MersV1, Main, Exploration, bibRecord, 001786

Functional Class I and II Amino Acid-activating Enzymes Can Be Coded by Opposite Strands of the Same Gene.

Identifieur interne : 001786 ( Main/Exploration ); précédent : 001785; suivant : 001787

Functional Class I and II Amino Acid-activating Enzymes Can Be Coded by Opposite Strands of the Same Gene.

Auteurs : Luis Martinez-Rodriguez [États-Unis] ; Ozgün Erdogan [États-Unis] ; Mariel Jimenez-Rodriguez [États-Unis] ; Katiria Gonzalez-Rivera [États-Unis] ; Tishan Williams [États-Unis] ; Li Li [États-Unis] ; Violetta Weinreb [États-Unis] ; Martha Collier [États-Unis] ; Srinivas Niranj Chandrasekaran [États-Unis] ; Xavier Ambroggio [États-Unis] ; Brian Kuhlman [États-Unis] ; Charles W. Carter [États-Unis]

Source :

The Journal of biological chemistry [ 1083-351X ] ; 2015.

RBID : pubmed:26088142

Descripteurs français

English descriptors

KwdEn :
- Adenosine Triphosphate (chemistry), Adenosine Triphosphate (metabolism), Amino Acid Sequence, Amino Acyl-tRNA Synthetases (chemistry), Amino Acyl-tRNA Synthetases (genetics), Amino Acyl-tRNA Synthetases (metabolism), Aminoacylation, Biocatalysis, Catalytic Domain, Codon (chemistry), Codon (metabolism), Escherichia coli (genetics), Escherichia coli (metabolism), Evolution, Molecular, Gene Expression, Genetic Code, Kinetics, Molecular Sequence Data, Mutation, Peptides (chemistry), Peptides (genetics), Peptides (metabolism), Protein Binding, Recombinant Proteins (chemistry), Recombinant Proteins (genetics), Recombinant Proteins (metabolism).
MESH :
- chemical , chemistry : Adenosine Triphosphate, Amino Acyl-tRNA Synthetases, Codon, Peptides, Recombinant Proteins.
- chemical , genetics : Amino Acyl-tRNA Synthetases, Peptides, Recombinant Proteins.
- chemical , metabolism : Adenosine Triphosphate, Amino Acyl-tRNA Synthetases, Codon, Peptides, Recombinant Proteins.
- genetics : Escherichia coli.
- metabolism : Escherichia coli.
- Amino Acid Sequence, Aminoacylation, Biocatalysis, Catalytic Domain, Evolution, Molecular, Gene Expression, Genetic Code, Kinetics, Molecular Sequence Data, Mutation, Protein Binding.

Abstract

Aminoacyl-tRNA synthetases (aaRS) catalyze both chemical steps that translate the universal genetic code. Rodin and Ohno offered an explanation for the existence of two aaRS classes, observing that codons for the most highly conserved Class I active-site residues are anticodons for corresponding Class II active-site residues. They proposed that the two classes arose simultaneously, by translation of opposite strands from the same gene. We have characterized wild-type 46-residue peptides containing ATP-binding sites of Class I and II synthetases and those coded by a gene designed by Rosetta to encode the corresponding peptides on opposite strands. Catalysis by WT and designed peptides is saturable, and the designed peptides are sensitive to active-site residue mutation. All have comparable apparent second-order rate constants 2.9-7.0E-3 M(-1) s(-1) or ∼750,000-1,300,000 times the uncatalyzed rate. The activities of the two complementary peptides demonstrate that the unique information in a gene can have two functional interpretations, one from each complementary strand. The peptides contain phylogenetic signatures of longer, more sophisticated catalysts we call Urzymes and are short enough to bridge the gap between them and simpler uncoded peptides. Thus, they directly substantiate the sense/antisense coding ancestry of Class I and II aaRS. Furthermore, designed 46-mers achieve similar catalytic proficiency to wild-type 46-mers by significant increases in both kcat and Km values, supporting suggestions that the earliest peptide catalysts activated ATP for biosynthetic purposes.

DOI: 10.1074/jbc.M115.642876
PubMed: 26088142

Affiliations:

Le document en format XML

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<author><name sortKey="Gonzalez Rivera, Katiria" sort="Gonzalez Rivera, Katiria" uniqKey="Gonzalez Rivera K" first="Katiria" last="Gonzalez-Rivera">Katiria Gonzalez-Rivera</name>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
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<author><name sortKey="Weinreb, Violetta" sort="Weinreb, Violetta" uniqKey="Weinreb V" first="Violetta" last="Weinreb">Violetta Weinreb</name>
<affiliation wicri:level="2"><nlm:affiliation>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7260.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
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<author><name sortKey="Collier, Martha" sort="Collier, Martha" uniqKey="Collier M" first="Martha" last="Collier">Martha Collier</name>
<affiliation wicri:level="2"><nlm:affiliation>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7260.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Chandrasekaran, Srinivas Niranj" sort="Chandrasekaran, Srinivas Niranj" uniqKey="Chandrasekaran S" first="Srinivas Niranj" last="Chandrasekaran">Srinivas Niranj Chandrasekaran</name>
<affiliation wicri:level="2"><nlm:affiliation>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7260.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Ambroggio, Xavier" sort="Ambroggio, Xavier" uniqKey="Ambroggio X" first="Xavier" last="Ambroggio">Xavier Ambroggio</name>
<affiliation wicri:level="2"><nlm:affiliation>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7260.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Kuhlman, Brian" sort="Kuhlman, Brian" uniqKey="Kuhlman B" first="Brian" last="Kuhlman">Brian Kuhlman</name>
<affiliation wicri:level="2"><nlm:affiliation>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7260.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
<wicri:cityArea>From the Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill</wicri:cityArea>
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<author><name sortKey="Carter, Charles W" sort="Carter, Charles W" uniqKey="Carter C" first="Charles W" last="Carter">Charles W. Carter</name>
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<country wicri:rule="url">États-Unis</country>
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<placeName><settlement type="city">Chapel Hill (Caroline du Nord)</settlement>
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<term>Adenosine Triphosphate (metabolism)</term>
<term>Amino Acid Sequence</term>
<term>Amino Acyl-tRNA Synthetases (chemistry)</term>
<term>Amino Acyl-tRNA Synthetases (genetics)</term>
<term>Amino Acyl-tRNA Synthetases (metabolism)</term>
<term>Aminoacylation</term>
<term>Biocatalysis</term>
<term>Catalytic Domain</term>
<term>Codon (chemistry)</term>
<term>Codon (metabolism)</term>
<term>Escherichia coli (genetics)</term>
<term>Escherichia coli (metabolism)</term>
<term>Evolution, Molecular</term>
<term>Gene Expression</term>
<term>Genetic Code</term>
<term>Kinetics</term>
<term>Molecular Sequence Data</term>
<term>Mutation</term>
<term>Peptides (chemistry)</term>
<term>Peptides (genetics)</term>
<term>Peptides (metabolism)</term>
<term>Protein Binding</term>
<term>Recombinant Proteins (chemistry)</term>
<term>Recombinant Proteins (genetics)</term>
<term>Recombinant Proteins (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Adénosine triphosphate ()</term>
<term>Adénosine triphosphate (métabolisme)</term>
<term>Amino acyl-tRNA synthetases ()</term>
<term>Amino acyl-tRNA synthetases (génétique)</term>
<term>Amino acyl-tRNA synthetases (métabolisme)</term>
<term>Aminoacylation</term>
<term>Biocatalyse</term>
<term>Cinétique</term>
<term>Code génétique</term>
<term>Codon ()</term>
<term>Codon (métabolisme)</term>
<term>Domaine catalytique</term>
<term>Données de séquences moléculaires</term>
<term>Escherichia coli (génétique)</term>
<term>Escherichia coli (métabolisme)</term>
<term>Expression des gènes</term>
<term>Liaison aux protéines</term>
<term>Mutation</term>
<term>Peptides ()</term>
<term>Peptides (génétique)</term>
<term>Peptides (métabolisme)</term>
<term>Protéines recombinantes ()</term>
<term>Protéines recombinantes (génétique)</term>
<term>Protéines recombinantes (métabolisme)</term>
<term>Séquence d'acides aminés</term>
<term>Évolution moléculaire</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Adenosine Triphosphate</term>
<term>Amino Acyl-tRNA Synthetases</term>
<term>Codon</term>
<term>Peptides</term>
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Amino Acyl-tRNA Synthetases</term>
<term>Peptides</term>
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Adenosine Triphosphate</term>
<term>Amino Acyl-tRNA Synthetases</term>
<term>Codon</term>
<term>Peptides</term>
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Escherichia coli</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Amino acyl-tRNA synthetases</term>
<term>Escherichia coli</term>
<term>Peptides</term>
<term>Protéines recombinantes</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Escherichia coli</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Adénosine triphosphate</term>
<term>Amino acyl-tRNA synthetases</term>
<term>Codon</term>
<term>Escherichia coli</term>
<term>Peptides</term>
<term>Protéines recombinantes</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term>
<term>Aminoacylation</term>
<term>Biocatalysis</term>
<term>Catalytic Domain</term>
<term>Evolution, Molecular</term>
<term>Gene Expression</term>
<term>Genetic Code</term>
<term>Kinetics</term>
<term>Molecular Sequence Data</term>
<term>Mutation</term>
<term>Protein Binding</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Adénosine triphosphate</term>
<term>Amino acyl-tRNA synthetases</term>
<term>Aminoacylation</term>
<term>Biocatalyse</term>
<term>Cinétique</term>
<term>Code génétique</term>
<term>Codon</term>
<term>Domaine catalytique</term>
<term>Données de séquences moléculaires</term>
<term>Expression des gènes</term>
<term>Liaison aux protéines</term>
<term>Mutation</term>
<term>Peptides</term>
<term>Protéines recombinantes</term>
<term>Séquence d'acides aminés</term>
<term>Évolution moléculaire</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en">Aminoacyl-tRNA synthetases (aaRS) catalyze both chemical steps that translate the universal genetic code. Rodin and Ohno offered an explanation for the existence of two aaRS classes, observing that codons for the most highly conserved Class I active-site residues are anticodons for corresponding Class II active-site residues. They proposed that the two classes arose simultaneously, by translation of opposite strands from the same gene. We have characterized wild-type 46-residue peptides containing ATP-binding sites of Class I and II synthetases and those coded by a gene designed by Rosetta to encode the corresponding peptides on opposite strands. Catalysis by WT and designed peptides is saturable, and the designed peptides are sensitive to active-site residue mutation. All have comparable apparent second-order rate constants 2.9-7.0E-3 M(-1) s(-1) or ∼750,000-1,300,000 times the uncatalyzed rate. The activities of the two complementary peptides demonstrate that the unique information in a gene can have two functional interpretations, one from each complementary strand. The peptides contain phylogenetic signatures of longer, more sophisticated catalysts we call Urzymes and are short enough to bridge the gap between them and simpler uncoded peptides. Thus, they directly substantiate the sense/antisense coding ancestry of Class I and II aaRS. Furthermore, designed 46-mers achieve similar catalytic proficiency to wild-type 46-mers by significant increases in both kcat and Km values, supporting suggestions that the earliest peptide catalysts activated ATP for biosynthetic purposes.</div>
</front>
</TEI>
<affiliations><list><country><li>États-Unis</li>
</country>
<region><li>Caroline du Nord</li>
</region>
<settlement><li>Chapel Hill (Caroline du Nord)</li>
</settlement>
<orgName><li>Université de Caroline du Nord à Chapel Hill</li>
</orgName>
</list>
<tree><country name="États-Unis"><region name="Caroline du Nord"><name sortKey="Martinez Rodriguez, Luis" sort="Martinez Rodriguez, Luis" uniqKey="Martinez Rodriguez L" first="Luis" last="Martinez-Rodriguez">Luis Martinez-Rodriguez</name>
</region>
<name sortKey="Ambroggio, Xavier" sort="Ambroggio, Xavier" uniqKey="Ambroggio X" first="Xavier" last="Ambroggio">Xavier Ambroggio</name>
<name sortKey="Carter, Charles W" sort="Carter, Charles W" uniqKey="Carter C" first="Charles W" last="Carter">Charles W. Carter</name>
<name sortKey="Chandrasekaran, Srinivas Niranj" sort="Chandrasekaran, Srinivas Niranj" uniqKey="Chandrasekaran S" first="Srinivas Niranj" last="Chandrasekaran">Srinivas Niranj Chandrasekaran</name>
<name sortKey="Collier, Martha" sort="Collier, Martha" uniqKey="Collier M" first="Martha" last="Collier">Martha Collier</name>
<name sortKey="Erdogan, Ozgun" sort="Erdogan, Ozgun" uniqKey="Erdogan O" first="Ozgün" last="Erdogan">Ozgün Erdogan</name>
<name sortKey="Gonzalez Rivera, Katiria" sort="Gonzalez Rivera, Katiria" uniqKey="Gonzalez Rivera K" first="Katiria" last="Gonzalez-Rivera">Katiria Gonzalez-Rivera</name>
<name sortKey="Jimenez Rodriguez, Mariel" sort="Jimenez Rodriguez, Mariel" uniqKey="Jimenez Rodriguez M" first="Mariel" last="Jimenez-Rodriguez">Mariel Jimenez-Rodriguez</name>
<name sortKey="Kuhlman, Brian" sort="Kuhlman, Brian" uniqKey="Kuhlman B" first="Brian" last="Kuhlman">Brian Kuhlman</name>
<name sortKey="Li, Li" sort="Li, Li" uniqKey="Li L" first="Li" last="Li">Li Li</name>
<name sortKey="Weinreb, Violetta" sort="Weinreb, Violetta" uniqKey="Weinreb V" first="Violetta" last="Weinreb">Violetta Weinreb</name>
<name sortKey="Williams, Tishan" sort="Williams, Tishan" uniqKey="Williams T" first="Tishan" last="Williams">Tishan Williams</name>
</country>
</tree>
</affiliations>
</record>

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Functional Class I and II Amino Acid-activating Enzymes Can Be Coded by Opposite Strands of the Same Gene.

Functional Class I and II Amino Acid-activating Enzymes Can Be Coded by Opposite Strands of the Same Gene.

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