Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer

Huaqing Cai, Mariko Katoh-Kurasawa, Tetsuya Muramoto, Balaji Santhanam, Yu Long, Lei Li, Masahiro Ueda, Pablo A Iglesias, Gad Shaulsky, Peter N Devreotes

Research output: Contribution to journalArticle

Abstract

Biological oscillations are observed at many levels of cellular organization. In the social amoeba Dictyostelium discoideum, starvation-triggered multicellular development is organized by periodic cyclic adenosine 3′,5′-monophosphate (cAMP) waves, which provide both chemoattractant gradients and developmental signals. We report that GtaC, a GATA transcription factor, exhibits rapid nucleocytoplasmic shuttling in response to cAMP waves. This behavior requires coordinated action of a nuclear localization signal and reversible G protein (heterotrimeric guanine nucleotide-binding protein)-coupled receptor-mediated phosphorylation. Although both are required for developmental gene expression, receptor occupancy promotes nuclear exit of GtaC, which leads to a transient burst of transcription at each cAMP cycle. We demonstrate that this biological circuit filters out high-frequency signals and counts those admitted, thereby enabling cells to modulate gene expression according to the dynamic pattern of the external stimuli.

Original languageEnglish (US)
Article number1249531
JournalScience
Volume343
Issue number6177
DOIs
StatePublished - 2014

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GATA Transcription Factors
Adenosine
Developmental Genes
Gene Expression
Heterotrimeric GTP-Binding Proteins
Nuclear Localization Signals
Amoeba
Dictyostelium
Guanine Nucleotides
Chemotactic Factors
Starvation
Carrier Proteins
Phosphorylation

ASJC Scopus subject areas

  • General
  • Medicine(all)

Cite this

Cai, H., Katoh-Kurasawa, M., Muramoto, T., Santhanam, B., Long, Y., Li, L., ... Devreotes, P. N. (2014). Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. Science, 343(6177), [1249531]. https://doi.org/10.1126/science.1249531

Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. / Cai, Huaqing; Katoh-Kurasawa, Mariko; Muramoto, Tetsuya; Santhanam, Balaji; Long, Yu; Li, Lei; Ueda, Masahiro; Iglesias, Pablo A; Shaulsky, Gad; Devreotes, Peter N.

In: Science, Vol. 343, No. 6177, 1249531, 2014.

Research output: Contribution to journalArticle

Cai, H, Katoh-Kurasawa, M, Muramoto, T, Santhanam, B, Long, Y, Li, L, Ueda, M, Iglesias, PA, Shaulsky, G & Devreotes, PN 2014, 'Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer', Science, vol. 343, no. 6177, 1249531. https://doi.org/10.1126/science.1249531
Cai H, Katoh-Kurasawa M, Muramoto T, Santhanam B, Long Y, Li L et al. Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. Science. 2014;343(6177). 1249531. https://doi.org/10.1126/science.1249531
Cai, Huaqing ; Katoh-Kurasawa, Mariko ; Muramoto, Tetsuya ; Santhanam, Balaji ; Long, Yu ; Li, Lei ; Ueda, Masahiro ; Iglesias, Pablo A ; Shaulsky, Gad ; Devreotes, Peter N. / Nucleocytoplasmic shuttling of a GATA transcription factor functions as a development timer. In: Science. 2014 ; Vol. 343, No. 6177.
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