Loading…

A Model of Myosin V Processivity

Cytoplasmic transport is mediated by a group of molecular motors that typically work in isolation, under conditions where they must move their cargos long distances without dissociating from their tracks. This processive behavior requires specific adaptations of motor enzymology to meet these unique...

Full description

Saved in:
Bibliographic Details
Published in:The Journal of biological chemistry 2004-09, Vol.279 (38), p.40100-40111
Main Authors: Rosenfeld, Steven S., Lee Sweeney, H.
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-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643
cites cdi_FETCH-LOGICAL-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643
container_end_page 40111
container_issue 38
container_start_page 40100
container_title The Journal of biological chemistry
container_volume 279
creator Rosenfeld, Steven S.
Lee Sweeney, H.
description Cytoplasmic transport is mediated by a group of molecular motors that typically work in isolation, under conditions where they must move their cargos long distances without dissociating from their tracks. This processive behavior requires specific adaptations of motor enzymology to meet these unique physiologic demands. One of these involves the ability of the two heads of a processive motor to communicate their structural states to each other. In this study, we examine a processive motor from the myosin superfamily myosin V. We have measured the kinetics of nucleotide release, of phosphate release, and of the weak-to-strong transition, as this motor interacts with actin, and we have used these studies to develop a model of how myosin V functions as a transport motor. Surprisingly, both heads release phosphate rapidly upon the initial encounter with an actin filament, suggesting that there is little or no intramolecular strain associated with this step. However, ADP release can be affected by both forward and rearward strain, and under steady-state conditions it is essentially prevented in the lead head until the rear head detaches. Many of these features are remarkably like those underlying the processive movement of kinesin on microtubules, supporting our hypothesis that different molecular motors satisfy the requirement for processive movement in similar ways, regardless of their particular family of origin.
doi_str_mv 10.1074/jbc.M402583200
format article
fullrecord <record><control><sourceid>elsevier_cross</sourceid><recordid>TN_cdi_crossref_primary_10_1074_jbc_M402583200</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0021925820728218</els_id><sourcerecordid>S0021925820728218</sourcerecordid><originalsourceid>FETCH-LOGICAL-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643</originalsourceid><addsrcrecordid>eNp1j01LAzEQhoMotlavHmUPXrdOvnaTYxG_oEUPKt5Ck8zalLZbklrpvze6hZ6cy8DM8w7zEHJJYUihFjdz64YTAUwqzgCOSJ-C4iWX9OOY9AEYLXXe9chZSnPIJTQ9JT0qmRTAZZ8Uo2LSelwUbVNMdm0Kq-K9eImtw5TCNmx25-SkmS4SXuz7gLzd373ePpbj54en29G4dLxWm1I1jHvpK0GVt05ICVajsL6RgHYqKFhbIZNeQyNAY0WVrEFb7ao8sJXgAzLs7rrYphSxMesYltO4MxTMr6rJquagmgNXXWD9ZZfoD_jeLQPXHTALn7PvENHY0LoZLg2rteHKCKB_d1SHYbbbBowmuYArhz5H3Mb4Nvz3wg-YtmuG</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>A Model of Myosin V Processivity</title><source>ScienceDirect Journals</source><creator>Rosenfeld, Steven S. ; Lee Sweeney, H.</creator><creatorcontrib>Rosenfeld, Steven S. ; Lee Sweeney, H.</creatorcontrib><description>Cytoplasmic transport is mediated by a group of molecular motors that typically work in isolation, under conditions where they must move their cargos long distances without dissociating from their tracks. This processive behavior requires specific adaptations of motor enzymology to meet these unique physiologic demands. One of these involves the ability of the two heads of a processive motor to communicate their structural states to each other. In this study, we examine a processive motor from the myosin superfamily myosin V. We have measured the kinetics of nucleotide release, of phosphate release, and of the weak-to-strong transition, as this motor interacts with actin, and we have used these studies to develop a model of how myosin V functions as a transport motor. Surprisingly, both heads release phosphate rapidly upon the initial encounter with an actin filament, suggesting that there is little or no intramolecular strain associated with this step. However, ADP release can be affected by both forward and rearward strain, and under steady-state conditions it is essentially prevented in the lead head until the rear head detaches. Many of these features are remarkably like those underlying the processive movement of kinesin on microtubules, supporting our hypothesis that different molecular motors satisfy the requirement for processive movement in similar ways, regardless of their particular family of origin.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M402583200</identifier><identifier>PMID: 15254035</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Actins - metabolism ; Adenosine Diphosphate - metabolism ; Animals ; Chickens ; Kinetics ; Molecular Motor Proteins - metabolism ; Myosin Type V - metabolism ; Phosphates - metabolism</subject><ispartof>The Journal of biological chemistry, 2004-09, Vol.279 (38), p.40100-40111</ispartof><rights>2004 © 2004 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643</citedby><cites>FETCH-LOGICAL-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0021925820728218$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3549,27924,27925,45780</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15254035$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rosenfeld, Steven S.</creatorcontrib><creatorcontrib>Lee Sweeney, H.</creatorcontrib><title>A Model of Myosin V Processivity</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Cytoplasmic transport is mediated by a group of molecular motors that typically work in isolation, under conditions where they must move their cargos long distances without dissociating from their tracks. This processive behavior requires specific adaptations of motor enzymology to meet these unique physiologic demands. One of these involves the ability of the two heads of a processive motor to communicate their structural states to each other. In this study, we examine a processive motor from the myosin superfamily myosin V. We have measured the kinetics of nucleotide release, of phosphate release, and of the weak-to-strong transition, as this motor interacts with actin, and we have used these studies to develop a model of how myosin V functions as a transport motor. Surprisingly, both heads release phosphate rapidly upon the initial encounter with an actin filament, suggesting that there is little or no intramolecular strain associated with this step. However, ADP release can be affected by both forward and rearward strain, and under steady-state conditions it is essentially prevented in the lead head until the rear head detaches. Many of these features are remarkably like those underlying the processive movement of kinesin on microtubules, supporting our hypothesis that different molecular motors satisfy the requirement for processive movement in similar ways, regardless of their particular family of origin.</description><subject>Actins - metabolism</subject><subject>Adenosine Diphosphate - metabolism</subject><subject>Animals</subject><subject>Chickens</subject><subject>Kinetics</subject><subject>Molecular Motor Proteins - metabolism</subject><subject>Myosin Type V - metabolism</subject><subject>Phosphates - metabolism</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><recordid>eNp1j01LAzEQhoMotlavHmUPXrdOvnaTYxG_oEUPKt5Ck8zalLZbklrpvze6hZ6cy8DM8w7zEHJJYUihFjdz64YTAUwqzgCOSJ-C4iWX9OOY9AEYLXXe9chZSnPIJTQ9JT0qmRTAZZ8Uo2LSelwUbVNMdm0Kq-K9eImtw5TCNmx25-SkmS4SXuz7gLzd373ePpbj54en29G4dLxWm1I1jHvpK0GVt05ICVajsL6RgHYqKFhbIZNeQyNAY0WVrEFb7ao8sJXgAzLs7rrYphSxMesYltO4MxTMr6rJquagmgNXXWD9ZZfoD_jeLQPXHTALn7PvENHY0LoZLg2rteHKCKB_d1SHYbbbBowmuYArhz5H3Mb4Nvz3wg-YtmuG</recordid><startdate>20040917</startdate><enddate>20040917</enddate><creator>Rosenfeld, Steven S.</creator><creator>Lee Sweeney, H.</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</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></search><sort><creationdate>20040917</creationdate><title>A Model of Myosin V Processivity</title><author>Rosenfeld, Steven S. ; Lee Sweeney, H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Actins - metabolism</topic><topic>Adenosine Diphosphate - metabolism</topic><topic>Animals</topic><topic>Chickens</topic><topic>Kinetics</topic><topic>Molecular Motor Proteins - metabolism</topic><topic>Myosin Type V - metabolism</topic><topic>Phosphates - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rosenfeld, Steven S.</creatorcontrib><creatorcontrib>Lee Sweeney, H.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rosenfeld, Steven S.</au><au>Lee Sweeney, H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Model of Myosin V Processivity</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2004-09-17</date><risdate>2004</risdate><volume>279</volume><issue>38</issue><spage>40100</spage><epage>40111</epage><pages>40100-40111</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Cytoplasmic transport is mediated by a group of molecular motors that typically work in isolation, under conditions where they must move their cargos long distances without dissociating from their tracks. This processive behavior requires specific adaptations of motor enzymology to meet these unique physiologic demands. One of these involves the ability of the two heads of a processive motor to communicate their structural states to each other. In this study, we examine a processive motor from the myosin superfamily myosin V. We have measured the kinetics of nucleotide release, of phosphate release, and of the weak-to-strong transition, as this motor interacts with actin, and we have used these studies to develop a model of how myosin V functions as a transport motor. Surprisingly, both heads release phosphate rapidly upon the initial encounter with an actin filament, suggesting that there is little or no intramolecular strain associated with this step. However, ADP release can be affected by both forward and rearward strain, and under steady-state conditions it is essentially prevented in the lead head until the rear head detaches. Many of these features are remarkably like those underlying the processive movement of kinesin on microtubules, supporting our hypothesis that different molecular motors satisfy the requirement for processive movement in similar ways, regardless of their particular family of origin.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>15254035</pmid><doi>10.1074/jbc.M402583200</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0021-9258
ispartof The Journal of biological chemistry, 2004-09, Vol.279 (38), p.40100-40111
issn 0021-9258
1083-351X
language eng
recordid cdi_crossref_primary_10_1074_jbc_M402583200
source ScienceDirect Journals
subjects Actins - metabolism
Adenosine Diphosphate - metabolism
Animals
Chickens
Kinetics
Molecular Motor Proteins - metabolism
Myosin Type V - metabolism
Phosphates - metabolism
title A Model of Myosin V Processivity
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T13%3A32%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-elsevier_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20Model%20of%20Myosin%20V%20Processivity&rft.jtitle=The%20Journal%20of%20biological%20chemistry&rft.au=Rosenfeld,%20Steven%20S.&rft.date=2004-09-17&rft.volume=279&rft.issue=38&rft.spage=40100&rft.epage=40111&rft.pages=40100-40111&rft.issn=0021-9258&rft.eissn=1083-351X&rft_id=info:doi/10.1074/jbc.M402583200&rft_dat=%3Celsevier_cross%3ES0021925820728218%3C/elsevier_cross%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c378t-8f23d5d6418dbc4550b9e4bdf50eba410bb6e25d90f409e6185709b9c60f4b643%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_id=info:pmid/15254035&rfr_iscdi=true