Loading…

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...

Full description

Saved in:
Bibliographic Details
Published in:Molecular microbiology 2010-04, Vol.76 (1), p.173-189
Main Authors: 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
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913
cites cdi_FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913
container_end_page 189
container_issue 1
container_start_page 173
container_title Molecular microbiology
container_volume 76
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
format article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2935252</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>744673625</sourcerecordid><originalsourceid>FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913</originalsourceid><addsrcrecordid>eNqNkktv1DAUhSMEokPhL4CFhFhl8CN27AVIaFSgUiuQoBJiY91xnKlHiZ3aCW3_PU5nGB4biBeJc79zc26OiwIRvCT5erVdEiZ4SRWXS4rzW1xjKZc394rFoXC_WGDFcckk_XpUPEppizFhWLCHxVHWVIpgtijaFUxdWIMZbUSfwvANtSH2CQEaQgcRpWndhB6cR40zI4zOb1CyV5P1o4MOmUvwG5tQrmfeIhP6ISQ3uuAR-Aa1kzfz5nHxoIUu2Sf7-3Fx8e7ky-pDefbx_enq7VlpuBSyNJLIiiiJTd0Y3ghMiDJWykrUBioQeZaKyqY2lnECuCam4mBrsBWnAhRhx8WbXd9hWve2MdlmhE4P0fUQb3UAp_-seHepN-G7popxymlu8HLfIIY8ZRp175KxXQfehinpuspemKD83yRjnFdKsUw-_4vchin6_B80UYLnkaXIkNxBJoaUom0PpgnWc-h6q-ds9ZytnkPXd6Hrmyx9-vvQB-HPlDPwYg9AMtC1Ebxx6RdH73zizL3ecdeus7f_bUCfn5_OT1n_bKdvIWjYxPyNi890PnVEEpUX-wEstdHD</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>196518486</pqid></control><display><type>article</type><title>Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function</title><source>Wiley-Blackwell Read &amp; Publish Collection</source><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</creator><creatorcontrib>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</creatorcontrib><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><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&amp;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 &amp; 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>
fulltext fulltext
identifier ISSN: 0950-382X
ispartof Molecular microbiology, 2010-04, Vol.76 (1), p.173-189
issn 0950-382X
1365-2958
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2935252
source Wiley-Blackwell Read & Publish Collection
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
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T12%3A54%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Caulobacter%20PopZ%20forms%20a%20polar%20subdomain%20dictating%20sequential%20changes%20in%20pole%20composition%20and%20function&rft.jtitle=Molecular%20microbiology&rft.au=Bowman,%20Grant%20R&rft.date=2010-04&rft.volume=76&rft.issue=1&rft.spage=173&rft.epage=189&rft.pages=173-189&rft.issn=0950-382X&rft.eissn=1365-2958&rft_id=info:doi/10.1111/j.1365-2958.2010.07088.x&rft_dat=%3Cproquest_pubme%3E744673625%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c5868-c81841980c7dc5d60119ce88467ca4a6382428d7ce351a071c45ae7ae4526a913%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=196518486&rft_id=info:pmid/20149103&rfr_iscdi=true