Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise

A fundamental problem in cell biology is to understand how spatial information is recognized and integrated into morphogenetic responses. Budding yeast undergoes differentiation to filamentous growth, which involves changes in cell polarity through mechanisms that remain obscure. Here we define a re...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2016-04, Vol.113 (14), p.E2019-E2028
Hauptverfasser: Basu, Sukanya, Vadaie, Nadia, Prabhakar, Aditi, Li, Boyang, Adhikari, Hema, Pitoniak, Andrew, Chow, Jacky, Chavel, Colin A., Cullen, Paul J.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page E2028
container_issue 14
container_start_page E2019
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 113
creator Basu, Sukanya
Vadaie, Nadia
Prabhakar, Aditi
Li, Boyang
Adhikari, Hema
Pitoniak, Andrew
Chow, Jacky
Chavel, Colin A.
Cullen, Paul J.
description A fundamental problem in cell biology is to understand how spatial information is recognized and integrated into morphogenetic responses. Budding yeast undergoes differentiation to filamentous growth, which involves changes in cell polarity through mechanisms that remain obscure. Here we define a regulatory input where spatial landmarks (bud-site–selection proteins) regulate the MAPK pathway that controls filamentous growth (fMAPK pathway). The bud-site GTPase Rsr1p regulated the fMAPK pathway through Cdc24p, the guanine nucleotide exchange factor for the polarity establishment GTPase Cdc42p. Positional landmarks that direct Rsr1p to bud sites conditionally regulated the fMAPK pathway, corresponding to their roles in regulating bud-site selection. Therefore, cell differentiation is achieved in part by the reorganization of polarity at bud sites. In line with this conclusion, dynamic changes in budding pattern during filamentous growth induced corresponding changes in fMAPK activity. Intrinsic compromise of bud-site selection also impacted fMAPK activity. Therefore, a surveillance mechanism monitors spatial position in response to extrinsic and intrinsic stress and modulates the response through a differentiation MAPK pathway.
doi_str_mv 10.1073/pnas.1522679113
format Article
fullrecord <record><control><sourceid>jstor_cross</sourceid><recordid>TN_cdi_crossref_primary_10_1073_pnas_1522679113</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26469210</jstor_id><sourcerecordid>26469210</sourcerecordid><originalsourceid>FETCH-LOGICAL-c468t-988546b49b52b4a2ce93c80744fc478a637c64560ef352899a3ec1a7d764dd93</originalsourceid><addsrcrecordid>eNpdkU1v1DAQhi0EokvhzAlkqRcuaccf8ccFqVoVqCgCid4tr-N0s2TjYDugXvjtOOx2WyoffPAzj9-ZQeg1gVMCkp2Ng02npKZUSE0Ie4IWBDSpBNfwFC0AqKwUp_wIvUhpAwC6VvAcHVEJQBSDBfrzfbS5sz3u7dBsbfyRcPQ3U2-zxxYvG8dp1fjRD40fMv5y_u0zLgXr3_YW54BdGHIMPW66tvWxEF2RhQEXF85rX1RpDEPyMzuG1M2P5S8XtmMM2y75l-hZa_vkX-3vY3T94eJ6-am6-vrxcnl-VTkuVK60UjUXK65XNV1xS53XzCmQnLeOS2UFk07wWoBvWU2V1pZ5R6xspOBNo9kxer_TjtNq6xtXkkbbmzF2peVbE2xn_n8ZurW5Cb8MV4xRNgve7QUx_Jx8yqakd74vU_NhSobIMtky9X_oySN0E6ZY2p4pRctRUBfqbEe5GFKKvj2EIWDm1Zp5teZ-taXi7cMeDvzdLguA98BcedARZgg3FxTInO3NDtmkHOK9QnChKQH2F9e0tZE</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1782828805</pqid></control><display><type>article</type><title>Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise</title><source>MEDLINE</source><source>JSTOR Archive Collection A-Z Listing</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Basu, Sukanya ; Vadaie, Nadia ; Prabhakar, Aditi ; Li, Boyang ; Adhikari, Hema ; Pitoniak, Andrew ; Chow, Jacky ; Chavel, Colin A. ; Cullen, Paul J.</creator><creatorcontrib>Basu, Sukanya ; Vadaie, Nadia ; Prabhakar, Aditi ; Li, Boyang ; Adhikari, Hema ; Pitoniak, Andrew ; Chow, Jacky ; Chavel, Colin A. ; Cullen, Paul J.</creatorcontrib><description>A fundamental problem in cell biology is to understand how spatial information is recognized and integrated into morphogenetic responses. Budding yeast undergoes differentiation to filamentous growth, which involves changes in cell polarity through mechanisms that remain obscure. Here we define a regulatory input where spatial landmarks (bud-site–selection proteins) regulate the MAPK pathway that controls filamentous growth (fMAPK pathway). The bud-site GTPase Rsr1p regulated the fMAPK pathway through Cdc24p, the guanine nucleotide exchange factor for the polarity establishment GTPase Cdc42p. Positional landmarks that direct Rsr1p to bud sites conditionally regulated the fMAPK pathway, corresponding to their roles in regulating bud-site selection. Therefore, cell differentiation is achieved in part by the reorganization of polarity at bud sites. In line with this conclusion, dynamic changes in budding pattern during filamentous growth induced corresponding changes in fMAPK activity. Intrinsic compromise of bud-site selection also impacted fMAPK activity. Therefore, a surveillance mechanism monitors spatial position in response to extrinsic and intrinsic stress and modulates the response through a differentiation MAPK pathway.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1522679113</identifier><identifier>PMID: 27001830</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Biological Sciences ; cdc42 GTP-Binding Protein, Saccharomyces cerevisiae - metabolism ; Cellular biology ; MAP Kinase Signaling System ; PNAS Plus ; Proteins ; Saccharomyces cerevisiae - metabolism ; Yeast</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2016-04, Vol.113 (14), p.E2019-E2028</ispartof><rights>Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Apr 5, 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c468t-988546b49b52b4a2ce93c80744fc478a637c64560ef352899a3ec1a7d764dd93</citedby><cites>FETCH-LOGICAL-c468t-988546b49b52b4a2ce93c80744fc478a637c64560ef352899a3ec1a7d764dd93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/113/14.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26469210$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26469210$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,729,782,786,805,887,27931,27932,53798,53800,58024,58257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27001830$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Basu, Sukanya</creatorcontrib><creatorcontrib>Vadaie, Nadia</creatorcontrib><creatorcontrib>Prabhakar, Aditi</creatorcontrib><creatorcontrib>Li, Boyang</creatorcontrib><creatorcontrib>Adhikari, Hema</creatorcontrib><creatorcontrib>Pitoniak, Andrew</creatorcontrib><creatorcontrib>Chow, Jacky</creatorcontrib><creatorcontrib>Chavel, Colin A.</creatorcontrib><creatorcontrib>Cullen, Paul J.</creatorcontrib><title>Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>A fundamental problem in cell biology is to understand how spatial information is recognized and integrated into morphogenetic responses. Budding yeast undergoes differentiation to filamentous growth, which involves changes in cell polarity through mechanisms that remain obscure. Here we define a regulatory input where spatial landmarks (bud-site–selection proteins) regulate the MAPK pathway that controls filamentous growth (fMAPK pathway). The bud-site GTPase Rsr1p regulated the fMAPK pathway through Cdc24p, the guanine nucleotide exchange factor for the polarity establishment GTPase Cdc42p. Positional landmarks that direct Rsr1p to bud sites conditionally regulated the fMAPK pathway, corresponding to their roles in regulating bud-site selection. Therefore, cell differentiation is achieved in part by the reorganization of polarity at bud sites. In line with this conclusion, dynamic changes in budding pattern during filamentous growth induced corresponding changes in fMAPK activity. Intrinsic compromise of bud-site selection also impacted fMAPK activity. Therefore, a surveillance mechanism monitors spatial position in response to extrinsic and intrinsic stress and modulates the response through a differentiation MAPK pathway.</description><subject>Biological Sciences</subject><subject>cdc42 GTP-Binding Protein, Saccharomyces cerevisiae - metabolism</subject><subject>Cellular biology</subject><subject>MAP Kinase Signaling System</subject><subject>PNAS Plus</subject><subject>Proteins</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Yeast</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1v1DAQhi0EokvhzAlkqRcuaccf8ccFqVoVqCgCid4tr-N0s2TjYDugXvjtOOx2WyoffPAzj9-ZQeg1gVMCkp2Ng02npKZUSE0Ie4IWBDSpBNfwFC0AqKwUp_wIvUhpAwC6VvAcHVEJQBSDBfrzfbS5sz3u7dBsbfyRcPQ3U2-zxxYvG8dp1fjRD40fMv5y_u0zLgXr3_YW54BdGHIMPW66tvWxEF2RhQEXF85rX1RpDEPyMzuG1M2P5S8XtmMM2y75l-hZa_vkX-3vY3T94eJ6-am6-vrxcnl-VTkuVK60UjUXK65XNV1xS53XzCmQnLeOS2UFk07wWoBvWU2V1pZ5R6xspOBNo9kxer_TjtNq6xtXkkbbmzF2peVbE2xn_n8ZurW5Cb8MV4xRNgve7QUx_Jx8yqakd74vU_NhSobIMtky9X_oySN0E6ZY2p4pRctRUBfqbEe5GFKKvj2EIWDm1Zp5teZ-taXi7cMeDvzdLguA98BcedARZgg3FxTInO3NDtmkHOK9QnChKQH2F9e0tZE</recordid><startdate>20160405</startdate><enddate>20160405</enddate><creator>Basu, Sukanya</creator><creator>Vadaie, Nadia</creator><creator>Prabhakar, Aditi</creator><creator>Li, Boyang</creator><creator>Adhikari, Hema</creator><creator>Pitoniak, Andrew</creator><creator>Chow, Jacky</creator><creator>Chavel, Colin A.</creator><creator>Cullen, Paul J.</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</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>20160405</creationdate><title>Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise</title><author>Basu, Sukanya ; Vadaie, Nadia ; Prabhakar, Aditi ; Li, Boyang ; Adhikari, Hema ; Pitoniak, Andrew ; Chow, Jacky ; Chavel, Colin A. ; Cullen, Paul J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c468t-988546b49b52b4a2ce93c80744fc478a637c64560ef352899a3ec1a7d764dd93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Biological Sciences</topic><topic>cdc42 GTP-Binding Protein, Saccharomyces cerevisiae - metabolism</topic><topic>Cellular biology</topic><topic>MAP Kinase Signaling System</topic><topic>PNAS Plus</topic><topic>Proteins</topic><topic>Saccharomyces cerevisiae - metabolism</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Basu, Sukanya</creatorcontrib><creatorcontrib>Vadaie, Nadia</creatorcontrib><creatorcontrib>Prabhakar, Aditi</creatorcontrib><creatorcontrib>Li, Boyang</creatorcontrib><creatorcontrib>Adhikari, Hema</creatorcontrib><creatorcontrib>Pitoniak, Andrew</creatorcontrib><creatorcontrib>Chow, Jacky</creatorcontrib><creatorcontrib>Chavel, Colin A.</creatorcontrib><creatorcontrib>Cullen, Paul J.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors 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>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Basu, Sukanya</au><au>Vadaie, Nadia</au><au>Prabhakar, Aditi</au><au>Li, Boyang</au><au>Adhikari, Hema</au><au>Pitoniak, Andrew</au><au>Chow, Jacky</au><au>Chavel, Colin A.</au><au>Cullen, Paul J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2016-04-05</date><risdate>2016</risdate><volume>113</volume><issue>14</issue><spage>E2019</spage><epage>E2028</epage><pages>E2019-E2028</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>A fundamental problem in cell biology is to understand how spatial information is recognized and integrated into morphogenetic responses. Budding yeast undergoes differentiation to filamentous growth, which involves changes in cell polarity through mechanisms that remain obscure. Here we define a regulatory input where spatial landmarks (bud-site–selection proteins) regulate the MAPK pathway that controls filamentous growth (fMAPK pathway). The bud-site GTPase Rsr1p regulated the fMAPK pathway through Cdc24p, the guanine nucleotide exchange factor for the polarity establishment GTPase Cdc42p. Positional landmarks that direct Rsr1p to bud sites conditionally regulated the fMAPK pathway, corresponding to their roles in regulating bud-site selection. Therefore, cell differentiation is achieved in part by the reorganization of polarity at bud sites. In line with this conclusion, dynamic changes in budding pattern during filamentous growth induced corresponding changes in fMAPK activity. Intrinsic compromise of bud-site selection also impacted fMAPK activity. Therefore, a surveillance mechanism monitors spatial position in response to extrinsic and intrinsic stress and modulates the response through a differentiation MAPK pathway.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>27001830</pmid><doi>10.1073/pnas.1522679113</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0027-8424
ispartof Proceedings of the National Academy of Sciences - PNAS, 2016-04, Vol.113 (14), p.E2019-E2028
issn 0027-8424
1091-6490
language eng
recordid cdi_crossref_primary_10_1073_pnas_1522679113
source MEDLINE; JSTOR Archive Collection A-Z Listing; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
subjects Biological Sciences
cdc42 GTP-Binding Protein, Saccharomyces cerevisiae - metabolism
Cellular biology
MAP Kinase Signaling System
PNAS Plus
Proteins
Saccharomyces cerevisiae - metabolism
Yeast
title Spatial landmarks regulate a Cdc42-dependent MAPK pathway to control differentiation and the response to positional compromise
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-05T09%3A41%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Spatial%20landmarks%20regulate%20a%20Cdc42-dependent%20MAPK%20pathway%20to%20control%20differentiation%20and%20the%20response%20to%20positional%20compromise&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Basu,%20Sukanya&rft.date=2016-04-05&rft.volume=113&rft.issue=14&rft.spage=E2019&rft.epage=E2028&rft.pages=E2019-E2028&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1522679113&rft_dat=%3Cjstor_cross%3E26469210%3C/jstor_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1782828805&rft_id=info:pmid/27001830&rft_jstor_id=26469210&rfr_iscdi=true