Regulatory Cohesion of Cell Cycle and Cell Differentiation through Interlinked Phosphorylation and Second Messenger Networks

In Caulobacter crescentus, phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell-cycle progression and differentiation. The diguanylate cyclase PleD directs pole morphogenesis, while the c-di-GMP effector PopA initiates degradation of the replication...

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Published in:	Molecular cell Vol. 43; no. 4; pp. 550 - 560
Main Authors:	Abel, Sören, Chien, Peter, Wassmann, Paul, Schirmer, Tilman, Kaever, Volkhard, Laub, Michael T., Baker, Tania A., Jenal, Urs
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 19-08-2011
Subjects:	Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Proteins - physiology Caulobacter crescentus Caulobacter crescentus - cytology Caulobacter crescentus - metabolism Caulobacter crescentus - physiology Cell Cycle - physiology cell differentiation Cell Polarity cohesion degradation interphase metabolism Models, Biological morphogenesis Phosphoric Diester Hydrolases - metabolism Phosphoric Diester Hydrolases - physiology Phosphorylation proteases protein degradation proteinases Second Messenger Systems
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Abstract	In Caulobacter crescentus, phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell-cycle progression and differentiation. The diguanylate cyclase PleD directs pole morphogenesis, while the c-di-GMP effector PopA initiates degradation of the replication inhibitor CtrA by the AAA+ protease ClpXP to license S phase entry. Here, we establish a direct link between PleD and PopA reliant on the phosphodiesterase PdeA and the diguanylate cyclase DgcB. PdeA antagonizes DgcB activity until the G1-S transition, when PdeA is degraded by the ClpXP protease. The unopposed DgcB activity, together with PleD activation, upshifts c-di-GMP to drive PopA-dependent CtrA degradation and S phase entry. PdeA degradation requires CpdR, a response regulator that delivers PdeA to the ClpXP protease in a phosphorylation-dependent manner. Thus, CpdR serves as a crucial link between phosphorylation pathways and c-di-GMP metabolism to mediate protein degradation events that irreversibly and coordinately drive bacterial cell-cycle progression and development. ► Coordinate action of the DGCs PleD and DgcB control Caulobacter cell cycle and development ► The PDE PdeA opposes DgcB and thereby determines the swarmer cell-specific program ► Cell cycle-dependent degradation of PdeA releases its antagonist DgcB ► CpdR plays a dual role as protease localization factor and adaptor for PdeA
AbstractList	In Caulobacter crescentus, phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell-cycle progression and differentiation. The diguanylate cyclase PleD directs pole morphogenesis, while the c-di-GMP effector PopA initiates degradation of the replication inhibitor CtrA by the AAA+ protease ClpXP to license S phase entry. Here, we establish a direct link between PleD and PopA reliant on the phosphodiesterase PdeA and the diguanylate cyclase DgcB. PdeA antagonizes DgcB activity until the G1-S transition, when PdeA is degraded by the ClpXP protease. The unopposed DgcB activity, together with PleD activation, upshifts c-di-GMP to drive PopA-dependent CtrA degradation and S phase entry. PdeA degradation requires CpdR, a response regulator that delivers PdeA to the ClpXP protease in a phosphorylation-dependent manner. Thus, CpdR serves as a crucial link between phosphorylation pathways and c-di-GMP metabolism to mediate protein degradation events that irreversibly and coordinately drive bacterial cell-cycle progression and development. In Caulobacter crescentus , phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell cycle progression and differentiation. The diguanylate cyclase PleD directs pole morphogenesis while the c-di-GMP effector PopA initiates degradation of the replication inhibitor CtrA by the AAA+ protease ClpXP to license S-phase entry. Here we establish a direct link between PleD and PopA reliant on the phosphodiesterase PdeA and the diguanylate cyclase DgcB. PdeA antagonizes DgcB activity until the G1-S transition when PdeA is degraded by the ClpXP protease. The unopposed DgcB activity, together with PleD activation, upshifts c-di-GMP to drive PopA-dependent CtrA degradation and S-phase entry. PdeA degradation requires CpdR, a response regulator that delivers PdeA to the ClpXP protease in a phosphorylation-dependent manner. Thus, CpdR serves as a crucial link between phosphorylation pathways and c-di-GMP metabolism to mediate protein degradation events that irreversibly and coordinately drive bacterial cell cycle progression and development. In Caulobacter crescentus, phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell-cycle progression and differentiation. The diguanylate cyclase PleD directs pole morphogenesis, while the c-di-GMP effector PopA initiates degradation of the replication inhibitor CtrA by the AAA+ protease ClpXP to license S phase entry. Here, we establish a direct link between PleD and PopA reliant on the phosphodiesterase PdeA and the diguanylate cyclase DgcB. PdeA antagonizes DgcB activity until the G1-S transition, when PdeA is degraded by the ClpXP protease. The unopposed DgcB activity, together with PleD activation, upshifts c-di-GMP to drive PopA-dependent CtrA degradation and S phase entry. PdeA degradation requires CpdR, a response regulator that delivers PdeA to the ClpXP protease in a phosphorylation-dependent manner. Thus, CpdR serves as a crucial link between phosphorylation pathways and c-di-GMP metabolism to mediate protein degradation events that irreversibly and coordinately drive bacterial cell-cycle progression and development. ► Coordinate action of the DGCs PleD and DgcB control Caulobacter cell cycle and development ► The PDE PdeA opposes DgcB and thereby determines the swarmer cell-specific program ► Cell cycle-dependent degradation of PdeA releases its antagonist DgcB ► CpdR plays a dual role as protease localization factor and adaptor for PdeA
Author	Chien, Peter Abel, Sören Kaever, Volkhard Wassmann, Paul Baker, Tania A. Schirmer, Tilman Laub, Michael T. Jenal, Urs
AuthorAffiliation	2 Massachusetts Institute of Technology, Department of Biology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA 1 Biozentrum of the University of Basel, Klingelbergstrasse 50, CH-4054 Basel, Switzerland 4 Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02139, USA 3 Institute of Pharmacology, Hannover Medical School, 30625 Hannover, Germany
AuthorAffiliation_xml	– name: 1 Biozentrum of the University of Basel, Klingelbergstrasse 50, CH-4054 Basel, Switzerland – name: 2 Massachusetts Institute of Technology, Department of Biology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA – name: 3 Institute of Pharmacology, Hannover Medical School, 30625 Hannover, Germany – name: 4 Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
Author_xml	– sequence: 1 givenname: Sören surname: Abel fullname: Abel, Sören organization: Biozentrum of the University of Basel, Klingelbergstrasse 50, CH-4054 Basel, Switzerland – sequence: 2 givenname: Peter surname: Chien fullname: Chien, Peter organization: Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA – sequence: 3 givenname: Paul surname: Wassmann fullname: Wassmann, Paul organization: Biozentrum of the University of Basel, Klingelbergstrasse 50, CH-4054 Basel, Switzerland – sequence: 4 givenname: Tilman surname: Schirmer fullname: Schirmer, Tilman organization: Biozentrum of the University of Basel, Klingelbergstrasse 50, CH-4054 Basel, Switzerland – sequence: 5 givenname: Volkhard surname: Kaever fullname: Kaever, Volkhard organization: Institute of Pharmacology, Hannover Medical School, 30625 Hannover, Germany – sequence: 6 givenname: Michael T. surname: Laub fullname: Laub, Michael T. organization: Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA – sequence: 7 givenname: Tania A. surname: Baker fullname: Baker, Tania A. organization: Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA – sequence: 8 givenname: Urs surname: Jenal fullname: Jenal, Urs email: urs.jenal@unibas.ch organization: Biozentrum of the University of Basel, Klingelbergstrasse 50, CH-4054 Basel, Switzerland
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21855795$$D View this record in MEDLINE/PubMed
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Snippet	In Caulobacter crescentus, phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell-cycle progression and... In Caulobacter crescentus, phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell-cycle progression and... In Caulobacter crescentus , phosphorylation of key regulators is coordinated with the second messenger cyclic di-GMP to drive cell cycle progression and...
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SubjectTerms	Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Proteins - physiology Caulobacter crescentus Caulobacter crescentus - cytology Caulobacter crescentus - metabolism Caulobacter crescentus - physiology Cell Cycle - physiology cell differentiation Cell Polarity cohesion degradation interphase metabolism Models, Biological morphogenesis Phosphoric Diester Hydrolases - metabolism Phosphoric Diester Hydrolases - physiology Phosphorylation proteases protein degradation proteinases Second Messenger Systems
Title	Regulatory Cohesion of Cell Cycle and Cell Differentiation through Interlinked Phosphorylation and Second Messenger Networks
URI	https://dx.doi.org/10.1016/j.molcel.2011.07.018 https://www.ncbi.nlm.nih.gov/pubmed/21855795 https://search.proquest.com/docview/884848064 https://pubmed.ncbi.nlm.nih.gov/PMC3298681
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