The mouse homolog of Drosophila Vasa is required for the development of male germ cells

Genes and Development

Volumn 14, Issue 7, 2000, Pages 841-853

  Tanaka, Satomi S ^a,c   Toyooka, Yayoi ^a,b   Akasu, Ryuko ^a   Katoh Fukui, Yuko ^a   Nakahara, Yoko ^a   Suzuki, Rika ^a   Yokoyama, Minesuke ^a   Noce, Toshiaki ^a  

^a MITSUBISHI KASEI INST OF LIFE SCI   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

Author keywords

Meiosis; Mouse; Primordial germ cell; Spermatogenesis; Vasa

Indexed keywords

APOPTOSIS; ARTICLE; CELL PROLIFERATION; DROSOPHILA; MEIOSIS; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SPERMATOGENESIS;

AGING; AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CONSERVED SEQUENCE; DEAD-BOX RNA HELICASES; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYONIC AND FETAL DEVELOPMENT; HETEROZYGOTE; HOMOZYGOTE; MALE; MEIOSIS; MICE; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA HELICASES; SPERMATOZOA; STEM CELLS; TESTIS;

HEXAPODA;

EID: 0034175552     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (80)

1. Allan, D.J., B.V. Harmon, and S.A. Roberts. 1992. Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif. 25: 241-250.
2. Anderson, R., R. Fassler, E. Georges-Labouesse, R.O. Hynes, B.L. Bader, J.A. Kreidberg, K. Schaible, J. Heasman, and C.C. Wylie. 1999. Mouse primordial germ cells lacking betal integrins enter the germline but fail to migrate normally to the gonads. Development 126: 1655-1664.
3. Baker, S.M., A.W. Plug, T.A. Prolla, C.E. Bronner, A.C. Harris, X. Yao, D.M. Christie, C. Monell, N. Arnheim, A. Bradley et al. 1996. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13: 336-342.
4. Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J.N. Crawley, T. Ried, D. Tagle et al. 1996. Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 86: 159-171.
5. Billig, H., I. Furuta, C. Rivier, J. Tapanainen, M. Parvinen, and A. Hsueh. 1995. Apoptosis in testis germ cells: Developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136: 5-12.
6. Beck, A.R.P., I.J. Miller, P. Anderson, and M. Streuli. 1998. RNA-binding protein TIAR is essential for primordial germ cell development. Proc. Natl. Acad. Sci. 95: 2331-2336.
7. Besmer, P., K. Manova, R. Duttlinger, E. J. Huang, A. Packer, C. Gyssler, and R.F. Bachvarova. 1993. The kit-ligand (steel factor) and its receptor c-kit/W: Pleiotropic roles in gametogenesis and melanogenesis. Development Suppl. 125-137.
8. Blendy, J.A., K.H. Kaestner, G.F. Weinbauer, E. Nieschlag, and G. Schutz. 1996. Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380: 162-165.
9. Boer, P.H., H. Potten, C.N. Adra, K. Jardine, G. Mullhofer, and M.W. McBurney. 1990. Polymorphisms in the coding and noncoding regions of murine Pgk-1 alleles. Biochem. Genet. 28: 299-308.
10. Coucouvanis, C.E. and P.P. Jones. 1993. Changes in protooncogene expression correlated with general and sex specific differentiation in murine primordial germ cells. Mech. Dev. 42: 49-58.
11. Dahanukar, A. and R.P. Wharton. 1996. The Nanos gradient in Drosophila embryos is generated by translational regulation. Genes & Dev. 10: 2610-2620.
12. de Vries, S.S., E.B. Baart, M. Dekker, A. Siezen, D.G. de Rooij, P. de Boer, and H. de Riele. 1999. Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes & Dev. 13: 523-531.
13. Dix, D.J., J.W. Allen, B.W. Collins, C. Mori, N. Nakamura, P. Poorman-Allen, E.H. Goulding, and E.M. Eddy. 1996. Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc. Natl. Acad. Sci. 93: 3264-3268.
14. Donovan, P.J., D. Stott, I. Godin, J. Heasman, and C.C. Wylie. 1986. Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44: 831-838.
15. Eddy, E.M. 1975. Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43: 229-280.
16. Edelmann, W., P.E. Cohen, M. Kane, K. Lau, B. Morrow, S. Bennett, A. Umar, T. Kunkel, G. Cattoretti, R. Chaganti et al. 1996. Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
17. Edelmann, W., P.E. Cohen, B. Kneitz, N. Winand, M. Lia, J. Heyer, R. Kolodner, J.W. Pollard, and R. Kucherlapati. 1999. Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet. 21: 123-127.
18. Elson, A., Y. Wang, C.J. Daugherty, C.C. Morton, F. Zhou, J. Campos-Torres, and P. Leder. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. 93: 13084-13089.
19. Foulkes, N.S., B. Mellstrom, E. Benusiglio, and P. Sassone-Corsi. 1992. Developmental switch of CREM function during spermatogenesis: From antagonist to activator. Nature 355: 80-84.
20. Fox, N., I. Damjanov, A. Martinez-Hernandez, B.B. Knowles, and D. Solter. 1981. Immunohistochemical localization of the early embryonic antigen (SSEA-1) in postimplantation mouse embryos and fetal and adult tissues. Dev. Biol. 83: 391-398.
21. Francavilla, S. and L. Zamboni. 1985. Differentiation of mouse ectopic germinal cells in intra- and perigonadal locations. J. Exp. Zool. 233: 101-109.
22. Fujiwara, Y., T. Komiya, H. Kawabata, M. Sato, H. Fujimoto, M. Furusawa, and T. Noce. 1994. 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. 91: 12258-12262.
23. Gavis, E.R., L. Lunsford, S.E. Bergsten, and R. Lehmann. 1996. A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122: 2791-2800.
24. Ginsburg, M., M.H. Snow, and A. McLaren. 1990. Primordial germ cells in the mouse embryo during gastrulation. Development 110: 521-528.
25. Gruidl, M.E., P.A. Smith, K.A. Kuznicki, J.S. McCrone, J. Kirchner, D.L. Roussell, S. Strome, and K.L. Bennett. 1996. Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans. Proc. Natl. Acad. Sci. 93: 13837-13842.
26. Habu, T., T. Taki, A. West, Y. Nishimune, and T. Morita. 1996. 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: 470-477.
27. Hahnel, A.C. and E.M. Eddy. 1986. Cell surface markers of mouse primordial germ cells defined by two monoclonal antibodies. Gamete Res. 15: 25-34.
28. Hahnel, A.C., D.A. Rappolee, J.L. Millan, T. Manes, C.A. Ziomek, N.G. Theodosiou, Z. Werb, R.A. Pedersen, and G.A. Schultz. 1990. Two alkaline phosphatase genes are expressed during early development in the mouse embryo. Development 110: 555-564.
29. Hay, B., L.Y. Jan, and Y.N. Jan. 1988. A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55: 577-587.
30. Hogan, B., R. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the mouse embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Klink, A., M. Lee, and H.J. Cooke. 1997. The mouse synaptosomal complex protein gene Sycp3 maps to band C of chromosome 10. Mamm. Genome 8: 376-377.
32. Komiya, T., K. Itoh, K. Ikenishi, and M. Furusawa. 1994. Isolation and characterization of a novel gene of the DEAD box protein family which is specifically expressed in germ cells of Xenopus laevis. Dev. Biol. 162: 354-363.
33. Koshimizu, U., D. Watanabe, K. Sawada, and Y. Nishimune. 1993. A novel stage-specific differentiation antigen is expressed on mouse testicular germ cells during early meiotic prophase. Biol. Reprod. 49: 875-884.
34. Lasko, P.F. and M. Ashburner. 1988. The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335: 611-617.
35. _. 1990. Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes & Dev. 4: 905-921.
36. Lawson, K.A. and W.J. Hage. 1994. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182: 68-84.
37. Lawson, K.A., N.R. Dunn, B.A. Roelen, L.M. Zeinstra, A.M. Davis, C.V. Wright, J.P. Korving, and B.L. Hogan. 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes & Dev. 13: 424-436.
38. Leroy, P., P. Alzari, D. Sassoon, D. Wolgemuth, and M. Fellous. 1989. The protein encoded by a murine male germ cell-specific transcript is a putative ATP-dependent RNA helicase. Cell 57: 549-559.
39. Liang, L., W. Diehl-Jones, and P. Lasko. 1994. Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120: 1201-1211.
40. MacGregor, R.G., P.R. Zambrowicz, and P. Soriano. 1995. Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells. Development 121: 1487-1496.
41. McLaren, A. 1994. Germline and soma: Interactions during early mouse development. Semin. Dev. Biol. 5: 43-49.
42. Mettus, R.V., J. Litvin, A. Wali, A. Toscani, K. Latham, K. Hatton, and E.P. Reddy. 1994. Murine A-myb: Evidence for differential splicing and tissue-specific expression. Oncogene 9: 3077-3086.
43. Meuwissen, R.L., H.H. Offenberg, A.J. Dietrich, A. Riesewijk, M. van lersel, and C. Heyting. 1992. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 11: 5091-5100.
44. Nantel, F., L. Monaco, N.S. Foulkes, D. Masquilier, M. LeMeur, K. Henriksen, A. Dierich, M. Parvinen, and P. Sassone-Corsi. 1996. Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380: 159-162.
45. Oakberg, E.F. 1956. A description of spermatogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am. J. Anat. 99: 391-414.
46. Okazawa, H., K. Okamoto, F. Ishino, T. Ishino-Kaneko, S. Takeda, Y. Toyoda, M. Muramatsu, and H. Hamada. 1991. The Oct3 gene, a gene for an embryonic transcription factor, is controlled by a retinoic acid repressible enhancer. EMBO J. 10: 2997-3005.
47. Olsen, L.C., R. Aasland, and A. Fjose. 1997. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech. Dev. 66: 95-105.
48. Pesce, M., M.G. Farrace, M. Piacentini, S. Dolci, and M. De Felici. 1993. Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development 118: 1089-1094.
49. Pesce, M., X. Wang, D.J. Wolgemuth, and H. Scholer. 1998. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech. Dev. 71: 89-98.
50. Roest, H.P., J. van Klaveren, J. de Wit, C.G. van Gurp, M.H. Koken, M. Vermey, J.H. van Roijen, J.W. Hoogerbrugge, J.T. Vreeburg, W.M. Baarends et al. 1996. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 86: 799-810.
51. Rongo, C. and R. Lehmann. 1996. Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet. 12: 102-109.
52. Roussell, D.L. and K.L. Bennett. 1993. glh-1, a germ-line putative RNA helicase from Caenorhabditis, has four zinc fingers. Proc. Natl. Acad. Sci. 90: 9300-9304.
53. Rubin, M.R., L.E. Toth, M.D. Patel, P. D'Eustachio, and M.C. Nguyen-Huu. 1986. A mouse homeo-box gene is expressed in spermatocytes and embryos. Science 233: 663-667.
54. Ruggiu, M., R. Speed, M. Taggart, S.J. McKay, F. Kilanowski, P. Saunders, J. Dorin, and H.J. Cooke. 1997. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389: 73-77.
55. Russell, L. and B. Frank. 1978. Ultrastructural characterization of nuage in spermatocytes of the rat testis. Anat. Rec. 190: 79-97.
56. Sage, J., L. Martin, F. Cuzin, and M. Rassoulzadegan. 1995. cDNA sequence of the murine synaptonemal complex protein 1 (SCP1). Biochim. Biophys. Acta 1263: 258-260.
57. Saijoh, Y., H. Fujii, C. Meno, M. Sato, Y. Hirota, S. Nagamatsu, M. Ikeda, and H. Hamada. 1996. Identification of putative downstream genes of Oct-3, a pluripotent cell-specific transcription factor. Genes Cells 1: 239-252.
58. Sowden, J., W. Putt, K. Morrison, R. Beddington, and Y. Edwards. 1995. The embryonic RNA helicase gene (ERH): A new member of the DEAD box family of RNA helicases. Biochem. J. 308: 839-846.
59. Styhler, S., A. Nakamura, A. Swan, B. Suter, and P. Lasko. 1998. Vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 125: 1569-1578.
60. Sweeney, C., M. Murphy, M. Kubelka, S.E. Ravnik, C.F. Hawkins, D.J. Wolgemuth, and M. Carrington. 1996. A distinct cyclin A is expressed in germ cells in the mouse. Development 122: 53-64.
61. Tam, P.P.L and M.H.L. Snow. 1981. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morph. 64: 133-147.
62. Tam, P.P.L. and S.X. Zhou. 1996. The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178: 124-132.
63. Tanaka, H., L.A. Pereira, M. Nozaki, J. Tsuchida, K. Sawada, H. Mori, and Y. Nishimune. 1997. A germ cell-specific nuclear antigen recognized by a monoclonal antibody raised against mouse testicular germ cells. Int. J. Androl. 20: 361-366.
64. Tomancak, P., A. Guichet, P. Zavorszky, and A. Ephrussi. 1998. Oocyte polarity depends on regulation of gurken by Vasa. Development 125: 1723-1732.
65. Toscani, A., R.V. Mettus, R. Coupland, H. Simpkins, J. Litvin, J. Orth, K.S. Hatton, and E.P. Reddy. 1997. Arrest of spermatogenesis and defective breast development in mice lacking A-myb. Nature 386: 713-717.
66. Toyooka, Y., S.S. Tanaka, O. Hirota, S. Tanaka, N. Takagi, K. Yamanouchi, H. Tojo, and C. Tachi. 1998. Wilms' tumor suppressor gene (WT1) as a target gene of SRY function in a mouse ES cell line transfected with SRY. Int. J. Dev. Biol. 42: 1143-1151.
67. Toyooka, Y., N. Tsunekawa, Y. Takahashi, Y. Matsui, M. Satoh, and T. Noce. 2000. Expression and intracellular localization of mouse Vasa-homolog protein during germ cell development. Mech. Dev. (in press).
68. Trauth, K., B. Mutschler, N.A. Jenkins, D.J. Gilbert, N.G. Copeland, and K.H. Klempnauer. 1994. 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: 5994-6005.
69. Watanabe, D., K. Sawada, U. Koshimizu, T. Kagawa, and Y. Nishimune. 1992. Characterization of male meiotic germ cell-specific antigen (Meg 1) by monoclonal antibody TRA 369 in mice. Mol. Reprod. Dev. 33: 307-312.
70. Watanabe, D., K. Yamada, Y. Nishina, Y. Tajima, U. Koshimizu, A. Nagata, and Y. Nishimune. 1994. Molecular cloning of a novel Ca(2+)-binding protein (calmegin) specifically expressed during male meiotic germ cell development. J. Biol. Chem. 269: 7744-7749.
71. Wylie, C. 1999. Germ cells. Cell 96: 165-174.
72. Xu, Y., T. Ashley, E.E. Brainerd, R.T. Bronson, M.S. Meyn, and D. Baltimore. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes & Dev. 10: 2411-2422.
73. Yagi, T., Y. Ikawa, K. Yoshida, Y. Shigetani, N. Takeda, I. Mabuchi, T. Yamamoto, and S. Aizawa. 1990. Homologous recombination at c-fyn locus of mouse embryonic stem cells with use of diphtheria toxin A-fragment gene in negative selection. Proc. Natl. Acad. Sci. 87: 9918-9922.
74. Yeom, Y.I., G. Fuhrmann, C.E. Ovitt, A. Brehm, K. Ohbo, M. Gross, K. Hubner, and H.R. Scholer. 1996. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122: 881-894.
75. Yoon, C., K. Kawakami, and N. Hopkins. 1997. Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124: 3157-3165.
76. Yoshinaga, K., H. Muramatsu, and T. Muramatsu. 1991. Immunohistochemical localization of the carbohydrate antigen 4C9 in the mouse embryo: A reliable marker of mouse primordial germ cells. Differentiation 48: 75-82.
77. Zamboni, L. and S. Upadhyay. 1983. Germ cell differentiation in mouse adrenal glands. J. Exp. Zool. 228: 173-193.
78. Zernicka-Goetz, M. 1998. Fertile offspring derived from mammalian eggs lacking either animal or vegetal poles. Development 125: 4803-4808.
79. Zhao, G.Q. and B.L. Hogan. 1996. Evidence that mouse Bmp8a (Op2) and Bmp8b are duplicated genes that play a role in spermatogenesis and placental development. Mech. Dev. 57: 159-168.
80. Zhu, D., D.J. Dix, and E. M. Eddy. 1997. HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development 124: 3007-3014.