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Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function
The bacterium Caulobacter crescentus has morphologically and functionally distinct cell poles that undergo sequential changes during the cell cycle. We show that the PopZ oligomeric network forms polar ribosome exclusion zones that change function during cell cycle progression. The parS/ParB chromos...
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Published in: | Molecular microbiology 2010-04, Vol.76 (1), p.173-189 |
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container_title | Molecular microbiology |
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creator | Bowman, Grant R Comolli, Luis R Gaietta, Guido M Fero, Michael Hong, Sun-Hae Jones, Ying Lee, Julie H Downing, Kenneth H Ellisman, Mark H McAdams, Harley H Shapiro, Lucy |
description | The bacterium Caulobacter crescentus has morphologically and functionally distinct cell poles that undergo sequential changes during the cell cycle. We show that the PopZ oligomeric network forms polar ribosome exclusion zones that change function during cell cycle progression. The parS/ParB chromosomal centromere is tethered to PopZ at one pole prior to the initiation of DNA replication. During polar maturation, the PopZ-centromere tether is broken, and the PopZ zone at that pole then switches function to act as a recruitment factor for the ordered addition of multiple proteins that promote the transformation of the flagellated pole into a stalked pole. Stalked pole assembly, in turn, triggers the initiation of chromosome replication, which signals the formation of a new PopZ zone at the opposite cell pole, where it functions to anchor the newly duplicated centromere that has traversed the long axis of the cell. We propose that pole-specific control of PopZ function co-ordinates polar development and cell cycle progression by enabling independent assembly and tethering activities at the two cell poles. |
doi_str_mv | 10.1111/j.1365-2958.2010.07088.x |
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We show that the PopZ oligomeric network forms polar ribosome exclusion zones that change function during cell cycle progression. The parS/ParB chromosomal centromere is tethered to PopZ at one pole prior to the initiation of DNA replication. During polar maturation, the PopZ-centromere tether is broken, and the PopZ zone at that pole then switches function to act as a recruitment factor for the ordered addition of multiple proteins that promote the transformation of the flagellated pole into a stalked pole. Stalked pole assembly, in turn, triggers the initiation of chromosome replication, which signals the formation of a new PopZ zone at the opposite cell pole, where it functions to anchor the newly duplicated centromere that has traversed the long axis of the cell. We propose that pole-specific control of PopZ function co-ordinates polar development and cell cycle progression by enabling independent assembly and tethering activities at the two cell poles.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2010.07088.x</identifier><identifier>PMID: 20149103</identifier><language>eng</language><publisher>Oxford, UK: Oxford, UK : Blackwell Publishing Ltd</publisher><subject>Bacteria ; Bacterial proteins ; Bacterial Proteins - metabolism ; Bacteriology ; Biological and medical sciences ; Caulobacter ; Caulobacter crescentus ; Caulobacter crescentus - metabolism ; Caulobacter crescentus - physiology ; Cell Cycle ; Cell Polarity ; Cells ; Centromere - metabolism ; Chromosomes ; Chromosomes, Bacterial - metabolism ; DNA Replication ; DNA, Bacterial - metabolism ; Fundamental and applied biological sciences. Psychology ; Microbiology ; Microscopy, Electron, Transmission ; Microscopy, Fluorescence ; Microscopy, Immunoelectron ; Miscellaneous ; Models, Biological ; Models, Molecular ; Morphology ; Protein Multimerization ; Ribonucleic acid ; RNA</subject><ispartof>Molecular microbiology, 2010-04, Vol.76 (1), p.173-189</ispartof><rights>2010 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>Copyright Blackwell Publishing Ltd. Apr 2010</rights><rights>2010 Blackwell Publishing Ltd 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913</citedby><cites>FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=22549930$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20149103$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bowman, Grant R</creatorcontrib><creatorcontrib>Comolli, Luis R</creatorcontrib><creatorcontrib>Gaietta, Guido M</creatorcontrib><creatorcontrib>Fero, Michael</creatorcontrib><creatorcontrib>Hong, Sun-Hae</creatorcontrib><creatorcontrib>Jones, Ying</creatorcontrib><creatorcontrib>Lee, Julie H</creatorcontrib><creatorcontrib>Downing, Kenneth H</creatorcontrib><creatorcontrib>Ellisman, Mark H</creatorcontrib><creatorcontrib>McAdams, Harley H</creatorcontrib><creatorcontrib>Shapiro, Lucy</creatorcontrib><title>Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>The bacterium Caulobacter crescentus has morphologically and functionally distinct cell poles that undergo sequential changes during the cell cycle. We show that the PopZ oligomeric network forms polar ribosome exclusion zones that change function during cell cycle progression. The parS/ParB chromosomal centromere is tethered to PopZ at one pole prior to the initiation of DNA replication. During polar maturation, the PopZ-centromere tether is broken, and the PopZ zone at that pole then switches function to act as a recruitment factor for the ordered addition of multiple proteins that promote the transformation of the flagellated pole into a stalked pole. Stalked pole assembly, in turn, triggers the initiation of chromosome replication, which signals the formation of a new PopZ zone at the opposite cell pole, where it functions to anchor the newly duplicated centromere that has traversed the long axis of the cell. We propose that pole-specific control of PopZ function co-ordinates polar development and cell cycle progression by enabling independent assembly and tethering activities at the two cell poles.</description><subject>Bacteria</subject><subject>Bacterial proteins</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Caulobacter</subject><subject>Caulobacter crescentus</subject><subject>Caulobacter crescentus - metabolism</subject><subject>Caulobacter crescentus - physiology</subject><subject>Cell Cycle</subject><subject>Cell Polarity</subject><subject>Cells</subject><subject>Centromere - metabolism</subject><subject>Chromosomes</subject><subject>Chromosomes, Bacterial - metabolism</subject><subject>DNA Replication</subject><subject>DNA, Bacterial - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Microbiology</subject><subject>Microscopy, Electron, Transmission</subject><subject>Microscopy, Fluorescence</subject><subject>Microscopy, Immunoelectron</subject><subject>Miscellaneous</subject><subject>Models, Biological</subject><subject>Models, Molecular</subject><subject>Morphology</subject><subject>Protein Multimerization</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><recordid>eNqNkktv1DAUhSMEokPhL4CFhFhl8CN27AVIaFSgUiuQoBJiY91xnKlHiZ3aCW3_PU5nGB4biBeJc79zc26OiwIRvCT5erVdEiZ4SRWXS4rzW1xjKZc394rFoXC_WGDFcckk_XpUPEppizFhWLCHxVHWVIpgtijaFUxdWIMZbUSfwvANtSH2CQEaQgcRpWndhB6cR40zI4zOb1CyV5P1o4MOmUvwG5tQrmfeIhP6ISQ3uuAR-Aa1kzfz5nHxoIUu2Sf7-3Fx8e7ky-pDefbx_enq7VlpuBSyNJLIiiiJTd0Y3ghMiDJWykrUBioQeZaKyqY2lnECuCam4mBrsBWnAhRhx8WbXd9hWve2MdlmhE4P0fUQb3UAp_-seHepN-G7popxymlu8HLfIIY8ZRp175KxXQfehinpuspemKD83yRjnFdKsUw-_4vchin6_B80UYLnkaXIkNxBJoaUom0PpgnWc-h6q-ds9ZytnkPXd6Hrmyx9-vvQB-HPlDPwYg9AMtC1Ebxx6RdH73zizL3ecdeus7f_bUCfn5_OT1n_bKdvIWjYxPyNi890PnVEEpUX-wEstdHD</recordid><startdate>201004</startdate><enddate>201004</enddate><creator>Bowman, Grant R</creator><creator>Comolli, Luis R</creator><creator>Gaietta, Guido M</creator><creator>Fero, Michael</creator><creator>Hong, Sun-Hae</creator><creator>Jones, Ying</creator><creator>Lee, Julie H</creator><creator>Downing, Kenneth H</creator><creator>Ellisman, Mark H</creator><creator>McAdams, Harley H</creator><creator>Shapiro, Lucy</creator><general>Oxford, UK : Blackwell Publishing Ltd</general><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201004</creationdate><title>Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function</title><author>Bowman, Grant R ; Comolli, Luis R ; Gaietta, Guido M ; Fero, Michael ; Hong, Sun-Hae ; Jones, Ying ; Lee, Julie H ; Downing, Kenneth H ; Ellisman, Mark H ; McAdams, Harley H ; Shapiro, Lucy</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Bacteria</topic><topic>Bacterial proteins</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>Caulobacter</topic><topic>Caulobacter crescentus</topic><topic>Caulobacter crescentus - metabolism</topic><topic>Caulobacter crescentus - physiology</topic><topic>Cell Cycle</topic><topic>Cell Polarity</topic><topic>Cells</topic><topic>Centromere - metabolism</topic><topic>Chromosomes</topic><topic>Chromosomes, Bacterial - metabolism</topic><topic>DNA Replication</topic><topic>DNA, Bacterial - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Microbiology</topic><topic>Microscopy, Electron, Transmission</topic><topic>Microscopy, Fluorescence</topic><topic>Microscopy, Immunoelectron</topic><topic>Miscellaneous</topic><topic>Models, Biological</topic><topic>Models, Molecular</topic><topic>Morphology</topic><topic>Protein Multimerization</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bowman, Grant R</creatorcontrib><creatorcontrib>Comolli, Luis R</creatorcontrib><creatorcontrib>Gaietta, Guido M</creatorcontrib><creatorcontrib>Fero, Michael</creatorcontrib><creatorcontrib>Hong, Sun-Hae</creatorcontrib><creatorcontrib>Jones, Ying</creatorcontrib><creatorcontrib>Lee, Julie H</creatorcontrib><creatorcontrib>Downing, Kenneth H</creatorcontrib><creatorcontrib>Ellisman, Mark H</creatorcontrib><creatorcontrib>McAdams, Harley H</creatorcontrib><creatorcontrib>Shapiro, Lucy</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bowman, Grant R</au><au>Comolli, Luis R</au><au>Gaietta, Guido M</au><au>Fero, Michael</au><au>Hong, Sun-Hae</au><au>Jones, Ying</au><au>Lee, Julie H</au><au>Downing, Kenneth H</au><au>Ellisman, Mark H</au><au>McAdams, Harley H</au><au>Shapiro, Lucy</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2010-04</date><risdate>2010</risdate><volume>76</volume><issue>1</issue><spage>173</spage><epage>189</epage><pages>173-189</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>The bacterium Caulobacter crescentus has morphologically and functionally distinct cell poles that undergo sequential changes during the cell cycle. We show that the PopZ oligomeric network forms polar ribosome exclusion zones that change function during cell cycle progression. The parS/ParB chromosomal centromere is tethered to PopZ at one pole prior to the initiation of DNA replication. During polar maturation, the PopZ-centromere tether is broken, and the PopZ zone at that pole then switches function to act as a recruitment factor for the ordered addition of multiple proteins that promote the transformation of the flagellated pole into a stalked pole. Stalked pole assembly, in turn, triggers the initiation of chromosome replication, which signals the formation of a new PopZ zone at the opposite cell pole, where it functions to anchor the newly duplicated centromere that has traversed the long axis of the cell. We propose that pole-specific control of PopZ function co-ordinates polar development and cell cycle progression by enabling independent assembly and tethering activities at the two cell poles.</abstract><cop>Oxford, UK</cop><pub>Oxford, UK : Blackwell Publishing Ltd</pub><pmid>20149103</pmid><doi>10.1111/j.1365-2958.2010.07088.x</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Bacterial proteins Bacterial Proteins - metabolism Bacteriology Biological and medical sciences Caulobacter Caulobacter crescentus Caulobacter crescentus - metabolism Caulobacter crescentus - physiology Cell Cycle Cell Polarity Cells Centromere - metabolism Chromosomes Chromosomes, Bacterial - metabolism DNA Replication DNA, Bacterial - metabolism Fundamental and applied biological sciences. Psychology Microbiology Microscopy, Electron, Transmission Microscopy, Fluorescence Microscopy, Immunoelectron Miscellaneous Models, Biological Models, Molecular Morphology Protein Multimerization Ribonucleic acid RNA |
title | Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function |
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