The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif
Summary Escherichia coli DnaA, an AAA+ superfamily protein, initiates chromosomal replication in an ATP‐binding‐dependent manner. Although DnaA has conserved Walker A/B motifs, it binds adenine nucleotides 10‐ to 100‐fold more tightly than do many other AAA+ proteins. This study shows that the DnaA...
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Veröffentlicht in: | Molecular microbiology 2006-12, Vol.62 (5), p.1310-1324 |
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creator | Kawakami, Hironori Ozaki, Shogo Suzuki, Shigeo Nakamura, Kenta Senriuchi, Takayuki Su'etsugu, Masayuki Fujimitsu, Kazuyuki Katayama, Tsutomu |
description | Summary
Escherichia coli DnaA, an AAA+ superfamily protein, initiates chromosomal replication in an ATP‐binding‐dependent manner. Although DnaA has conserved Walker A/B motifs, it binds adenine nucleotides 10‐ to 100‐fold more tightly than do many other AAA+ proteins. This study shows that the DnaA Asp‐269 residue, located in the sensor 1 motif, plays a specific role in supporting high‐affinity ATP/ADP binding. The affinity of the DnaA D269A mutant for ATP/ADP is at least 10‐ to 100‐fold reduced compared with that of the wild‐type and DnaA R270A proteins. In contrast, the abilities of DnaA D269A to bind a typical DnaA box, unwind oriC duplex in the presence of elevated concentrations of ATP, load DnaB onto DNA and support minichromosomal replication in a reconstituted system are retained. Whereas the acidic Asp residue is highly conserved among eubacterial DnaA homologues, the corresponding residue in many other AAA+ proteins is Asn/Thr and in some AAA+ proteins these neutral residues are essential for ATP hydrolysis but not ATP binding. As the intrinsic ATPase activity of DnaA is extremely weak, this study reveals a novel and specific function for the sensor 1 motif in tight ATP/ADP binding, one that depends on the alternate key residue Asp. |
doi_str_mv | 10.1111/j.1365-2958.2006.05450.x |
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Escherichia coli DnaA, an AAA+ superfamily protein, initiates chromosomal replication in an ATP‐binding‐dependent manner. Although DnaA has conserved Walker A/B motifs, it binds adenine nucleotides 10‐ to 100‐fold more tightly than do many other AAA+ proteins. This study shows that the DnaA Asp‐269 residue, located in the sensor 1 motif, plays a specific role in supporting high‐affinity ATP/ADP binding. The affinity of the DnaA D269A mutant for ATP/ADP is at least 10‐ to 100‐fold reduced compared with that of the wild‐type and DnaA R270A proteins. In contrast, the abilities of DnaA D269A to bind a typical DnaA box, unwind oriC duplex in the presence of elevated concentrations of ATP, load DnaB onto DNA and support minichromosomal replication in a reconstituted system are retained. Whereas the acidic Asp residue is highly conserved among eubacterial DnaA homologues, the corresponding residue in many other AAA+ proteins is Asn/Thr and in some AAA+ proteins these neutral residues are essential for ATP hydrolysis but not ATP binding. As the intrinsic ATPase activity of DnaA is extremely weak, this study reveals a novel and specific function for the sensor 1 motif in tight ATP/ADP binding, one that depends on the alternate key residue Asp.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2006.05450.x</identifier><identifier>PMID: 17042785</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Adenosine Diphosphate - metabolism ; Adenosine triphosphatase ; Adenosine Triphosphate - metabolism ; Amino Acid Motifs ; Aspartic Acid - chemistry ; Bacterial Proteins - chemistry ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Binding Sites ; Biological and medical sciences ; Deoxyribonucleic acid ; DNA ; DNA-Binding Proteins - chemistry ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; E coli ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli - growth & development ; Escherichia coli - metabolism ; Fundamental and applied biological sciences. Psychology ; Microbiology ; Protein folding ; Studies</subject><ispartof>Molecular microbiology, 2006-12, Vol.62 (5), p.1310-1324</ispartof><rights>2007 INIST-CNRS</rights><rights>Copyright Blackwell Publishing Dec 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5710-7e69aa74b6c6e15b21a435abd0a52479fe5a1c0dfaede8970dbb30b3cb5f0a1e3</citedby><cites>FETCH-LOGICAL-c5710-7e69aa74b6c6e15b21a435abd0a52479fe5a1c0dfaede8970dbb30b3cb5f0a1e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-2958.2006.05450.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-2958.2006.05450.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,1434,27926,27927,45576,45577,46411,46835</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18287256$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17042785$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kawakami, Hironori</creatorcontrib><creatorcontrib>Ozaki, Shogo</creatorcontrib><creatorcontrib>Suzuki, Shigeo</creatorcontrib><creatorcontrib>Nakamura, Kenta</creatorcontrib><creatorcontrib>Senriuchi, Takayuki</creatorcontrib><creatorcontrib>Su'etsugu, Masayuki</creatorcontrib><creatorcontrib>Fujimitsu, Kazuyuki</creatorcontrib><creatorcontrib>Katayama, Tsutomu</creatorcontrib><title>The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Escherichia coli DnaA, an AAA+ superfamily protein, initiates chromosomal replication in an ATP‐binding‐dependent manner. Although DnaA has conserved Walker A/B motifs, it binds adenine nucleotides 10‐ to 100‐fold more tightly than do many other AAA+ proteins. This study shows that the DnaA Asp‐269 residue, located in the sensor 1 motif, plays a specific role in supporting high‐affinity ATP/ADP binding. The affinity of the DnaA D269A mutant for ATP/ADP is at least 10‐ to 100‐fold reduced compared with that of the wild‐type and DnaA R270A proteins. In contrast, the abilities of DnaA D269A to bind a typical DnaA box, unwind oriC duplex in the presence of elevated concentrations of ATP, load DnaB onto DNA and support minichromosomal replication in a reconstituted system are retained. Whereas the acidic Asp residue is highly conserved among eubacterial DnaA homologues, the corresponding residue in many other AAA+ proteins is Asn/Thr and in some AAA+ proteins these neutral residues are essential for ATP hydrolysis but not ATP binding. As the intrinsic ATPase activity of DnaA is extremely weak, this study reveals a novel and specific function for the sensor 1 motif in tight ATP/ADP binding, one that depends on the alternate key residue Asp.</description><subject>Adenosine Diphosphate - metabolism</subject><subject>Adenosine triphosphatase</subject><subject>Adenosine Triphosphate - metabolism</subject><subject>Amino Acid Motifs</subject><subject>Aspartic Acid - chemistry</subject><subject>Bacterial Proteins - chemistry</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Binding Sites</subject><subject>Biological and medical sciences</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA-Binding Proteins - chemistry</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - growth & development</subject><subject>Escherichia coli - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Microbiology</subject><subject>Protein folding</subject><subject>Studies</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU1r3DAQhkVpaTZp_0IRheYSvBlJlmwfejBJPwIJzWELvYmxLDVavPZGssnuv6_cXRropdVFYuaZl0EPIZTBkqVzuV4yoWTGK1kuOYBagswlLHcvyOJP4yVZQCUhEyX_cUJOY1wDMAFKvCYnrICcF6VckKfVg6V2Z-x29EOPXbeno__5MFJ0zvd-3NPB0esea-qGQOvV_WV9fU-DfZx8sJEinXr_OFmKcYth9Iai8W3qR9-mqu_pmPLrur6g0fYxRTC6GUbv3pBXDrto3x7vM_L986fV1dfs9tuXm6v6NjOyYJAVVlWIRd4ooyyTDWeYC4lNCyh5XlTOSmQGWoe2tWVVQNs0AhphGukAmRVn5PyQuw1D2jOOeuOjsV2HvR2mqFXJiirn1T9BVkkFvOIJfP8XuB6mkL5uZpQUICQkqDxAJgwxBuv0NvgNhr1moGeFeq1nU3o2pWeF-rdCvUuj7475U7Ox7fPg0VkCPhwBjAY7F7A3Pj5zJS8LLlXiPh64J9_Z_X8voO_ubuaX-AX-G7Zc</recordid><startdate>200612</startdate><enddate>200612</enddate><creator>Kawakami, Hironori</creator><creator>Ozaki, Shogo</creator><creator>Suzuki, Shigeo</creator><creator>Nakamura, Kenta</creator><creator>Senriuchi, Takayuki</creator><creator>Su'etsugu, Masayuki</creator><creator>Fujimitsu, Kazuyuki</creator><creator>Katayama, Tsutomu</creator><general>Blackwell Publishing Ltd</general><general>Blackwell Science</general><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></search><sort><creationdate>200612</creationdate><title>The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif</title><author>Kawakami, Hironori ; Ozaki, Shogo ; Suzuki, Shigeo ; Nakamura, Kenta ; Senriuchi, Takayuki ; Su'etsugu, Masayuki ; Fujimitsu, Kazuyuki ; Katayama, Tsutomu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5710-7e69aa74b6c6e15b21a435abd0a52479fe5a1c0dfaede8970dbb30b3cb5f0a1e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Adenosine Diphosphate - metabolism</topic><topic>Adenosine triphosphatase</topic><topic>Adenosine Triphosphate - metabolism</topic><topic>Amino Acid Motifs</topic><topic>Aspartic Acid - chemistry</topic><topic>Bacterial Proteins - chemistry</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Binding Sites</topic><topic>Biological and medical sciences</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA-Binding Proteins - chemistry</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>E coli</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - growth & development</topic><topic>Escherichia coli - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Microbiology</topic><topic>Protein folding</topic><topic>Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kawakami, Hironori</creatorcontrib><creatorcontrib>Ozaki, Shogo</creatorcontrib><creatorcontrib>Suzuki, Shigeo</creatorcontrib><creatorcontrib>Nakamura, Kenta</creatorcontrib><creatorcontrib>Senriuchi, Takayuki</creatorcontrib><creatorcontrib>Su'etsugu, Masayuki</creatorcontrib><creatorcontrib>Fujimitsu, Kazuyuki</creatorcontrib><creatorcontrib>Katayama, Tsutomu</creatorcontrib><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><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kawakami, Hironori</au><au>Ozaki, Shogo</au><au>Suzuki, Shigeo</au><au>Nakamura, Kenta</au><au>Senriuchi, Takayuki</au><au>Su'etsugu, Masayuki</au><au>Fujimitsu, Kazuyuki</au><au>Katayama, Tsutomu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2006-12</date><risdate>2006</risdate><volume>62</volume><issue>5</issue><spage>1310</spage><epage>1324</epage><pages>1310-1324</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Escherichia coli DnaA, an AAA+ superfamily protein, initiates chromosomal replication in an ATP‐binding‐dependent manner. Although DnaA has conserved Walker A/B motifs, it binds adenine nucleotides 10‐ to 100‐fold more tightly than do many other AAA+ proteins. This study shows that the DnaA Asp‐269 residue, located in the sensor 1 motif, plays a specific role in supporting high‐affinity ATP/ADP binding. The affinity of the DnaA D269A mutant for ATP/ADP is at least 10‐ to 100‐fold reduced compared with that of the wild‐type and DnaA R270A proteins. In contrast, the abilities of DnaA D269A to bind a typical DnaA box, unwind oriC duplex in the presence of elevated concentrations of ATP, load DnaB onto DNA and support minichromosomal replication in a reconstituted system are retained. Whereas the acidic Asp residue is highly conserved among eubacterial DnaA homologues, the corresponding residue in many other AAA+ proteins is Asn/Thr and in some AAA+ proteins these neutral residues are essential for ATP hydrolysis but not ATP binding. As the intrinsic ATPase activity of DnaA is extremely weak, this study reveals a novel and specific function for the sensor 1 motif in tight ATP/ADP binding, one that depends on the alternate key residue Asp.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>17042785</pmid><doi>10.1111/j.1365-2958.2006.05450.x</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adenosine Diphosphate - metabolism Adenosine triphosphatase Adenosine Triphosphate - metabolism Amino Acid Motifs Aspartic Acid - chemistry Bacterial Proteins - chemistry Bacterial Proteins - genetics Bacterial Proteins - metabolism Binding Sites Biological and medical sciences Deoxyribonucleic acid DNA DNA-Binding Proteins - chemistry DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism E coli Escherichia coli Escherichia coli - genetics Escherichia coli - growth & development Escherichia coli - metabolism Fundamental and applied biological sciences. Psychology Microbiology Protein folding Studies |
title | The exceptionally tight affinity of DnaA for ATP/ADP requires a unique aspartic acid residue in the AAA+ sensor 1 motif |
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