Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc

H Richardson, L V O'Keefe, T Marty, R Saint

Research output: Contribution to journalArticle

166 Citations (Scopus)

Abstract

During animal development, cell proliferation is controlled in many cases by regulation of the G1 to S phase transition. Studies of mammalian tissue culture cells have shown that the G1-specific cyclin, cyclin E, can be rate limiting for progression from G1 to S phase. During Drosophila development, down-regulation of cyclin E is required for G1 arrest in terminally differentiating embryonic epidermal cells. Whether cyclin E expression limits progression into S phase in proliferating, as opposed to differentiating, cells during development has not been investigated. Here we show that Drosophila cyclin E (DmcycE) protein is absent in G1 phase cells but appears at the onset of S phase in proliferating cells of the larval optic lobe and eye imaginal disc. We have examined cells in the eye imaginal epithelium, where a clearly defined developmentally regulated G1 to S phase transition occurs. Ectopic expression of DmcycE induces premature entry of most of these G1 cells into S phase. Thus in these cells, control of DmcycE expression is required for regulated entry into S phase. Significantly, a band of eye imaginal disc cells in G1 phase was not induced to enter S phase by ectopic expression of DmcycE. This provides evidence for additional regulatory mechanisms that operate during G1 phase to limit cell proliferation during development. These results demonstrate that the role of cyclin E in regulating progression into S phase in mammalian tissue culture cells applies to some, but not all, cells during Drosophila development.(ABSTRACT TRUNCATED AT 250 WORDS)

LanguageEnglish
Pages3371-9
Number of pages9
JournalDevelopment
Volume121
Issue number10
Publication statusPublished - Oct 1995
Externally publishedYes

Keywords

  • Animals
  • Base Sequence
  • Cell Division
  • Cyclins
  • DNA Primers
  • Drosophila
  • Eye
  • G1 Phase
  • Gene Expression
  • Genes, Insect
  • In Situ Hybridization
  • Molecular Sequence Data
  • Morphogenesis
  • S Phase
  • Journal Article
  • Research Support, Non-U.S. Gov't

Cite this

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title = "Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc",
abstract = "During animal development, cell proliferation is controlled in many cases by regulation of the G1 to S phase transition. Studies of mammalian tissue culture cells have shown that the G1-specific cyclin, cyclin E, can be rate limiting for progression from G1 to S phase. During Drosophila development, down-regulation of cyclin E is required for G1 arrest in terminally differentiating embryonic epidermal cells. Whether cyclin E expression limits progression into S phase in proliferating, as opposed to differentiating, cells during development has not been investigated. Here we show that Drosophila cyclin E (DmcycE) protein is absent in G1 phase cells but appears at the onset of S phase in proliferating cells of the larval optic lobe and eye imaginal disc. We have examined cells in the eye imaginal epithelium, where a clearly defined developmentally regulated G1 to S phase transition occurs. Ectopic expression of DmcycE induces premature entry of most of these G1 cells into S phase. Thus in these cells, control of DmcycE expression is required for regulated entry into S phase. Significantly, a band of eye imaginal disc cells in G1 phase was not induced to enter S phase by ectopic expression of DmcycE. This provides evidence for additional regulatory mechanisms that operate during G1 phase to limit cell proliferation during development. These results demonstrate that the role of cyclin E in regulating progression into S phase in mammalian tissue culture cells applies to some, but not all, cells during Drosophila development.(ABSTRACT TRUNCATED AT 250 WORDS)",
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Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. / Richardson, H; O'Keefe, L V; Marty, T; Saint, R.

In: Development, Vol. 121, No. 10, 10.1995, p. 3371-9.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc

AU - Richardson, H

AU - O'Keefe, L V

AU - Marty, T

AU - Saint, R

PY - 1995/10

Y1 - 1995/10

N2 - During animal development, cell proliferation is controlled in many cases by regulation of the G1 to S phase transition. Studies of mammalian tissue culture cells have shown that the G1-specific cyclin, cyclin E, can be rate limiting for progression from G1 to S phase. During Drosophila development, down-regulation of cyclin E is required for G1 arrest in terminally differentiating embryonic epidermal cells. Whether cyclin E expression limits progression into S phase in proliferating, as opposed to differentiating, cells during development has not been investigated. Here we show that Drosophila cyclin E (DmcycE) protein is absent in G1 phase cells but appears at the onset of S phase in proliferating cells of the larval optic lobe and eye imaginal disc. We have examined cells in the eye imaginal epithelium, where a clearly defined developmentally regulated G1 to S phase transition occurs. Ectopic expression of DmcycE induces premature entry of most of these G1 cells into S phase. Thus in these cells, control of DmcycE expression is required for regulated entry into S phase. Significantly, a band of eye imaginal disc cells in G1 phase was not induced to enter S phase by ectopic expression of DmcycE. This provides evidence for additional regulatory mechanisms that operate during G1 phase to limit cell proliferation during development. These results demonstrate that the role of cyclin E in regulating progression into S phase in mammalian tissue culture cells applies to some, but not all, cells during Drosophila development.(ABSTRACT TRUNCATED AT 250 WORDS)

AB - During animal development, cell proliferation is controlled in many cases by regulation of the G1 to S phase transition. Studies of mammalian tissue culture cells have shown that the G1-specific cyclin, cyclin E, can be rate limiting for progression from G1 to S phase. During Drosophila development, down-regulation of cyclin E is required for G1 arrest in terminally differentiating embryonic epidermal cells. Whether cyclin E expression limits progression into S phase in proliferating, as opposed to differentiating, cells during development has not been investigated. Here we show that Drosophila cyclin E (DmcycE) protein is absent in G1 phase cells but appears at the onset of S phase in proliferating cells of the larval optic lobe and eye imaginal disc. We have examined cells in the eye imaginal epithelium, where a clearly defined developmentally regulated G1 to S phase transition occurs. Ectopic expression of DmcycE induces premature entry of most of these G1 cells into S phase. Thus in these cells, control of DmcycE expression is required for regulated entry into S phase. Significantly, a band of eye imaginal disc cells in G1 phase was not induced to enter S phase by ectopic expression of DmcycE. This provides evidence for additional regulatory mechanisms that operate during G1 phase to limit cell proliferation during development. These results demonstrate that the role of cyclin E in regulating progression into S phase in mammalian tissue culture cells applies to some, but not all, cells during Drosophila development.(ABSTRACT TRUNCATED AT 250 WORDS)

KW - Animals

KW - Base Sequence

KW - Cell Division

KW - Cyclins

KW - DNA Primers

KW - Drosophila

KW - Eye

KW - G1 Phase

KW - Gene Expression

KW - Genes, Insect

KW - In Situ Hybridization

KW - Molecular Sequence Data

KW - Morphogenesis

KW - S Phase

KW - Journal Article

KW - Research Support, Non-U.S. Gov't

M3 - Article

VL - 121

SP - 3371

EP - 3379

JO - Development

T2 - Development

JF - Development

SN - 0950-1991

IS - 10

ER -