H, Han DY, Harris RA, Coarfa C, Gunaratne PH, Yan W, Matzuk MM, (2009) GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet 5: e1000635
52. Martin SL, Branciforte D, (1993) Synchronous expression of LINE-1 RNA and protein in mouse embryonal carcinoma cells. Mol Cell Biol 13: 5383-5392
53. Moens PB, (1995) Histones H1 and H4 of surface-spread meiotic chromosomes. Chromosoma 104: 169-174
54. Newton I, Rinke J, Brimacombe R, (1975) Random exchange of ribosomal proteins in EDTA sub-particles. FEBS Lett 51: 215-218
55. Nishimasu H, Ishizu H, Saito K, Fukuhara S, Kamatani MK, Bonnefond L, Matsumoto N, Nishizawa T, Nakanaga K, Aoki J, Ishitani R, Siomi H, Siomi MC, Nureki O, (2012) Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491: 284-287
56. Ogura A, Matsuda J, Yanagimachi R, (1994) Birth of normal young after electrofusion of mouse oocytes with round spermatids. Proc Natl Acad Sci USA 91: 7460-7462
57. Pan J, Goodheart M, Chuma S, Nakatsuji N, Page DC, Wang PJ, (2005) RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis. Development 132: 4029-4039
58. Pek JW, Lim AK, Kai T, (2009) Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev Cell 17: 417-424
59. Pek JW, Anand A, Kai T, (2012) Tudor domain proteins in development. Development 139: 2255-2266
60. Pillai RS, Chuma S, (2012) piRNAs and their involvement in male germline development in mice. Dev Growth Differ 54: 78-92
61. Reddi PP, Naaby-Hansen S, Aguolnik I, Tsai JY, Silver LM, Flickinger CJ, Herr JC, (1995) Complementary deoxyribonucleic acid cloning and characterization of mSP-10: the mouse homologue of human acrosomal protein SP-10. Biol Reprod 53: 873-881
62. Reuter M, Chuma S, Tanaka T, Franz T, Stark A, Pillai RS, (2009) Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat Struct Mol Biol 16: 639-646
63. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C, Antony C, Sachidanandam R, Pillai RS, (2011) Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480: 264-267
64. Russell LD, Ettlin RA, SinhaHikim AP, Clegg ED, (1990) Histological and Histopathological Evaluation of the Testis. St. Louis, MO: Cache River Press
65. Sanford LP, Kallapur S, Ormsby I, Doetschman T, (2001) Influence of genetic background on knockout mouse phenotypes. Methods Mol Biol 158: 217-225
66. Sato K, Nishida KM, Shibuya A, Siomi MC, Siomi H, (2011) Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC. Genes Dev 25: 2361-2373
67. Saxe JP, Chen M, Zhao H, Lin H, (2013) Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline. EMBO J 32: 1869-1885
68. Shoji M, Tanaka T, Hosokawa M, Reuter M, Stark A, Kato Y, Kondoh G, Okawa K, Chujo T, Suzuki T, Hata K, Martin SL, Noce T, Kuramochi-Miyagawa S, Nakano T, Sasaki H, Pillai RS, Nakatsuji N, Chuma S, (2009) The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell 17: 775-787
69. Sienski G, Donertas D, Brennecke J, (2012) Transcriptional silencing of transposons by piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964-980
70. 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
71. Soper SF, van der Heijden GW, Hardiman TC, Goodheart M, Martin SL, de Boer P, Bortvin A, (2008) Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15: 285-297
72. Spirin AS, (1974) Structural transformations of ribosomes (dissociation, unfolding and disassembly). FEBS Lett 40 (Suppl.): S38-S47
73. Tanaka T, Hosokawa M, Vagin VV, Reuter M, Hayashi E, Mochizuki AL, Kitamura K, Yamanaka H, Kondoh G, Okawa K, Kuramochi-Miyagawa S, Nakano T, Sachidanandam R, Hannon GJ, Pillai RS, Nakatsuji N, Chuma S, (2011) Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis. Proc Natl Acad Sci USA 108: 10579-10584
74. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111
75. Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, Chuma S, Girard A, Sachidanandam R, Hannon GJ, Aravin AA, (2009) Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 23: 1749-1762
76. Vasileva A, Tiedau D, Firooznia A, Muller-Reichert T, Jessberger R, (2009) Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Curr Biol 19: 630-639
77. Vourekas A, Kirino Y, Mourelatos Z, (2010) Elective affinities: a Tudor-Aubergine tale of germline partnership. Genes Dev 24: 1963-1966
78. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, Gregory BD, Mourelatos Z, (2012) Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol 19: 773-781
79. Vranis NM, van der Heijden GW, Malki S, Bortvin A, (2010) Synaptonemal complex length variation in wild-type male mice. Genes 1: 505-520
80. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, 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
81. Watanabe T, Chuma S, Yamamoto Y, Kuramochi-Miyagawa S, Totoki Y, Toyoda A, Hoki Y, Fujiyama A, Shibata T, Sado T, Noce T, Nakano T, Nakatsuji N, Lin H, Sasaki H, (2011) MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev Cell 20: 364-375
82. Yabuta Y, Ohta H, Abe T, Kurimoto K, Chuma S, Saitou M, (2011) TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J Cell Biol 192: 781-795
83. Yanagimachi R, Wakayama T, Kishikawa H, Fimia GM, Monaco L, Sassone-Corsi P, (2004) Production of fertile offspring from genetically infertile male mice. Proc Natl Acad Sci USA 101: 1691-1695
84. Zhang D, Xiong H, Shan J, Xia X, Trudeau VL, (2008) Functional insight into Maelstrom in the germline piRNA pathway: a unique domain homologous to the DnaQ-H 3′-5′ exonuclease, its lineage-specific expansion/loss and evolutionarily active site switch. Biol Direct 3: 48
85. Zhao S, Gou LT, Zhang M, Zu LD, Hua MM, Hua Y, Shi HJ, Li Y, Li J, Li D, Wang ED, Liu MF, (2013) piRNA-triggered MIWI ubiquitination and removal by APC/C in late spermatogenesis. Dev Cell 24: 13-25
86. Zheng Q, Wang XJ, (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res 36: W358-W363
87. 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