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Research Article

A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program

Krista M. Giglio, Nora Caberoy, Garret Suen, Dale Kaiser, and Anthony G. Garza
PNAS August 9, 2011 108 (32) E431-E439; first published June 13, 2011; https://doi.org/10.1073/pnas.1105876108
Krista M. Giglio
aDepartment of Biology, Syracuse University, Syracuse, NY 13244;
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Nora Caberoy
bDepartment of Ophthalmology, Bascom Palmer Eye Institute, University of Miami School of Medicine, Miami, FL 33136;
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Garret Suen
cDepartment of Bacteriology, University of Wisconsin-Madison, Madison, WI 53706; and
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Dale Kaiser
dDepartment of Biochemistry, Stanford University School of Medicine, Stanford, CA 94305
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Anthony G. Garza
aDepartment of Biology, Syracuse University, Syracuse, NY 13244;
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  • For correspondence: agarza@syr.edu
  1. Edited by Emil C. Gotschlich, The Rockefeller University, New York, NY, and approved May 12, 2011 (received for review April 27, 2011)

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  • A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program
    - Jun 13, 2011
  • A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program
    - Jun 13, 2011
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Abstract

The signal transduction networks that initiate multicellular development in bacteria remain largely undefined. Here, we report that Myxococcus xanthus regulates entry into its multicellular developmental program using a novel strategy: a cascade of transcriptional activators known as enhancer binding proteins (EBPs). The EBPs in the cascade function in sequential stages of early development, and several lines of evidence indicate that the cascade is propagated when EBPs that function at one stage of development directly regulate transcription of an EBP gene important for the next developmental stage. We also show that the regulatory cascade is designed in a novel way that extensively expands on the typical use of EBPs: Instead of using only one EBP to regulate a particular gene or group of genes, which is the norm in other bacterial systems, the cascade uses multiple EBPs to regulate EBP genes that are positioned at key transition points in early development. Based on the locations of the putative EBP promoter binding sites, several different mechanisms of EBP coregulation are possible, including the formation of coregulating EBP transcriptional complexes. We propose that M. xanthus uses an EBP coregulation strategy to make expression of EBP genes that modulate stage-stage transitions responsive to multiple signal transduction pathways, which provide information that is important for a coordinated decision to advance the developmental process.

  • σ54 promoters
  • biofilms
  • two-component systems

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: agarza{at}syr.edu.
  • Author contributions: A.G.G. designed research; K.M.G. and N.C. performed research; G.S. contributed new reagents/analytic tools; K.M.G., N.C., and A.G.G. analyzed data; and K.M.G., D.K., and A.G.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • See Author Summary on page 12981.

  • Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE13523).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1105876108/-/DCSupplemental.

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A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program
Krista M. Giglio, Nora Caberoy, Garret Suen, Dale Kaiser, Anthony G. Garza
Proceedings of the National Academy of Sciences Aug 2011, 108 (32) E431-E439; DOI: 10.1073/pnas.1105876108

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A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program
Krista M. Giglio, Nora Caberoy, Garret Suen, Dale Kaiser, Anthony G. Garza
Proceedings of the National Academy of Sciences Aug 2011, 108 (32) E431-E439; DOI: 10.1073/pnas.1105876108
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