Gtsf1/Cue110, a gene encoding a protein with two copies of a CHHC Zn-finger motif, is involved in spermatogenesis and retrotransposon suppression in murine testes

Developmental Biology

Volumn 335, Issue 1, 2009, Pages 216-227

  Yoshimura, Takuji ^a,b   Toyoda, Shuichi ^b   Kuramochi Miyagawa, Satomi ^b   Miyazaki, Tatsushi ^b   Miyazaki, Satsuki ^b   Tashiro, Fumi ^b   Yamato, Eiji ^b   Nakano, Toru ^b   Miyazaki, Jun ichi ^b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

CHHC Zn finger; Cue110; DNA methylation; Gtsf1; IAP; Knockout mouse; Line 1; Male sterility; Retrotransposon; Spermatogenesis

Indexed keywords

PROTEIN CUE110; PROTEIN GTSF1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEMETHYLATION; FEMALE; FEMALE FERTILITY; GENE FUNCTION; GENE TARGETING; GENETIC TRANSCRIPTION; GERM CELL; GROWTH; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LONG INTERSPERSED REPEAT; MALE; MALE STERILITY; MEIOSIS; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROMOTER REGION; RETROPOSON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; SPERMATOGENESIS; TESTIS; WESTERN BLOTTING;

INTRACISTERNAL A-PARTICLES; MURINAE; MUS;

EID: 70349784966     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.09.003     Document Type: Article

References (69)

1. Andreeva A., and Tidow H. A novel CHHC Zn-finger domain found in spliceosomal proteins and tRNA modifying enzymes. Bioinformatics 24 (2008) 2277-2280
2. Aravin A.A., and Bourc'his D. Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev. 22 (2008) 970-975
3. Aravin A.A., Hannon G.J., and Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318 (2007) 761-764
4. Aravin A.A., Sachidanandam R., Girard A., Fejes-Toth K., and Hannon G.J. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316 (2007) 744-747
5. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., and Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol. Cell 31 (2008) 785-799
6. Baker S.M., Plug A.W., Prolla T.A., Bronner C.E., Harris A.C., Yao X., Christie D.M., Monell C., Arnheim N., Bradley A., Ashley T., and Liskay R.M. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13 (1996) 336-342
7. Ballow D., Meistrich M.L., Matzuk M., and Rajkovic A. Sohlh1 is essential for spermatogonial differentiation. Dev. Biol. 294 (2006) 161-167
8. Bellve A.R., Cavicchia J.C., Millette C.F., O'Brien D.A., Bhatnagar Y.M., and Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74 (1977) 68-85
9. Boswell R.E., and Mahowald A.P. tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43 (1985) 97-104
10. Branciforte D., and Martin S.L. Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition. Mol. Cell. Biol. 14 (1994) 2584-2592
11. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., and Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12 (2007) 503-514
12. Chuma S., Hiyoshi M., Yamamoto A., Hosokawa M., Takamune K., and Nakatsuji N. 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 (2003) 979-990
13. Chuma S., Hosokawa M., Kitamura K., Kasai S., Fujioka M., Hiyoshi M., Takamune K., Noce T., and Nakatsuji N. 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. U. S. A. 103 (2006) 15894-15899
14. Chuma S., Hosokawa M., Tanaka T., and Nakatsuji N. Ultrastructural characterization of spermatogenesis and its evolutionary conservation in the germline: Germinal granules in mammals. Mol. Cell Endocrinol. 306 (2009) 17-23
15. Cohen P.E., and Pollard J.W. Regulation of meiotic recombination and prophase I progression in mammals. Bioessays 23 (2001) 996-1009
16. Cohen P.E., Pollack S.E., and Pollard J.W. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr. Rev. 27 (2006) 398-426
17. Costa Y., Speed R.M., Gautier P., Semple C.A., Maratou K., Turner J.M., and Cooke H.J. Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway?. Hum. Mol. Genet. 15 (2006) 2324-2334
18. Cox D.N., Chao A., Baker J., Chang L., Qiao D., and Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12 (1998) 3715-3727
19. Crackower M.A., Kolas N.K., Noguchi J., Sarao R., Kikuchi K., Kaneko H., Kobayashi E., Kawai Y., Kozieradzki I., Landers R., Mo R., Hui C.C., Nieves E., Cohen P.E., Osborne L.R., Wada T., Kunieda T., Moens P.B., and Penninger J.M. Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 300 (2003) 1291-1295
20. Dupressoir A., and Heidmann T. Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol. Cell. Biol. 16 (1996) 4495-4503
21. Edelmann W., Cohen P.E., Kane M., Lau K., Morrow B., Bennett S., Umar A., Kunkel T., Cattoretti G., Chaganti R., Pollard J.W., Kolodner R.D., and Kucherlapati R. Meiotic pachytene arrest in MLH1-deficient mice. Cell 85 (1996) 1125-1134
22. Findley S.D., Tamanaha M., Clegg N.J., and Ruohola-Baker H. Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130 (2003) 859-871
23. Fujiwara Y., Komiya T., Kawabata H., Sato M., Fujimoto H., Furusawa M., and Noce T. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 12258-12262
24. Gasior S.L., Wakeman T.P., Xu B., and Deininger P.L. The human LINE-1 retrotransposon creates DNA double-strand breaks. J. Mol. Biol. 357 (2006) 1383-1393
25. Goodier J.L., Ostertag E.M., Du K., and Kazazian Jr. H.H. A novel active L1 retrotransposon subfamily in the mouse. Genome Res. 11 (2001) 1677-1685
26. Habu T., Taki T., West A., Nishimune Y., and Morita T. The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis. Nucleic Acids Res. 24 (1996) 470-477
27. Hay B., Jan L.Y., and Jan Y.N. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55 (1988) 577-587
28. Hay B., Jan L.Y., and Jan Y.N. Localization of vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity. Development 109 (1990) 425-433
29. Hecht N.B., Bower P.A., Waters S.H., Yelick P.C., and Distel R.J. Evidence for haploid expression of mouse testicular genes. Exp. Cell Res. 164 (1986) 183-190
30. Hunt P.A., and Hassold T.J. Sex matters in meiosis. Science 296 (2002) 2181-2183
31. Kazazian Jr. H.H. Mobile elements: drivers of genome evolution. Science 303 (2004) 1626-1632
32. Kleene K.C., Distel R.J., and Hecht N.B. Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev. Biol. 105 (1984) 71-79
33. Klink A., Lee M., and Cooke H.J. The mouse synaptosomal complex protein gene Sycp3 maps to band C of chromosome 10. Mamm. Genome. 8 (1997) 376-377
34. Kuramochi-Miyagawa S., Kimura T., Yomogida K., Kuroiwa A., Tadokoro Y., Fujita Y., Sato M., Matsuda Y., and Nakano T. Two mouse piwi-related genes: miwi and mili. Mech. Dev. 108 (2001) 121-133
35. Kuramochi-Miyagawa S., Kimura T., Ijiri T.W., Isobe T., Asada N., Fujita Y., Ikawa M., Iwai N., Okabe M., Deng W., Lin H., Matsuda Y., and Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131 (2004) 839-849
36. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Totoki Y., Toyoda A., Ikawa M., Asada N., Kojima K., Yamaguchi Y., Ijiri T.W., Hata K., Li E., Matsuda Y., Kimura T., Okabe M., Sakaki Y., Sasaki H., and Nakano T. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22 (2008) 908-917
37. Lammers J.H., Offenberg H.H., van Aalderen M., Vink A.C., Dietrich A.J., and Heyting C. The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol. Cell. Biol. 14 (1994) 1137-1146
38. Lasko P.F., and Ashburner M. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335 (1988) 611-617
39. Lasko P.F., and Ashburner M. Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 4 (1990) 905-921
40. Mahadevaiah S.K., Turner J.M., Baudat F., Rogakou E.P., de Boer P., Blanco-Rodriguez J., Jasin M., Keeney S., Bonner W.M., and Burgoyne P.S. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27 (2001) 271-276
41. Mettus R.V., Litvin J., Wali A., Toscani A., Latham K., Hatton K., and Reddy E.P. Murine A-myb: evidence for differential splicing and tissue-specific expression. Oncogene 9 (1994) 3077-3086
42. Meuwissen R.L., Offenberg H.H., Dietrich A.J., Riesewijk A., van Iersel M., and Heyting C. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 11 (1992) 5091-5100
43. Miyazaki S., Yamato E., and Miyazaki J. Regulated expression of pdx-1 promotes in vitro differentiation of insulin-producing cells from embryonic stem cells. Diabetes 53 (2004) 1030-1037
44. Miyazaki S., Miyazaki T., Tashiro F., Yamato E., and Miyazaki J. Development of a single-cassette system for spatiotemporal gene regulation in mice. Biochem. Biophys. Res. Commun. 338 (2005) 1083-1088
45. Morelli M.A., and Cohen P.E. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130 (2005) 761-781
46. Mountford P., Zevnik B., Duwel A., Nichols J., Li M., Dani C., Robertson M., Chambers I., and Smith A. Dicistronic targeting constructs: reporters and modifiers of mammalian gene expression. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 4303-4307
47. Ostertag E.M., and Kazazian Jr. H.H. Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 35 (2001) 501-538
48. Ostertag E.M., DeBerardinis R.J., Goodier J.L., Zhang Y., Yang N., Gerton G.L., and Kazazian Jr. H.H. A mouse model of human L1 retrotransposition. Nat. Genet. 32 (2002) 655-660
49. Peters A.H., Plug A.W., van Vugt M.J., and de Boer P. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5 (1997) 66-68
50. Ramirez-Solis R., Davis A.C., and Bradley A. Gene targeting in embryonic stem cells. Methods Enzymol. 225 (1993) 855-878
51. Robertson E.J. In: Robertson E.J. (Ed). Teratocarcinomas and embryonic stem cells: a practical approach (1987), IRL, Oxford 71-112
52. Rubin M.R., Toth L.E., Patel M.D., D'Eustachio P., and Nguyen-Huu M.C. A mouse homeo box gene is expressed in spermatocytes and embryos. Science 233 (1986) 663-667
53. Sage J., Martin L., Cuzin F., and Rassoulzadegan M. cDNA sequence of the murine synaptonemal complex protein 1 (SCP1). Biochim. Biophys. Acta. 1263 (1995) 258-260
54. Seaman F., Sawhney P., Giammona C.J., and Richburg J.H. Cisplatin-induced pulse of germ cell apoptosis precedes long-term elevated apoptotic rates in C57/BL/6 mouse testis. Apoptosis 8 (2003) 101-108
55. Smith R.C., Dworkin M.B., and Dworkin-Rastl E. Destruction of a translationally controlled mRNA in Xenopus oocytes delays progesterone-induced maturation. Genes Dev. 2 (1988) 1296-1306
56. Smith R.C., Bement W.M., Dersch M.A., Dworkin-Rastl E., Dworkin M.B., and Capco D.G. Nonspecific effects of oligodeoxynucleotide injection in Xenopus oocytes: a reevaluation of previous D7 mRNA ablation experiments. Development 110 (1990) 769-779
57. Smith R.C., Dworkin M.B., and Dworkin-Rastl E. The maternal gene product D7 is not required for early Xenopus development. Mech. Dev. 35 (1991) 213-225
58. Smith R.C., Dworkin M.B., and Dworkin-Rastl E. Synthesis and modification of D7 protein during Xenopus oocyte maturation. Mol. Reprod. Dev. 32 (1992) 293-301
59. Soper S.F., van der Heijden G.W., Hardiman T.C., Goodheart M., Martin S.L., de Boer P., and Bortvin A. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 15 (2008) 285-297
60. Sweeney C., Murphy M., Kubelka M., Ravnik S.E., Hawkins C.F., Wolgemuth D.J., and Carrington M. A distinct cyclin A is expressed in germ cells in the mouse. Development 122 (1996) 53-64
61. Tanaka S.S., Toyooka Y., Akasu R., Katoh-Fukui Y., Nakahara Y., Suzuki R., Yokoyama M., and Noce T. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14 (2000) 841-853
62. Toyoda S., Miyazaki T., Miyazaki S., Yoshimura T., Yamamoto M., Tashiro F., Yamato E., and Miyazaki J. Sohlh2 affects differentiation of KIT positive oocytes and spermatogonia. Dev. Biol. 325 (2009) 238-248
63. Toyooka Y., Tsunekawa N., Takahashi Y., Matsui Y., Satoh M., and Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech. Dev. 93 (2000) 139-149
64. Trauth K., Mutschler B., Jenkins N.A., Gilbert D.J., Copeland N.G., and Klempnauer K.H. Mouse A-myb encodes a trans-activator and is expressed in mitotically active cells of the developing central nervous system, adult testis and B lymphocytes. EMBO J. 13 (1994) 5994-6005
65. Turunen J.J., Will C.L., Grote M., Lührmann R., and Frilander M.J. The U11-48K protein contacts the 5'splice site of U12-type introns and the U11-59K protein. Mol. Cell. Biol. 28 (2008) 3548-3560
66. Wang C., and Lehmann R. Nanos is the localized posterior determinant in Drosophila. Cell 66 (1991) 637-647
67. Watanabe D., Yamada K., Nishina Y., Tajima Y., Koshimizu U., Nagata A., and Nishimune Y. Molecular cloning of a novel Ca(2+)-binding protein (calmegin) specifically expressed during male meiotic germ cell development. J. Biol. Chem. 269 (1994) 7744-7749
68. Wilkinson M.L., Crary S.M., Jackman J.E., Grayhack E.J., and Phizicky E.M. The 2′-O-methyltransferase responsible for modification of yeast tRNA at position 4. RNA 13 (2007) 404-413
69. Yoshimura T., Miyazaki T., Toyoda S., Miyazaki S., Tashiro F., Yamato E., and Miyazaki J. Gene expression pattern of Cue110: A member of the uncharacterized UPF0224 gene family preferentially expressed in germ cells. Gene Expr. Patterns 8 (2007) 27-35