Proteomic profiling of the monothiol glutaredoxin Grx3 reveals its global role in the regulation of iron dependent processes.
Identifieur interne : 000031 ( Main/Exploration ); précédent : 000030; suivant : 000032Proteomic profiling of the monothiol glutaredoxin Grx3 reveals its global role in the regulation of iron dependent processes.
Auteurs : Selma S. Alkafeef [États-Unis, Koweït] ; Shelley Lane [États-Unis] ; Clinton Yu [États-Unis] ; Tingting Zhou [États-Unis] ; Norma V. Solis [États-Unis] ; Scott G. Filler [États-Unis] ; Lan Huang [États-Unis] ; Haoping Liu [États-Unis]Source :
- PLoS genetics [ 1553-7404 ] ; 2020.
Descripteurs français
- KwdFr :
- Animaux (MeSH), Candida albicans (pathogénicité), Candida albicans (physiologie), Candidose invasive (microbiologie), Cartes d'interactions protéiques (génétique), Cartographie d'interactions entre protéines (MeSH), Facteurs de transcription GATA (métabolisme), Fer (métabolisme), Glutarédoxines (génétique), Glutarédoxines (isolement et purification), Glutarédoxines (métabolisme), Homéostasie (MeSH), Humains (MeSH), Hyphae (MeSH), Modèles animaux de maladie humaine (MeSH), Mutation (MeSH), Mâle (MeSH), Protéines fongiques (génétique), Protéines fongiques (isolement et purification), Protéines fongiques (métabolisme), Protéomique (MeSH), Régulation de l'expression des gènes fongiques (MeSH), Souris (MeSH), Virulence (génétique).
- MESH :
- génétique : Cartes d'interactions protéiques, Glutarédoxines, Protéines fongiques, Virulence.
- isolement et purification : Glutarédoxines, Protéines fongiques.
- microbiologie : Candidose invasive.
- métabolisme : Facteurs de transcription GATA, Fer, Glutarédoxines, Protéines fongiques.
- pathogénicité : Candida albicans.
- physiologie : Candida albicans.
- Animaux, Cartographie d'interactions entre protéines, Homéostasie, Humains, Hyphae, Modèles animaux de maladie humaine, Mutation, Mâle, Protéomique, Régulation de l'expression des gènes fongiques, Souris.
English descriptors
- KwdEn :
- Animals (MeSH), Candida albicans (pathogenicity), Candida albicans (physiology), Candidiasis, Invasive (microbiology), Disease Models, Animal (MeSH), Fungal Proteins (genetics), Fungal Proteins (isolation & purification), Fungal Proteins (metabolism), GATA Transcription Factors (metabolism), Gene Expression Regulation, Fungal (MeSH), Glutaredoxins (genetics), Glutaredoxins (isolation & purification), Glutaredoxins (metabolism), Homeostasis (MeSH), Humans (MeSH), Hyphae (MeSH), Iron (metabolism), Male (MeSH), Mice (MeSH), Mutation (MeSH), Protein Interaction Mapping (MeSH), Protein Interaction Maps (genetics), Proteomics (MeSH), Virulence (genetics).
- MESH :
- chemical , genetics : Fungal Proteins, Glutaredoxins.
- chemical , isolation & purification : Fungal Proteins, Glutaredoxins.
- chemical , metabolism : Fungal Proteins, GATA Transcription Factors, Glutaredoxins, Iron.
- genetics : Protein Interaction Maps, Virulence.
- microbiology : Candidiasis, Invasive.
- pathogenicity : Candida albicans.
- physiology : Candida albicans.
- Animals, Disease Models, Animal, Gene Expression Regulation, Fungal, Homeostasis, Humans, Hyphae, Male, Mice, Mutation, Protein Interaction Mapping, Proteomics.
Abstract
Iron is an essential nutrient required as a cofactor for many biological processes. As a fungal commensal-pathogen of humans, Candida albicans encounters a range of bioavailable iron levels in the human host and maintains homeostasis with a conserved regulatory circuit. How C. albicans senses and responds to iron availability is unknown. In model yeasts, regulation of the iron homeostasis circuit requires monothiol glutaredoxins (Grxs), but their functions beyond the regulatory circuit are unclear. Here, we show Grx3 is required for virulence and growth on low iron for C. albicans. To explore the global roles of Grx3, we applied a proteomic approach and performed in vivo cross-linked tandem affinity purification coupled with mass spectrometry. We identified a large number of Grx3 interacting proteins that function in diverse biological processes. This included Fra1 and Bol2/Fra2, which function with Grxs in intracellular iron trafficking in other organisms. Grx3 interacts with and regulates the activity of Sfu1 and Hap43, components of the C. albicans iron regulatory circuit. Unlike the regulatory circuit, which determines expression or repression of target genes in response to iron availability, Grx3 amplifies levels of gene expression or repression. Consistent with the proteomic data, the grx3 mutant is sensitive to heat shock, oxidative, nitrosative, and genotoxic stresses, and shows growth dependence on histidine, leucine, and tryptophan. We suggest Grx3 is a conserved global regulator of iron-dependent processes occurring within the cell.
DOI: 10.1371/journal.pgen.1008881
PubMed: 32525871
PubMed Central: PMC7319344
Affiliations:
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Alkafeef</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Chemistry, University of California, Irvine, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait.</nlm:affiliation><country xml:lang="fr">Koweït</country><wicri:regionArea>Department of Biochemistry, Faculty of Medicine, Kuwait University, Kuwait City</wicri:regionArea><wicri:noRegion>Kuwait City</wicri:noRegion></affiliation></author><author><name sortKey="Lane, Shelley" sort="Lane, Shelley" uniqKey="Lane S" first="Shelley" last="Lane">Shelley Lane</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Chemistry, University of California, Irvine, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Yu, Clinton" sort="Yu, Clinton" uniqKey="Yu C" first="Clinton" last="Yu">Clinton Yu</name><affiliation wicri:level="2"><nlm:affiliation>Department of Physiology & Biophysics, University of California, Irvine, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology & Biophysics, University of California, Irvine, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Zhou, Tingting" sort="Zhou, Tingting" uniqKey="Zhou T" first="Tingting" last="Zhou">Tingting Zhou</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Chemistry, University of California, Irvine, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Solis, Norma V" sort="Solis, Norma V" uniqKey="Solis N" first="Norma V" last="Solis">Norma V. 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Huang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Physiology & Biophysics, University of California, Irvine, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology & Biophysics, University of California, Irvine, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Liu, Haoping" sort="Liu, Haoping" uniqKey="Liu H" first="Haoping" last="Liu">Haoping Liu</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Chemistry, University of California, Irvine, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">PLoS genetics</title><idno type="eISSN">1553-7404</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Candida albicans (pathogenicity)</term><term>Candida albicans (physiology)</term><term>Candidiasis, Invasive (microbiology)</term><term>Disease Models, Animal (MeSH)</term><term>Fungal Proteins (genetics)</term><term>Fungal Proteins (isolation & purification)</term><term>Fungal Proteins (metabolism)</term><term>GATA Transcription Factors (metabolism)</term><term>Gene Expression Regulation, Fungal (MeSH)</term><term>Glutaredoxins (genetics)</term><term>Glutaredoxins (isolation & purification)</term><term>Glutaredoxins (metabolism)</term><term>Homeostasis (MeSH)</term><term>Humans (MeSH)</term><term>Hyphae (MeSH)</term><term>Iron (metabolism)</term><term>Male (MeSH)</term><term>Mice (MeSH)</term><term>Mutation (MeSH)</term><term>Protein Interaction Mapping (MeSH)</term><term>Protein Interaction Maps (genetics)</term><term>Proteomics (MeSH)</term><term>Virulence (genetics)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux (MeSH)</term><term>Candida albicans (pathogénicité)</term><term>Candida albicans (physiologie)</term><term>Candidose invasive (microbiologie)</term><term>Cartes d'interactions protéiques (génétique)</term><term>Cartographie d'interactions entre protéines (MeSH)</term><term>Facteurs de transcription GATA (métabolisme)</term><term>Fer (métabolisme)</term><term>Glutarédoxines (génétique)</term><term>Glutarédoxines (isolement et purification)</term><term>Glutarédoxines (métabolisme)</term><term>Homéostasie (MeSH)</term><term>Humains (MeSH)</term><term>Hyphae (MeSH)</term><term>Modèles animaux de maladie humaine (MeSH)</term><term>Mutation (MeSH)</term><term>Mâle (MeSH)</term><term>Protéines fongiques (génétique)</term><term>Protéines fongiques (isolement et purification)</term><term>Protéines fongiques (métabolisme)</term><term>Protéomique (MeSH)</term><term>Régulation de l'expression des gènes fongiques (MeSH)</term><term>Souris (MeSH)</term><term>Virulence (génétique)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Fungal Proteins</term><term>Glutaredoxins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="isolation & purification" xml:lang="en"><term>Fungal Proteins</term><term>Glutaredoxins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Fungal Proteins</term><term>GATA Transcription Factors</term><term>Glutaredoxins</term><term>Iron</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Protein Interaction Maps</term><term>Virulence</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Cartes d'interactions protéiques</term><term>Glutarédoxines</term><term>Protéines fongiques</term><term>Virulence</term></keywords><keywords scheme="MESH" qualifier="isolement et purification" xml:lang="fr"><term>Glutarédoxines</term><term>Protéines fongiques</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Candidose invasive</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Candidiasis, Invasive</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Facteurs de transcription GATA</term><term>Fer</term><term>Glutarédoxines</term><term>Protéines fongiques</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Candida albicans</term></keywords><keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr"><term>Candida albicans</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Candida albicans</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Candida albicans</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Disease Models, Animal</term><term>Gene Expression Regulation, Fungal</term><term>Homeostasis</term><term>Humans</term><term>Hyphae</term><term>Male</term><term>Mice</term><term>Mutation</term><term>Protein Interaction Mapping</term><term>Proteomics</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Cartographie d'interactions entre protéines</term><term>Homéostasie</term><term>Humains</term><term>Hyphae</term><term>Modèles animaux de maladie humaine</term><term>Mutation</term><term>Mâle</term><term>Protéomique</term><term>Régulation de l'expression des gènes fongiques</term><term>Souris</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Iron is an essential nutrient required as a cofactor for many biological processes. As a fungal commensal-pathogen of humans, Candida albicans encounters a range of bioavailable iron levels in the human host and maintains homeostasis with a conserved regulatory circuit. How C. albicans senses and responds to iron availability is unknown. In model yeasts, regulation of the iron homeostasis circuit requires monothiol glutaredoxins (Grxs), but their functions beyond the regulatory circuit are unclear. Here, we show Grx3 is required for virulence and growth on low iron for C. albicans. To explore the global roles of Grx3, we applied a proteomic approach and performed in vivo cross-linked tandem affinity purification coupled with mass spectrometry. We identified a large number of Grx3 interacting proteins that function in diverse biological processes. This included Fra1 and Bol2/Fra2, which function with Grxs in intracellular iron trafficking in other organisms. Grx3 interacts with and regulates the activity of Sfu1 and Hap43, components of the C. albicans iron regulatory circuit. Unlike the regulatory circuit, which determines expression or repression of target genes in response to iron availability, Grx3 amplifies levels of gene expression or repression. Consistent with the proteomic data, the grx3 mutant is sensitive to heat shock, oxidative, nitrosative, and genotoxic stresses, and shows growth dependence on histidine, leucine, and tryptophan. We suggest Grx3 is a conserved global regulator of iron-dependent processes occurring within the cell.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32525871</PMID><DateCompleted><Year>2020</Year><Month>08</Month><Day>31</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>18</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1553-7404</ISSN><JournalIssue CitedMedium="Internet"><Volume>16</Volume><Issue>6</Issue><PubDate><Year>2020</Year><Month>06</Month></PubDate></JournalIssue><Title>PLoS genetics</Title><ISOAbbreviation>PLoS Genet</ISOAbbreviation></Journal><ArticleTitle>Proteomic profiling of the monothiol glutaredoxin Grx3 reveals its global role in the regulation of iron dependent processes.</ArticleTitle><Pagination><MedlinePgn>e1008881</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pgen.1008881</ELocationID><Abstract><AbstractText>Iron is an essential nutrient required as a cofactor for many biological processes. As a fungal commensal-pathogen of humans, Candida albicans encounters a range of bioavailable iron levels in the human host and maintains homeostasis with a conserved regulatory circuit. How C. albicans senses and responds to iron availability is unknown. In model yeasts, regulation of the iron homeostasis circuit requires monothiol glutaredoxins (Grxs), but their functions beyond the regulatory circuit are unclear. Here, we show Grx3 is required for virulence and growth on low iron for C. albicans. To explore the global roles of Grx3, we applied a proteomic approach and performed in vivo cross-linked tandem affinity purification coupled with mass spectrometry. We identified a large number of Grx3 interacting proteins that function in diverse biological processes. This included Fra1 and Bol2/Fra2, which function with Grxs in intracellular iron trafficking in other organisms. Grx3 interacts with and regulates the activity of Sfu1 and Hap43, components of the C. albicans iron regulatory circuit. Unlike the regulatory circuit, which determines expression or repression of target genes in response to iron availability, Grx3 amplifies levels of gene expression or repression. Consistent with the proteomic data, the grx3 mutant is sensitive to heat shock, oxidative, nitrosative, and genotoxic stresses, and shows growth dependence on histidine, leucine, and tryptophan. We suggest Grx3 is a conserved global regulator of iron-dependent processes occurring within the cell.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Alkafeef</LastName><ForeName>Selma S</ForeName><Initials>SS</Initials><AffiliationInfo><Affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biochemistry, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lane</LastName><ForeName>Shelley</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0003-2325-7207</Identifier><AffiliationInfo><Affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yu</LastName><ForeName>Clinton</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-2931-5474</Identifier><AffiliationInfo><Affiliation>Department of Physiology & Biophysics, University of California, Irvine, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Tingting</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Solis</LastName><ForeName>Norma V</ForeName><Initials>NV</Initials><AffiliationInfo><Affiliation>Division of Infectious Diseases, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Filler</LastName><ForeName>Scott G</ForeName><Initials>SG</Initials><Identifier Source="ORCID">0000-0001-7278-3700</Identifier><AffiliationInfo><Affiliation>Division of Infectious Diseases, Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, California, United States of America.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>David Geffen School of Medicine at UCLA, Los Angeles, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huang</LastName><ForeName>Lan</ForeName><Initials>L</Initials><Identifier Source="ORCID">0000-0002-3140-4687</Identifier><AffiliationInfo><Affiliation>Department of Physiology & Biophysics, University of California, Irvine, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Haoping</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0003-3489-7103</Identifier><AffiliationInfo><Affiliation>Department of Biological Chemistry, University of California, Irvine, California, United States of America.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 AI124566</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 AI099190</GrantID><Acronym>AI</Acronym><Agency>NIAID NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 GM074830</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 DE026600</GrantID><Acronym>DE</Acronym><Agency>NIDCR NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 GM130144</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 DE017088</GrantID><Acronym>DE</Acronym><Agency>NIDCR NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 GM117111</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>11</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS Genet</MedlineTA><NlmUniqueID>101239074</NlmUniqueID><ISSNLinking>1553-7390</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D050980">GATA Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D054477">Glutaredoxins</NameOfSubstance></Chemical><Chemical><RegistryNumber>E1UOL152H7</RegistryNumber><NameOfSubstance UI="D007501">Iron</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002176" MajorTopicYN="N">Candida albicans</DescriptorName><QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D058365" MajorTopicYN="N">Candidiasis, Invasive</DescriptorName><QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D004195" MajorTopicYN="N">Disease Models, Animal</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName><QualifierName UI="Q000235" 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MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D025301" MajorTopicYN="N">Hyphae</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007501" MajorTopicYN="N">Iron</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009154" MajorTopicYN="N">Mutation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D025941" MajorTopicYN="N">Protein Interaction Mapping</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D060066" MajorTopicYN="N">Protein Interaction Maps</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D040901" 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Solis</name><name sortKey="Yu, Clinton" sort="Yu, Clinton" uniqKey="Yu C" first="Clinton" last="Yu">Clinton Yu</name><name sortKey="Zhou, Tingting" sort="Zhou, Tingting" uniqKey="Zhou T" first="Tingting" last="Zhou">Tingting Zhou</name></country><country name="Koweït"><noRegion><name sortKey="Alkafeef, Selma S" sort="Alkafeef, Selma S" uniqKey="Alkafeef S" first="Selma S" last="Alkafeef">Selma S. Alkafeef</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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