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JOURNAL ARTICLES
The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis
P. Gonczy, S. DiNardo
Development 1996 122: 2437-2447;

Summary

Spermatogenesis relies on the function of germ-line stem cells, as a continuous supply of differentiated spermatids is produced throughout life. In Drosophila, there must also be somatic stem cells that produce the cyst cells that accompany germ cells throughout spermatogenesis. By lineage tracing, we demonstrate the existence of such somatic stem cells and confirm that of germ-line stem cells. The somatic stem cells likely correspond to the ultrastructurally described cyst progenitor cells. The stem cells for both the germ-line and cyst lineage are anchored around the hub of non-dividing somatic cells located at the testis tip. We then address whether germ cells regulate the behavior of somatic hub cells, cyst progenitors and their daughter cyst cells by analyzing cell proliferation and fate in testes in which the germ line has been genetically ablated. Daughter cyst cells, which normally withdraw from the cell cycle, continue to proliferate in the absence of germ cells. In addition, cells from the cyst lineage switch to the hub cell fate. Male-sterile alleles of chickadee and diaphanous, which are deficient in germ cells, exhibit similar cyst cell phenotypes. We conclude that signaling from germ cells regulates the proliferation and fate of cells in the somatic cyst lineage.

Reference

    1. Aboïm A. N.
    (1945) Developement embryonnaire et postembryonnaire des gonades normales et agametiques de Drosophila melanogaster. Rev. Suisse Zool 52, 53–154
    OpenUrl
    1. Austin J.,
    2. Kimble J.
    (1989) Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58, 565–571
    OpenUrlCrossRefPubMedWeb of Science
    1. Brower D. L.,
    2. Smith R. J.,
    3. Wilcox M.
    (1981) Differentiation within the gonads of Drosophila revealed by immunofluorescence. J. Embryol. Exp. Morph 63, 233–242
    OpenUrlPubMedWeb of Science
    1. Castrillon D. H.,
    2. Gönczy P.,
    3. Alexander S.,
    4. Rawson R.,
    5. Eberhart C. G.,
    6. Viswanathan S.,
    7. DiNardo S.,
    8. Wasserman S. A.
    (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. Castrillon D. H.,
    2. Wasserman S. A.
    (1994) diaphanous is required for cytokenesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120, 3367–3377
    OpenUrlAbstract
    1. Cheng C. Y.,
    2. Grima J.,
    3. Stahler M. S.,
    4. Lockshin R. A.,
    5. Bardin C. W.
    (1989) Testins are structurally related Sertoli cell proteins whose secretion is tightly coupled to the presence of germ cells. J. Biol. Chem 264, 21386–21393
    OpenUrlAbstract/FREE Full Text
    1. Chou T. B.,
    2. Perrimon N.
    (1992) Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643–653
    OpenUrlAbstract/FREE Full Text
    1. Cooley L.,
    2. Kelley R.,
    3. Spradling A. C.
    (1992) chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69, 173–184
    OpenUrlCrossRefPubMedWeb of Science
    1. Geigy R.
    (1931) Action de l'ultra-violet sur le pôle germinal dans l'oeuf de Drosphila melanogaster. (Castration et mutabilite). Rev. Suisse Zool 38, 187–288
    OpenUrl
    1. Goldschmidt-Clermont P. J.,
    2. Kin J. W.,
    3. Machesky L. M.,
    4. Rhee S. G.,
    5. Pollard T. D.
    (1991) Regulation of phospholipase C- y 1 by profilin and tyrosine phosphorylation. Science 251, 1231–1233
    OpenUrlAbstract/FREE Full Text
    1. Golic K. G.
    (1991) Site-specific recombination between homologous chromosomes in Drosophila. Science 252, 958–961
    OpenUrlAbstract/FREE Full Text
    1. Gönczy P.,
    2. Viswanathan S.,
    3. DiNardo S.
    (1992) Probing spermatogenesis in Drosophila with P-element enhancer detectors. Development 114, 89–98
    OpenUrlAbstract
    1. Hall P. A.,
    2. Watt F. M.
    (1989) Stem cells:the generation and maintenance of cellular diversity. Development 106, 619–633
    OpenUrlFREE Full Text
    1. Hardy R. W.,
    2. Tokuyasu K. T.,
    3. Lindsley D. L.,
    4. Garavito M.
    (1979) The germinal proliferation center in the testis of Drosophila melanogaster. J. Ultrastruct. Res 69, 180–190
    OpenUrlCrossRefPubMedWeb of Science
    1. Harrison D. A.,
    2. Perrimon N.
    (1993) Simple and efficient generation of marked clones in Drosophila. Current Biology 3, 424–433
    OpenUrlCrossRefPubMedWeb of Science
    1. Hartl D. L.,
    2. Green M. M.
    (1970) Genetic studies of germinal mosaicism in Drosophila melanogaster using the mutable wc gene. Genetics 65, 449–456
    OpenUrlFREE Full Text
    1. Henderson S. T.,
    2. Gao D.,
    3. Lambie E. J.,
    4. Kimble J.
    (1994) lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120, 2913–2924
    OpenUrlAbstract
    1. Kassis J. A.,
    2. Noll E.,
    3. VanSickle E. P.,
    4. Odenwald W. F.,
    5. Perrimon N.
    (1992) Altering the insertional specificity of a Drosophila transposable element. Proc. Natl. Acad. Sci. USA 89, 1919–1923
    OpenUrlAbstract/FREE Full Text
    1. Kimble J. E.,
    2. White J. G.
    (1981) On the control of germ cell development in Caenorhabditis elegans. Dev. Biol 81, 208–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Koury M. J.,
    2. Bondurant M. C.
    (1990) Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science 248, 378–81
    OpenUrlAbstract/FREE Full Text
    1. Lehmann R.,
    2. Nusslein-Volhard C.
    (1986) Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47, 141–152
    OpenUrlCrossRefPubMedWeb of Science
    1. LeMagueresse B.,
    2. Pineau C.,
    3. Guillou F.,
    4. Jegou B.
    (1988) Influence of germ cells upon transferrin secretion by rat Sertoli cells in vitro. J. Endocrinol 118, 13–.
    OpenUrlCrossRef
    1. Lin H.,
    2. Spradling A. C.
    (1993) Germ line stem cell division and egg chamber development in transplanted Drosophila germaria. Dev. Biol 159, 140–152
    OpenUrlCrossRefPubMedWeb of Science
    1. Lowry P. A.,
    2. Deacon D.,
    3. Whitefield P.,
    4. McGrath H. E.,
    5. Quesenberry P. J.
    (1992) Stem cell factor induction of in vitro murine hematopoietic colony formation by ‘subliminal’ cytokine combinations: the role of ‘anchor factors’. Blood 80, 663–9
    OpenUrlAbstract/FREE Full Text
    1. Marsh L.,
    2. Neiman A. M.,
    3. Herskowitz I.
    (1991) Signal transduction during pheromone response in yeast. Annu. Rev. Cell. Biol 7, 699–728
    OpenUrlCrossRefWeb of Science
    1. Matzuk M. M.,
    2. Finegold M. J.,
    3. Su J. G.,
    4. Hsueh A. J.,
    5. Bradley A.
    (1992) Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360, 313–319
    OpenUrlCrossRefPubMedWeb of Science
    1. Patel N. H.,
    2. Snow P. M.,
    3. Goodman C. S.
    (1987) Characterization and cloning of Fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48, 975–988
    OpenUrlCrossRefPubMedWeb of Science
    1. Peter M.,
    2. Gartner A.,
    3. Horecka J.,
    4. Ammerer G.,
    5. Herskowitz I.
    (1993) FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73, 747–760
    OpenUrlCrossRefPubMedWeb of Science
    1. Peter M.,
    2. Herskowitz I.
    (1994) Direct inhibition of the yeast cyclin-dependent kinase Cdc28-Cln by Far1. Science 265, 1228–1231
    OpenUrlAbstract/FREE Full Text
    1. Pineau C.,
    2. Sharpe R. M.,
    3. Saunders P. T.,
    4. Gerard N.,
    5. Jegou B.
    (1990) Regulation of Sertoli cell inhibin production and of inhibin alpha-subunit mRNA levels by specific germ cell types. Mol. Cell. Endo 72, 13–22
    OpenUrlCrossRefPubMedWeb of Science
    1. Reed S. I.
    (1991) Pheromone signaling pathways in yeast. Curr. Opin. Genet. Dev 1, 391–396
    OpenUrlCrossRefPubMed
    1. Schubiger M.,
    2. Palka J.
    (1987) Changing spatial patterns of DNA replication in the developing wing of Drosophila. Dev. Biol 123, 145–153
    OpenUrlCrossRefPubMedWeb of Science
    1. Skaer H.
    (1989) Cell division in Malpighian tubule development in Drosophila melanogaster is regulated by a single tip cell. Nature 342, 566–569
    OpenUrlCrossRef
    1. Skaer H.
    (1992) Cell proliferation and rearrangement in the development of the malpighian tubules of the hemipteran, Rhodnius prolixus. Dev. Biol 150, 372–380
    OpenUrlCrossRefPubMed
    1. Sulston J. E.,
    2. White J. G.
    (1980) Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev. Biol 78, 577–597
    OpenUrlCrossRefPubMedWeb of Science
    1. Tax F. E.,
    2. Yeargers J. J.,
    3. Thomas J. H.
    (1994) Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature 368, 150–154
    OpenUrlCrossRefPubMed
    1. Tres L. L.,
    2. Kierszenbaum A. L.
    (1983) Viability of rat spermatogenic cells in vitro is facilitated by their coculture with Sertoli cells in serum-free hormone-supplemented medium. Proc. Natn. Acad. Sci. USA 80, 3377–3381
    OpenUrlAbstract/FREE Full Text
    1. Verheyen E. M.,
    2. Cooley L.
    (1994) Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120, 717–728
    OpenUrlAbstract
    1. Vojtek A.,
    2. Haarer B.,
    3. Field J.,
    4. Gerst J.,
    5. Pollard T. D.,
    6. Brown S.,
    7. Wigler M.
    (1991) Evidence for a functional link between profilin and CAP in the yeast S. cerevisiae. Cell 66, 497–505
    OpenUrlCrossRefPubMedWeb of Science
    1. Welsh M. K.,
    2. Ireland M. E.,
    3. Treisman G. J.
    (1985) Stimulation of rat Sertoli cell adenylate cyclase by germ cells in vitro. Biol. Reprod 33, 1050–1056
    OpenUrlAbstract
    1. Whetton A. D.,
    2. Dexter T. M.
    (1993) Influence of growth factors and substrates on differentiation of haemopoietic stem cells. Curr. Opin. Cell Biol 5, 1044–1049
    OpenUrlCrossRefPubMed
    1. Williams G. T.,
    2. Smith C. A.,
    3. Spooncer E.,
    4. Dexter T. M.,
    5. Taylor D. R.
    (1990) Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature 343, 76–79
    OpenUrlCrossRefPubMedWeb of Science
    1. Yochem J.,
    2. Weston K.,
    3. Greenwald I.
    (1989) The Caenorhabditis eleganslin-12 gene encodes a transmembrane protein with overall similarity to Drosophila Notch. Nature 335, 547–550
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JOURNAL ARTICLES
The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis
P. Gonczy, S. DiNardo
Development 1996 122: 2437-2447;
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