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JOURNAL ARTICLES
Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males
T.Y. Lin, S. Viswanathan, C. Wood, P.G. Wilson, N. Wolf, M.T. Fuller
Development 1996 122: 1331-1341;
T.Y. Lin
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S. Viswanathan
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C. Wood
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P.G. Wilson
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N. Wolf
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M.T. Fuller
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Summary

Wild-type function of four Drosophila genes, spermatocyte arrest, cannonball, always early and meiosis I arrest, is required both for cell-cycle progression through the G2/M transition of meiosis I in males and for onset of spermatid differentiation. In males mutant for any one of these meiotic arrest genes, mature primary spermatocytes with partially condensed chromosomes accumulate and postmeiotic cells are lacking. The arrest in cell-cycle progression occurs prior to degradation of cyclin A protein. The block in spermatogenesis in these mutants is not simply a secondary consequence of meiotic cell-cycle arrest, as spermatid differentiation proceeds in males mutant for the cell cycle activating phosphatase twine. Instead, the arrest of both meiosis and spermiogenesis suggests a control point that may serve to coordinate the male meiotic cell cycle with the spermatid differentiation program. The phenotype of the Drosophila meiotic arrest mutants is strikingly similar to the histopathological features of meiosis I maturation arrest infertility in human males, suggesting that the control point may be conserved from flies to man.

Reference

    1. Alphey L.,
    2. Jimenez J.,
    3. White-Cooper H.,
    4. Dawson I.,
    5. Nurse P.,
    6. Glover D. M.
    (1992) twine, a cdc25 homologue that functions in the male and female germ line of Drosophila. Cell 69, 977–988
    OpenUrlCrossRefPubMedWeb of Science
    1. Bishop D. K.,
    2. Park D.,
    3. Xu L.,
    4. Kleckner N.
    (1992) DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439–456
    OpenUrlCrossRefPubMedWeb of Science
    1. Bridges C. B.
    (1935) Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster. J. Hered 26, 60–.
    OpenUrlFREE Full Text
    1. Castrillon D.,
    2. Gönczy P.,
    3. Alexzander S.,
    4. Rawson R.,
    5. Eberhart C.,
    6. Viswanathan S.,
    7. DiNardo S.,
    8. Wasserman S.
    (1993) Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: Characterization of male sterile mutants generated by single P-element mutagenesis. Genetics 135, 489–505
    OpenUrlAbstract/FREE Full Text
    1. Cenci G.,
    2. Bonaccorsi S.,
    3. Pisano C.,
    4. Verni F.,
    5. Gatti M.
    (1994) Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J. Cell Sci 107, 3521–3534
    OpenUrlAbstract/FREE Full Text
    1. Colgan T. J.,
    2. Bedard Y. C.,
    3. Strawbridge T. G.,
    4. Buckspan M. B.,
    5. Klotz P. G.
    (1980) Reappraisal of the value of testicular biopsy in the investigation of infertility. Fertil. Steril 33, 56–60
    OpenUrlPubMed
    1. Cooley L.,
    2. Berg C.,
    3. Spradling A.
    (1988) Controlling P element insertional mutagenesis. Trends in Genetics 4, 254–258
    OpenUrlCrossRefPubMedWeb of Science
    1. Courtot C.,
    2. Frankhauser C.,
    3. Simanis V.,
    4. Lehner C.
    (1992) The Drosophilacdc25 homolog twine is required for meiosis. Development 116, 405–416
    OpenUrlAbstract/FREE Full Text
    1. Doane W. W.
    (1960) Completion of meiosis in uninseminated eggs of Drosophila melanogaster. Science 132, 677–678
    OpenUrlAbstract/FREE Full Text
    1. Eberhart C. G.,
    2. Wasserman S. A.
    (1995) The pelota locus encodes a protein required for meiotic cell division: an analysis of G2/M arrest in Drosophila spermatogenesis. Development 121, 3477–3486
    OpenUrlAbstract
    1. Edgar B. A.
    (1995) Diversification of cell cycle controls in developing embryos. Current Opinion in Cell Biology 7, 815–824
    OpenUrlCrossRefPubMedWeb of Science
    1. Edgar B. A.,
    2. O'Farrell P. H.
    (1989) Genetic control of cell division patterns in the Drosophila embryo. Cell 57, 177–187
    OpenUrlCrossRefPubMedWeb of Science
    1. Edgar B. A.,
    2. O'Farrell P. H.
    (1990) The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2by string. Cell 62, 469–480
    OpenUrlCrossRefPubMedWeb of Science
    1. Edgar B. A.,
    2. Sprenger F.,
    3. Duronio R. J.,
    4. Leopold P.,
    5. O'Farrell P.
    (1994) Distinct molecular mechanisms time mitosis at four successive stages of Drosophila embryogenesis. Genes Dev 8, 440–452
    OpenUrlAbstract/FREE Full Text
    1. Glotzer M.,
    2. Murray A. W.,
    3. Kirschner M. W.
    (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349, 132–138
    OpenUrlCrossRefPubMedWeb of Science
    1. Gönczy P.,
    2. Thomas B. J.,
    3. DiNardo S.
    (1994) roughex is a dose-dependent regulator of the second meiotic division during Drosophila spermatogenesis. Cell 77, 1015–1025
    OpenUrlCrossRefPubMedWeb of Science
    1. Hackstein J. H. P.
    (1991) Spermatogenesis in Drosophila: A genetic approach to cellular and subcellular differentiation. Eur. J. Cell Biol 56, 151–169
    OpenUrlPubMed
    1. Jimenez J.,
    2. Alphey L.,
    3. Nurse P.,
    4. Glover D. M.
    (1990) Complementation of fission yeast cdc2ts and cdc25ts mutants identifies two cell cycle genes from Drosophila: a cdc2 homologue and string. EMBO J 9, 3565–3571
    OpenUrlPubMedWeb of Science
    1. Kemphues K. J.,
    2. Raff E. C.,
    3. Raff R. A.,
    4. Kaufman T. C.
    (1980) Mutation in a testis-specific-tubulin in Drosophila: analysis of its effects on meiosis and map location of the gene. Cell 21, 445–451
    OpenUrlCrossRefPubMed
    1. Lewis E. B.,
    2. Bacher F.
    (1968) Method for feeding ethyl methane sulfonate (EMS) to Drosophila males. Drosophila Inform. Serv 43, 193–.
    OpenUrl
    1. Lifschytz E.
    (1987) The developmental program of spermiogenesis in Drosophila: a genetic analysis. Int. Rev. Cytol 109, 211–258
    OpenUrlCrossRefPubMed
    1. Luca F. C.,
    2. Shibuya E. K.,
    3. Dohrmann C. E.,
    4. Ruderman J. V.
    (1991) Both cyclin A60 and B 97 are stable and arrest cells in M-phase, but only cyclin B97 turns on cyclin destruction. EMBO J 10, 4311–4320
    OpenUrlPubMedWeb of Science
    1. McKearin D.,
    2. Spradling A. C.
    (1990) bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev 4, 2242–2251
    OpenUrlAbstract/FREE Full Text
    1. Meyer J. M.,
    2. Maetz J. L.,
    3. Rumpler Y.
    (1992) Cellular relationship impairment in maturation arrest of human spermatogenesis: an ultrastructural study. Histopathology 21, 25–33
    OpenUrlPubMedWeb of Science
    1. Nurse P.
    (1990) Universal control mechanism regulating onset of M-phase. Nature 344, 503–508
    OpenUrlCrossRefPubMedWeb of Science
    1. Olivieri G.,
    2. Olivieri A.
    (1965) Autoradiographic study of nucleic acid synthesis during spermatogenesis in Drosophila melanogaster. Mutat. Res 2, 366–380
    OpenUrlCrossRefPubMedWeb of Science
    1. Robertson H.,
    2. Preston C.,
    3. Phillis R.,
    4. Johnson-Schlitz D.,
    5. Benz W.,
    6. Engels W.
    (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470
    OpenUrlAbstract/FREE Full Text
    1. Sandler L.,
    2. Lindsley D. L.,
    3. Nicoletti B.,
    4. Trippa G.
    (1968) Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics 60, 525–558
    OpenUrlFREE Full Text
    1. Sigrist S.,
    2. Ried G.,
    3. Lehner C. F.
    (1995) Dmcdc2 kinase is required for both meiotic divisions during Drosophila spermatogenesis and is activated by the Twine/cdc25 phosphatase. Mechan. Development 53, 247–260
    OpenUrlCrossRefPubMedWeb of Science
    1. Soderstrom K.-O.,
    2. Suominen M.
    (1980) Histopathology and ultrastructure of meiotic arrest in human spermatogenesis. Arch. Pathol. Lab. Med 104, 476–482
    OpenUrlPubMedWeb of Science
    1. Stern B.,
    2. Ried G.,
    3. Clegg N. J.,
    4. Grigliatti T. A.,
    5. Lehner C. F.
    (1993) Genetic analysis of the Drosophila cdc2 homolog. Development 117, 219–232
    OpenUrlAbstract/FREE Full Text
    1. Sudakin V.,
    2. Ganoth D.,
    3. Dahan A.,
    4. Heller H.,
    5. Hershko J.,
    6. Luca F. C.,
    7. Ruderman J. V.,
    8. Hershko A.
    (1995) The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Molec. Biol. Cell 6, 185–197
    OpenUrlAbstract/FREE Full Text
    1. Sym M.,
    2. Engebrecht J.,
    3. Roeder G. S.
    (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72, 365–378
    OpenUrlCrossRefPubMedWeb of Science
    1. Theurkauf W. E.,
    2. Hawley R. S.
    (1992) Meiotic spindle assembly in Drosophila females: Behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J. Cell Biol 116, 1167–1180
    OpenUrlAbstract/FREE Full Text
    1. Weber L.,
    2. Byers B.
    (1992) A RAD9-dependent checkpoint blocks meiosis of cdc13 yeast cells. Genetics 131, 55–63
    OpenUrlAbstract/FREE Full Text
    1. White-Cooper H.,
    2. Alphey L.,
    3. Glover D. M.
    (1993) The cdc25 homologue twine is required for only some aspects of the entry into meiosis in Drosophila. J. Cell Sci 106, 1035–1044
    OpenUrlAbstract/FREE Full Text
    1. Wohlwill A. D.,
    2. Bonner J. J.
    (1991) Genetic analysis of chromosome region 63 of Drosophila melanogaster. Genetics 128, 763–776
    OpenUrlAbstract/FREE Full Text
    1. Wong T. W.,
    2. Straus F. H.,
    3. Warner N. E.
    (1973) Testicular biopsy in the study of male infertility. Arch. Pathol 95, 151–159
    OpenUrlPubMedWeb of Science
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JOURNAL ARTICLES
Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males
T.Y. Lin, S. Viswanathan, C. Wood, P.G. Wilson, N. Wolf, M.T. Fuller
Development 1996 122: 1331-1341;
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JOURNAL ARTICLES
Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males
T.Y. Lin, S. Viswanathan, C. Wood, P.G. Wilson, N. Wolf, M.T. Fuller
Development 1996 122: 1331-1341;

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