Skip to main content
SpringerLink
Log in

Mitosis in neoplastic and hyperplastic imaginal discs ofDrosophila

  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Homozygosity for recessive mutations inDrosophila tumour suppressor genes likelethal giant larvae (Igl), lethal giant discs (Igd) orfat (ft) induce uncontrolled cell proliferations in the imaginal discs of the mutant larvae. Imaginal discs of larvae mutant forIgl tumour suppressor gene display neoplastic growths while those mutant forIgd orfat display hyperplastic growths. Results presented in this study reveal that mutant wing imaginal discs with neoplastic or hyperplastic overgrowths display high mitotic activity primarily during the extended period of larval life when their wild-type siblings have already pupariated. Both these categories of overgrowths show overall stability of the karyotypes and only low frequency of aneuploidy. The hyperplastic imaginal discs ofIgd orft mutant larvae displayed normal chromosome condensation. In contrast, the neoplastic imaginal discs ofIgl mutants showed high frequency of mitotic cells with undercondensed chromosomes. In this respect the neoplastic discs resemble malignant neuroblastomas of theIgl larvae which also display undercondensed chromosomes. These results thus suggest an indirect role of the cytoskeletal protein encoded byIgl tumour suppressor gene in aspects of normal chromosome condensation during mitosis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agrawal N., Joshi S., Kango M., Saha D., Mishra A. and Sinha P. 1995 Epithelial hyperplasia of imaginal discs induced by mutations inDrosophila tumour suppressor genes: growth and pattern formation in genetic mosaics.Dev. Biol. 169: 387–398

    Article  PubMed  CAS  Google Scholar 

  • Bryant P. J. 1987 Experimental and genetic analysis of growth and cell proliferation inDrosophila imaginal discs. InGenetic regulation of Drosophila, Proceedings of the 45th Annual Symposium of the Society of Developmental Biologists (ed.) W. F. Loomis (New York: Liss) pp. 339–372

    Google Scholar 

  • Bryant P. J. and Levinson P. 1985 Intrinsic growth control in the imaginal disc primordia ofDrosophila and the autonomous action of a lethal mutation causing overgrowth.Dev. Biol. 107: 355–363

    Article  PubMed  CAS  Google Scholar 

  • Bryant P. J. And Schubiger G. 1971 Giant and duplicated imaginal discs in a new lethal mutant ofDrosophila melanogaster.Dev. Biol. 27: 233–263

    Article  Google Scholar 

  • Bryant P. J., Heuttner B., Held L. I., Ryerse J. and Szidonya J. 1988 Mutation at thefat locus interface with cell proliferation and epithelial morphogenesis inDrosophila.Dev. Biol. 129: 541–554

    Article  PubMed  CAS  Google Scholar 

  • Bryant P. J., Watson K. L., Justice R. S. and Woods D. F. 1993 Tumour suppressor genes encoding proteins required for cell interactions and signal transduction inDrosophila. Development (suppl.) 239–249

  • Gateff E. 1978 Malignant neoplasms of genetic origin inDrosophila melanogaster.Science 200: 1448–1459

    Article  PubMed  CAS  Google Scholar 

  • Gateff E. 1994 Tumour suppressor and overgrowth suppressor genes ofDrosophila melanogaster: developmental aspects.Int. J. Dev. Biol. 38: 565–590

    PubMed  CAS  Google Scholar 

  • Gatti M. and Baker B. S. 1989 Genes controlling essential cell functions inDrosophila melanogaster.Genes Dev. 3: 438–453

    Article  PubMed  CAS  Google Scholar 

  • Gatti M., Smith D. A. and Baker B. S. 1983 A gene controlling condensation of heterochromatin inDrosophila melanogaster.Science 221: 83–85

    Article  PubMed  CAS  Google Scholar 

  • Glover D. M. 1989 Mitosis inDrosophila.J. Cell Sci. 92: 137–146

    PubMed  Google Scholar 

  • Jacob L., Opper M., Metzroth B., Phannavong B. and Mechler B. M. 1987 Structure of the1(2)gl gene ofDrosophila and delimitation of its tumour suppressor domain.Cell 50: 215–225

    Article  PubMed  CAS  Google Scholar 

  • Knudson A. G. Jr. 1986 Genetics of human cancer.Anna. Rev. Genet. 20: 231–251

    Article  Google Scholar 

  • Kuhn E. M. and Therman E. 1986 Cytogenetics of Bloom’s syndrome.Cancer Genet. Cytogenet. 22: 1–18

    Article  PubMed  CAS  Google Scholar 

  • Lakhotia S. C, Roy J. K. and Kumar M. 1979 A study of heterochromatin inDrosophila nasuta by the 5-bromodeoxy-uridine-Giemsa staining technique.Chromosoma 72: 249–255

    Article  PubMed  CAS  Google Scholar 

  • Lakhotia S. C, Roy J. K. and Chowdhuri S. K. 1995 Cell cycle and DNA content of mitotic cells in brain ganglia ofDrosophila larvae.J. Biosci. 20: 175–195

    Article  Google Scholar 

  • Lindsley D. L. and Zimm G. G. 1992The genome of Drosophila melanogaster (San Diego: Academic Press)

    Google Scholar 

  • Mechler B. M. 1994 When the control is lacking—the role of tumour suppressor genes in cancer development.J. Biosci. 55: 213–232

    Google Scholar 

  • Mechler B. M., McGinnis W. and Gehring W. J. 1985 Molecular cloning oflethal(2)giant larvae, a recessive oncogene ofDrosophila melanogaster.EMBO J. 4: 1551–1557

    PubMed  CAS  Google Scholar 

  • Neumann B., Merdes G., Strand D. and Mechler B. M. 1996 Association between the tumour suppressor pl271(2)gl and a related nucleosome-assembly-protein-1, NAP-1, suggests a new mechanism in the regulation of cell proliferation. Abstract, 37th Drosophila Research Conference, San Diego, USA

  • Opper M., Schuler G. and Mechler B. M. 1987 Hereditary suppression oflethal(2)giant larvae malignant tumour development inDrosophila by gene transfer.Oncogene 1: 91–96

    PubMed  CAS  Google Scholar 

  • Radhakrishnan V. 1989 Chromosomal organizationof Drosophila neuroblastoma. Ph. D thesis, Devi Ahilya Vishwavidyalaya, Indore, India

  • Radhakrishnan V. and Sinha P. 1987 Mitotic chromosome organization of neuroblastomas induced by the recessive oncogenelethal(2)giant larvae4 of Drosophila melanogaster.Chromosoma 96: 77–82

    Article  PubMed  CAS  Google Scholar 

  • Roy S. and Lakhotia S. C. 1991In situ patterns of nuclear replication in brain ganglia ofl(2)gl4 mutant larvaeof Drosophila melanogaster.J. Genet. 70: 161–168

    Article  Google Scholar 

  • Strand D., Raska I. and Mechler B. M. 1994a TheDrosophila lethal (2) giant larvae tumour suppressor protein is a component of the cytoskeleton.J. Cell Biol. 121: 1345–1360

    Article  Google Scholar 

  • Strand D., Jakobs R., Merdes G., Neumann B., Kalmes A., Heid H. W., Husmann I. and Mechler B. M. 1994b TheDrosophila melanogaster lethal(2)giant larvae tumour suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain.J. Cell Biol. 127: 1361–1373

    Article  PubMed  CAS  Google Scholar 

  • Török R., Harvie P. D., Buratovich M. and Bryant P. J. 1997 The product ofproliferation disrupter is concentrated at centromeres and required for mitotic chromosome condensation and cell proliferation inDrosophila.Genes Dev. 11: 213–225

    Article  PubMed  Google Scholar 

  • Woods D. F. and Bryant P. J. 1989 Molecular cloning of thelethal (1) discs large-1 oncogeneof Drosophila melanogaster.Dev. Biol. 134: 222–235

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Drosophila Stock Center, School of Life Sciences, Devi Ahilya Vishwavidyalaya, Vigyan Bhawan, Khandwa Road Campus, 452001, Indore, India

    Arati Mishra, Verneth Radhakrishnan, Sunita Sardesai, Namita Agrawal & Pradip Sinha

Authors
  1. Arati Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Verneth Radhakrishnan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sunita Sardesai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Namita Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pradip Sinha
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mishra, A., Radhakrishnan, V., Sardesai, S. et al. Mitosis in neoplastic and hyperplastic imaginal discs ofDrosophila . J. Genet. 76, 209–220 (1997). https://doi.org/10.1007/BF02932219

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02932219

Keywords

Search

Navigation