Advertisement
JOURNAL ARTICLES
Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms
J.S. Britton, B.A. Edgar
Development 1998 125: 2149-2158;

Summary

In newly hatched Drosophila larvae, quiescent cells reenter the cell cycle in response to dietary amino acids. To understand this process, we varied larval nutrition and monitored effects on cell cycle initiation and maintenance in the mitotic neuroblasts and imaginal disc cells, as well as the endoreplicating cells in other larval tissues. After cell cycle activation, mitotic and endoreplicating cells respond differently to the withdrawal of nutrition: mitotic cells continue to proliferate in a nutrition-independent manner, while most endoreplicating cells reenter a quiescent state. We also show that ectopic expression of Drosophila Cyclin E or the E2F transcription factor can drive quiescent endoreplicating cells, but not quiescent imaginal neuroblasts, into S-phase. Conversely, we demonstrate that quiescent imaginal neuroblasts, but not quiescent endoreplicating cells, can be induced to enter the cell cycle when co-cultured with larval fat body in vitro. These results demonstrate a fundamental difference in the control of cell cycle activation and maintenance in these two cell types, and imply the existence of a novel mitogen generated by the larval fat body in response to nutrition.

REFERENCES

    1. Altman J. S.,
    2. Bell E. M.
    (1973) A rapid method for the demonstration of nerve cell bodies in invertebrate central nervous systems. Brain Res 63, 487–489
    OpenUrlCrossRefPubMedWeb of Science
    1. Awad T. A.,
    2. Truman J. W.
    (1997) Postembryonic development of the midline glia in the CNS of Drosophila: Proliferation, programmed cell death and endocrine regulation. Dev. Biol 187, 283–297
    OpenUrlCrossRefPubMedWeb of Science
    1. Berridge M. J.
    (1997) Lymphocyte activation in health and disease. Crit. Rev. Immunol 17, 155–178
    OpenUrlPubMedWeb of Science
    1. Bownes M.,
    2. Blair M.
    (1986) The effects of a sugar diet and hormones on the expression of the Drosophila yolk-protein genes. J. Insect Physiol 32, 493–501
    OpenUrlCrossRef
    1. Bownes M.,
    2. Reid G.
    (1990) The role of the ovary and nutritional signals in the regulation of fat body yolk protein gene expression in Drosophila melanogaster. J. Insect Physiol 36, 471–479
    OpenUrlCrossRef
    1. Bownes M.,
    2. Scott A.,
    3. Shirras A.
    (1988) Dietary components modulate yolk protein gene transcription in Drosophila melanogaster. Development 103, 119–128
    OpenUrlAbstract
    1. Burke R.,
    2. Basler K.
    (1997) Hedgehog signaling in Drosophila eye and limb development—conserved machinery, divergent roles?. Curr. Opin. Neurobiol 7, 55–61
    OpenUrlCrossRefPubMed
    1. Cui X.,
    2. Doe C. Q.
    (1997) The role of the cell cycle and cytokinesis in regulating neuroblast sublineage gene expression in the Drosophila CNS. Development 121, 3233–3243
    OpenUrlAbstract
    1. Datta S.
    (1995) Control of proliferation activation in quiescent neuroblasts of the Drosophila central nervous system. Development 121, 1173–1182
    OpenUrlAbstract
    1. Davis K. T.,
    2. Shearn A.
    (1977) In vitro growth of imaginal disks from Drosophila melanogaster. Science 196, 438–440
    OpenUrlAbstract/FREE Full Text
    1. Doe C. Q.,
    2. Smouse D. T.
    (1990) The origins of cell diversity in the insect central nervous system. Semin. Cell Biol 1, 211–218
    OpenUrlPubMed
    1. Doe C. Q.,
    2. Technau G. M.
    (1993) Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci 16, 510–514
    OpenUrlCrossRefPubMedWeb of Science
    1. Duronio R. J.,
    2. O'Farrell P. H.
    (1994) Developmental control of a G1-S transcriptional program in Drosophila. Development 120, 1503–1515
    OpenUrlAbstract
    1. Duronio R. J.,
    2. Brook A.,
    3. Dyson N.,
    4. O'Farrell P. H.
    (1996) E2F-induced S phase requires cyclin E. Genes Dev 10, 2505–2513
    OpenUrlAbstract/FREE Full Text
    1. Ebens A. J.,
    2. Garren H.,
    3. Cheyette B. N. R.,
    4. Zipursky S. L.
    (1993) The Drosophilaanachronism locus: A glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74, 15–27
    OpenUrlCrossRefPubMedWeb of Science
    1. Edgar B. E.,
    2. Lehner C. F.
    (1996) Developmental control of cell cycle regulators: A fly's perspective. Science 274, 1646–1652
    OpenUrlAbstract/FREE Full Text
    1. Ito K.,
    2. Hotta Y.
    (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev. Biol 149, 134–148
    OpenUrlCrossRefPubMedWeb of Science
    1. Knoblich J. A.,
    2. Sauer K.,
    3. Jones L.,
    4. Richardson H.,
    5. Saint R.,
    6. Lehner C. F.
    (1994) Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77, 107–120
    OpenUrlCrossRefPubMedWeb of Science
    1. Ohtani K.,
    2. Nevins J. R.
    (1994) Functional properties of a Drosophila homolog of the E2F1 gene. Mol. Cell Biol 14, 1603–1612
    OpenUrlAbstract/FREE Full Text
    1. Pardee A. B.
    (1989) G1 events and regulation of cell proliferation. Science 246, 603–608
    OpenUrlAbstract/FREE Full Text
    1. Peifer M.,
    2. Bejsovec A.
    (1992) Knowing your neighbors: Cell interactions determine intrasegmental patterning in Drosophila. Trends Genet 8, 243–249
    1. Perrimon N.,
    2. Perkins L. A.
    (1997) There must be 50 ways to rule the signal: The case of the Drosophila EGF receptor. Cell 89, 13–16
    OpenUrlCrossRefPubMedWeb of Science
    1. Pignoni F.,
    2. Zipursky S.
    (1997) Induction of Drosophila eye development by decapentaplegic. Development 124, 271–278
    OpenUrlAbstract
    1. Prokop A.,
    2. Technau G. M.
    (1991) The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111, 79–88
    OpenUrlAbstract
    1. Richardson H.,
    2. O'Keefe L. V.,
    3. Marty T.,
    4. Saint R.
    (1995) Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. Development 121, 3371–3379
    OpenUrlAbstract
    1. Robertson F. W.
    (1963) The ecological genetics of growth in Drosophila. 6. The genetic correlation between the duration of the larval period and body size in relation to larval diet. Genet. Res 4, 74–92
    OpenUrlWeb of Science
    1. Royzman I.,
    2. Whittaker A. J.,
    3. Orr-Weaver T. L.
    (1997) Mutations in DrosophilaDP and E2F distinguish G1-S progression from an associated transcriptional program. Genes Dev 11, 1999–2011
    OpenUrlAbstract/FREE Full Text
    1. Schubiger G.
    (1972) Regeneration of Drosophila melanogaster male leg disc fragments in sugar fed female hosts. Experientia 29, 631–632
    1. Siegfried W.,
    2. Perrimon N.
    (1994) Drosophila wingless: A paradigm for the function and mechanism of Wnt signaling. BioEssays 16, 395–404
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith A. V.,
    2. Orr-Weaver T. L.
    (1991) The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development 112, 997–1008
    OpenUrlAbstract
    1. Sondergaard L.,
    2. Mauchline D.,
    3. Egetoft P.,
    4. White N.,
    5. Wulff P.,
    6. Bownes M.
    (1995) Nutritional response in a Drosophila yolk protein gene promoter. Mol. Gen. Genet 248, 25–32
    OpenUrlCrossRefPubMed
    1. Truman J. W.,
    2. Bate M.
    (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol 125, 145–157
    OpenUrlCrossRefPubMedWeb of Science
    1. White K.,
    2. Kankel D. R.
    (1978) Patterns of cell division and cell movement in the formation of the imaginal nervous system in Drosophila melanogaster. Dev. Biol 65, 296–321
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms
J.S. Britton, B.A. Edgar
Development 1998 125: 2149-2158;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights