Skip to main content
Log in

Ectopic expression of the Suppressor of Underreplication gene inhibits endocycles but not the mitotic cell cycle in Drosophila melanogaster

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The Suppressor of Underreplication ( SuUR) gene contributes to the regulation of DNA replication in regions of intercalary heterochromatin in salivary gland polytene chromosomes. In the SuUR mutant these regions complete replication earlier than in wild type and, as a consequence, undergo full polytenization. Here we describe the effects of ectopic expression of SuUR using the GAL4-UAS system. We demonstrate that ectopically expressed SuUR exerts qualitatively distinct influences on polyploid and diploid tissues. Ectopic expression of SuUR inhibits DNA replication in polytene salivary gland nuclei, and reduces the degree of amplification of chorion protein genes that occurs in the follicle cell lineage. Effects caused by ectopic SuUR in diploid tissues vary considerably; there is no obvious effect on eye formation, but apoptosis is observed in the wing disc, and wing shape is distorted. The effect of ectopic SuUR expression is enhanced by mutations in the genes E2F and mus209 ( PCNA). Differential responses of polyploid and diploid cells to ectopic SuUR may reflect differences in the mechanisms underlying mitotic cell cycles and endocycles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A, B
Fig. 2A–D
Fig. 3A–H

Similar content being viewed by others

References

  • Abrams JM, White K, Fessler LI, Steller H (1993) Programmed cell death during Drosophila embryogenesis. Development 117:29–43

    CAS  PubMed  Google Scholar 

  • Belyaeva ES, Zhimulev IF, Volkova EI, Alekseyenko AA, Moshkin YM, Koryakov DE (1998) Su(UR)ES: A gene suppressing DNA underreplication in intercalary and pericentric heterochromatin of Drosophila melanogaster polytene chromosomes. Proc Natl Acad Sci USA 95:7532–7537

    Article  CAS  PubMed  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    CAS  PubMed  Google Scholar 

  • Burgers PMJ (1998) Eukaryotic DNA polymerases in DNA replication and DNA repair. Chromosoma 107:218–227

    Article  CAS  PubMed  Google Scholar 

  • Calvi BR, Lilly MA, Spradling AC (1998) Cell cycle control of chorion gene amplification. Genes Dev 12:734–744

    CAS  PubMed  Google Scholar 

  • Capdevila J, Guerrero I (1994) Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J 13:4459–4468

    CAS  PubMed  Google Scholar 

  • Chesnokov I, Gossen M, Remus D, Botchan M (1999) Assembly of functionally active Drosophila origin recognition complex from recombinant proteins. Genes Dev 13:1289–1296

    CAS  PubMed  Google Scholar 

  • Datar SA, Jacobs HW, de La Cruz AF, Lehner CF, Edgar BA (2000) The Drosophila cyclin D-cdk4 complex promotes cellular growth. EMBO J 19:4543–4554

    Article  CAS  PubMed  Google Scholar 

  • Dyson N (1998) The regulation of E2F by pRB-family proteins. Genes Dev 12:2245–2262

    CAS  PubMed  Google Scholar 

  • Edgar BA, Orr-Weaver TL (2001) Endoreplication cell cycles: more for less. Cell 105:297–306

    CAS  PubMed  Google Scholar 

  • Edgar BA, Britton J, Johnston LA, Reis T, Prober D, de la Cruz A (2001) Growth-linked and pattern-linked cell cycles in Drosophila. Cell Biol Int Rep 25:A2–A3

    Google Scholar 

  • Follette PJ, Duronio RJ, O'Farrell PH (1998) Fluctuations in cyclin E levels are required for multiple rounds of endocycle S phase in Drosophila. Curr Biol 8:235–238

    CAS  PubMed  Google Scholar 

  • Harrington M, Whalen J, Grigliatti T (1994) Isolation and initial characterization of P-element induced Enhancers of position-effect variegation. Abstracts Dros Res Conf 35:324

    Google Scholar 

  • Heck MMS, Spradling AC (1990) Multiple replication origins are used during Drosophila chorion gene amplification. J Cell Biol 110:903–914

    CAS  PubMed  Google Scholar 

  • Henderson DS, Banga SS, Grigliatti TA, Boyd JB (1994) Mutagen sensitivity and suppression of position-effect variegation result from mutations in mus209, the Drosophila gene encoding PCNA. EMBO J 13:1450–1459

    CAS  PubMed  Google Scholar 

  • Hirose F, Yamaguchi M, Matsukage A (1999) Targeted expression of the DNA binding domain of DRE-binding factor, a Drosophila transcription factor, attenuates DNA replication of the salivary gland and eye imaginal disc. Mol Cell Biol 19:6020–6028

    CAS  PubMed  Google Scholar 

  • Ito K, Awano W, Yamamoto D (1997) Cell lineage analysis of adult fly brains using the FLIPPASE/FRT and GAL4/UAS systems. J Neurogenet 11:164–165

    Google Scholar 

  • Lilly MA, Spradling AC (1996) The Drosophila endocycle is controlled by cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev 10:2514–2526

    PubMed  Google Scholar 

  • Loupart M, Krause SA, Heck MMS (2000) Aberrant replication timing induces defective chromosome condensation in Drosophila ORC2 mutants. Curr Biol 10:1547–1556

    CAS  PubMed  Google Scholar 

  • Lunde K, Biehs B, Nauber U, Bier E (1998) The knirps and knirps-related genes organize development of the second wing vein in Drosophila. Development 125:4145–4154

    CAS  PubMed  Google Scholar 

  • Makunin IV, Volkova EI, Belyaeva ES, Nabirochkina EN, Pirrotta V, Zhimulev IF (2002) The Drosophila suppressor of underreplication protein binds to late-replicating regions of polytene chromosomes. Genetics 160:1023–1034

    CAS  PubMed  Google Scholar 

  • Manseau L, Baradaran A, Brower D, Budhu A, Elefant F, Phan H, Philip AV, Yang M, Glover D, Kaiser K, Palter K, Selleck S (1997) GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dynamics 209:310–322

    Article  CAS  Google Scholar 

  • Milan M (1998) Cell cycle control in the Drosophila wing. Bioessays 20:969–971

    Article  CAS  PubMed  Google Scholar 

  • Pflumm MF, Botchan MR (2001) Orc mutants arrest in metaphase with abnormally condensed chromosomes. Development 128:1697–1707

    CAS  PubMed  Google Scholar 

  • Richardson H, O'Keefe LV, Marty T, 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

    CAS  PubMed  Google Scholar 

  • Sauer K, Knoblich JA, Richardson H, Lehner CF (1995) Distinct modes of cyclin E/cdc2c kinase regulation and S-phase control in mitotic and endoreduplication cycles of Drosophila embryogenesis. Genes Dev 9:1327–1339

    CAS  PubMed  Google Scholar 

  • Smith AV, Orr-Weaver TL (1991) The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development 112:997–1008

    CAS  PubMed  Google Scholar 

  • Staehling-Hampton K, Ciampa PJ, Brook A, Dyson N (1999) A genetic screen for modifiers of E2F in Drosophila melanogaster. Genetics 153:275–287

    CAS  Google Scholar 

  • The FlyBase Consortium (2003) The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Research 31:172–175

    Article  PubMed  Google Scholar 

  • Treisman JE, Follette PJ, O'Farrell PH, Rubin GM (1995) Cell proliferation and DNA replication defects in a Drosophila MCM2 mutant. Genes Dev 9:1709–1715

    CAS  PubMed  Google Scholar 

  • Weiss A, Herzig A, Jacobs H, Lehner CF (1998) Continuous cyclin E expression inhibits progression through endoreduplication cycles in Drosophila. Curr Biol 8:239–242

    CAS  PubMed  Google Scholar 

  • Wodarz A, Hinz U, Engelbert M, Knust E (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82:67–76

    CAS  PubMed  Google Scholar 

  • Zhimulev IF, Belyaeva ES, Makunin IV, Pirrotta V, Volkova EI, Alekseyenko AA, Andreyeva EN, Makarevich GF, Boldyreva LV, Nanayev RA, Demakova OV (2003a) Influence of the SuUR gene on intercalary heterochromatin in Drosophila melanogaster polytene chromosomes. Chromosoma 111:377–398

    CAS  PubMed  Google Scholar 

  • Zhimulev IF, Belyaeva ES, Semeshin VF, Shloma VV, Makunin IV, Volkova EI (2003b) Overexpression of the SuUR gene induces reversible modifications at pericentric, telomeric and intercalary heterochromatin of Drosophila melanogaster polytene chromosomes. J Cell Sci 116:169–176

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Gines Morata, Lynn Manseau, Carole Seum, Francois Karch, Yuri Moshkin and Bloomington Drosophila Stock Center for providing fly stocks. The work was supported by grants from the program "Frontiers in Genetics" of the Russian Federation (Grant 2-02 PNG), the RFBR program 02-04-48222 and the program for Physical-Chemical Biology. The experiments comply with the current laws of the Russian Federation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. F. Zhimulev.

Additional information

Communicated by G. P. Georgiev

Rights and permissions

Reprints and permissions

About this article

Cite this article

Volkova, E.I., Yurlova, A.A., Kolesnikova, T.D. et al. Ectopic expression of the Suppressor of Underreplication gene inhibits endocycles but not the mitotic cell cycle in Drosophila melanogaster . Mol Genet Genomics 270, 387–393 (2004). https://doi.org/10.1007/s00438-003-0924-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-003-0924-1

Keywords

Navigation