Morphogenetic apoptosis: A mechanism for correcting discontinuities in morphogen gradients

Takashi Adachi-Yamada, Michael B. O'Connor

Research output: Contribution to journalArticlepeer-review

112 Scopus citations

Abstract

Smooth gradients of the morphogens Hh, Dpp, and Wg are required for proper development of Drosophila imaginal discs. Here, it is reported that, when a discontinuity is generated between two adjacent cells in the reception of either the Dpp or Wg signal, then cells on either side of the discontinuity boundary undergo apoptosis by activating the c-Jun N-terminal Kinase (JNK) pathway. Furthermore, in the medial region of the wing imaginal disc, the JNK pathway is also activated if cells do not receive the proper levels of Dpp and Hh signals. These observations suggest that cells within a developing field have the ability to access their spatial positions by comparing the level of morphogen signal they receive with that of their neighbors. This phenomenon is likely related to the process of cell competition, and we suggest that it is an evolutionarily important mechanism that helps prevent abnormal tissue specification and growth during development.

Original languageEnglish (US)
Pages (from-to)74-90
Number of pages17
JournalDevelopmental Biology
Volume251
Issue number1
DOIs
StatePublished - 2002

Bibliographical note

Funding Information:
We thank K. Basler, S. B. Carroll, W. J. Gehring, S. Goto, Y. Hiromi, Y. H. Inoue, W. Janning, M. Nakamura, G. Marques, E. Martín-Blanco, A. Martinez-Arias, S. Noselli, M. Peifer, G. O. Pflugfelder, G. Struhl, T. Tabata, K. Takahashi, D. Yamamoto, and the Bloomington Stock Center for the fly strains; P. ten Dijke for the anti-phospho-Mad antibody; the Developmental Studies Hybridoma Bank at the University of Iowa for anti-Arm antibody; T. Neufeld for technical advice; T. Neufeld, J. Simon, and G. Marqués for comments on the manuscript, and Y. Aoki for technical assistance. This work was supported by grants from Japan Science and Technology Corporation and Ministry of Education, Science, Sports and Culture in Japan. M.B.O. is an Associate Investigator of the Howard Hughes Medical Institute.

Keywords

  • Apoptosis
  • Caspase-3
  • Cell autonomy
  • Decapentaplegic
  • Drosophila
  • Hedgehog
  • JNK
  • Morphogen gradient
  • Noncell autonomy
  • Wingless

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