RapamycinFungusV1, Main, Exploration, bibRecord, 000651

Azole resistance in a Candida albicans mutant lacking the ABC transporter CDR6/ROA1 depends on TOR signaling.

Identifieur interne : 000651 ( Main/Exploration ); précédent : 000650; suivant : 000652

Azole resistance in a Candida albicans mutant lacking the ABC transporter CDR6/ROA1 depends on TOR signaling.

Auteurs : Nitesh Kumar Khandelwal [Inde] ; Neeraj Chauhan [États-Unis] ; Parijat Sarkar [Inde] ; Brooke D. Esquivel [États-Unis] ; Paola Coccetti [Italie] ; Ashutosh Singh [Inde] ; Alix T. Coste [Suisse] ; Meghna Gupta [Inde, États-Unis] ; Dominique Sanglard [Suisse] ; Theodore C. White [États-Unis] ; Murielle Chauvel [France] ; Christophe D'Enfert [France] ; Amitabha Chattopadhyay [Inde] ; Naseem A. Gaur ; Alok Kumar Mondal [Inde] ; Rajendra Prasad [Oman, Inde]

Source :

The Journal of biological chemistry [ 1083-351X ] ; 2018.

RBID : pubmed:29158264

Descripteurs français

English descriptors

KwdEn :
- ATP-Binding Cassette Transporters (genetics), ATP-Binding Cassette Transporters (metabolism), Antifungal Agents (pharmacology), Azoles (pharmacology), Biological Transport (drug effects), Biological Transport (genetics), Candida albicans (drug effects), Candida albicans (genetics), Candida albicans (metabolism), Drug Resistance, Fungal (drug effects), Drug Resistance, Fungal (genetics), Fluconazole (pharmacology), Fluorescence Recovery After Photobleaching (MeSH), Fungal Proteins (genetics), Fungal Proteins (metabolism), Membrane Transport Proteins (genetics), Membrane Transport Proteins (metabolism), Microbial Sensitivity Tests (MeSH), TOR Serine-Threonine Kinases (genetics), TOR Serine-Threonine Kinases (metabolism).
MESH :
- chemical , genetics : ATP-Binding Cassette Transporters, Fungal Proteins, Membrane Transport Proteins, TOR Serine-Threonine Kinases.
- chemical , metabolism : ATP-Binding Cassette Transporters, Fungal Proteins, Membrane Transport Proteins, TOR Serine-Threonine Kinases.
- chemical , pharmacology : Antifungal Agents, Azoles, Fluconazole.
- drug effects : Biological Transport, Candida albicans, Drug Resistance, Fungal.
- genetics : Biological Transport, Candida albicans, Drug Resistance, Fungal.
- metabolism : Candida albicans.
- Fluorescence Recovery After Photobleaching, Microbial Sensitivity Tests.

Abstract

ATP-binding cassette (ABC) transporters help export various substrates across the cell membrane and significantly contribute to drug resistance. However, a recent study reported an unusual case in which the loss of an ABC transporter in Candida albicans, orf19.4531 (previously named ROA1), increases resistance against antifungal azoles, which was attributed to an altered membrane potential in the mutant strain. To obtain further mechanistic insights into this phenomenon, here we confirmed that the plasma membrane-localized transporter (renamed CDR6/ROA1 for consistency with C. albicans nomenclature) could efflux xenobiotics such as berberine, rhodamine 123, and paraquat. Moreover, a CDR6/ROA1 null mutant, NKKY101, displayed increased susceptibility to these xenobiotics. Interestingly, fluorescence recovery after photobleaching (FRAP) results indicated that NKKY101 mutant cells exhibited increased plasma membrane rigidity, resulting in reduced azole accumulation and contributing to azole resistance. Transcriptional profiling revealed that ribosome biogenesis genes were significantly up-regulated in the NKKY101 mutant. As ribosome biogenesis is a well-known downstream phenomenon of target of rapamycin (TOR1) signaling, we suspected a link between ribosome biogenesis and TOR1 signaling in NKKY101. Therefore, we grew NKKY101 cells on rapamycin and observed TOR1 hyperactivation, which leads to Hsp90-dependent calcineurin stabilization and thereby increased azole resistance. This in vitro finding was supported by in vivo data from a mouse model of systemic infection in which NKKY101 cells led to higher fungal load after fluconazole challenge than wild-type cells. Taken together, our study uncovers a mechanism of azole resistance in C. albicans, involving increased membrane rigidity and TOR signaling.

DOI: 10.1074/jbc.M117.807032
PubMed: 29158264
PubMed Central: PMC5767851

Affiliations:

France, Inde, Italie, Oman, Suisse, États-Unis
Californie, Lombardie, Missouri (État), New Jersey, Île-de-France
Milan, Paris

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Le document en format XML

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 mutant lacking the ABC transporter <i>CDR6/ROA1</i>
 depends on TOR signaling.</title>
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<author><name sortKey="Esquivel, Brooke D" sort="Esquivel, Brooke D" uniqKey="Esquivel B" first="Brooke D" last="Esquivel">Brooke D. Esquivel</name>
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<author><name sortKey="Singh, Ashutosh" sort="Singh, Ashutosh" uniqKey="Singh A" first="Ashutosh" last="Singh">Ashutosh Singh</name>
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<affiliation wicri:level="1"><nlm:affiliation>the Department of Biochemistry, Lucknow University, Lucknow 226024, Uttar Pradesh, India.</nlm:affiliation>
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<author><name sortKey="Coste, Alix T" sort="Coste, Alix T" uniqKey="Coste A" first="Alix T" last="Coste">Alix T. Coste</name>
<affiliation wicri:level="1"><nlm:affiliation>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011, Switzerland.</nlm:affiliation>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011</wicri:regionArea>
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</affiliation>
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<author><name sortKey="Gupta, Meghna" sort="Gupta, Meghna" uniqKey="Gupta M" first="Meghna" last="Gupta">Meghna Gupta</name>
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</placeName>
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<author><name sortKey="Sanglard, Dominique" sort="Sanglard, Dominique" uniqKey="Sanglard D" first="Dominique" last="Sanglard">Dominique Sanglard</name>
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<country xml:lang="fr">Suisse</country>
<wicri:regionArea>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011</wicri:regionArea>
<wicri:noRegion>CH-1011</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="White, Theodore C" sort="White, Theodore C" uniqKey="White T" first="Theodore C" last="White">Theodore C. White</name>
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<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Missouri (État)</region>
</placeName>
<wicri:cityArea>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City</wicri:cityArea>
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<author><name sortKey="Chauvel, Murielle" sort="Chauvel, Murielle" uniqKey="Chauvel M" first="Murielle" last="Chauvel">Murielle Chauvel</name>
<affiliation wicri:level="3"><nlm:affiliation>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris</wicri:regionArea>
<placeName><region type="region" nuts="2">Île-de-France</region>
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<author><name sortKey="D Enfert, Christophe" sort="D Enfert, Christophe" uniqKey="D Enfert C" first="Christophe" last="D'Enfert">Christophe D'Enfert</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris</wicri:regionArea>
<placeName><region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Chattopadhyay, Amitabha" sort="Chattopadhyay, Amitabha" uniqKey="Chattopadhyay A" first="Amitabha" last="Chattopadhyay">Amitabha Chattopadhyay</name>
<affiliation wicri:level="1"><nlm:affiliation>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007</wicri:regionArea>
<wicri:noRegion>Hyderabad 500007</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Gaur, Naseem A" sort="Gaur, Naseem A" uniqKey="Gaur N" first="Naseem A" last="Gaur">Naseem A. Gaur</name>
<affiliation><nlm:affiliation>the International Centre for Genetic Engineering and Biotechnology, New Delhi 110067, India, and.</nlm:affiliation>
<wicri:noCountry code="subField">and</wicri:noCountry>
</affiliation>
</author>
<author><name sortKey="Mondal, Alok Kumar" sort="Mondal, Alok Kumar" uniqKey="Mondal A" first="Alok Kumar" last="Mondal">Alok Kumar Mondal</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067</wicri:regionArea>
<wicri:noRegion>New Delhi 110067</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Prasad, Rajendra" sort="Prasad, Rajendra" uniqKey="Prasad R" first="Rajendra" last="Prasad">Rajendra Prasad</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India, rp47jnu@gmail.com.</nlm:affiliation>
<country wicri:rule="url">Oman</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India</wicri:regionArea>
<wicri:noRegion>India</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:affiliation>the Amity Institute of Integrative Sciences and Health, Amity University Haryana, Amity Education Valley Gurgaon-122413, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>the Amity Institute of Integrative Sciences and Health, Amity University Haryana, Amity Education Valley Gurgaon-122413</wicri:regionArea>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Azole resistance in a <i>Candida albicans</i>
 mutant lacking the ABC transporter <i>CDR6/ROA1</i>
 depends on TOR signaling.</title>
<author><name sortKey="Khandelwal, Nitesh Kumar" sort="Khandelwal, Nitesh Kumar" uniqKey="Khandelwal N" first="Nitesh Kumar" last="Khandelwal">Nitesh Kumar Khandelwal</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067</wicri:regionArea>
<wicri:noRegion>New Delhi 110067</wicri:noRegion>
</affiliation>
<affiliation><nlm:affiliation>the International Centre for Genetic Engineering and Biotechnology, New Delhi 110067, India, and.</nlm:affiliation>
<wicri:noCountry code="subField">and</wicri:noCountry>
</affiliation>
</author>
<author><name sortKey="Chauhan, Neeraj" sort="Chauhan, Neeraj" uniqKey="Chauhan N" first="Neeraj" last="Chauhan">Neeraj Chauhan</name>
<affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology, Biochemistry, and Molecular Genetics, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, New Jersey 07103.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">New Jersey</region>
</placeName>
<wicri:cityArea>Department of Microbiology, Biochemistry, and Molecular Genetics, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Sarkar, Parijat" sort="Sarkar, Parijat" uniqKey="Sarkar P" first="Parijat" last="Sarkar">Parijat Sarkar</name>
<affiliation wicri:level="1"><nlm:affiliation>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007</wicri:regionArea>
<wicri:noRegion>Hyderabad 500007</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Esquivel, Brooke D" sort="Esquivel, Brooke D" uniqKey="Esquivel B" first="Brooke D" last="Esquivel">Brooke D. Esquivel</name>
<affiliation wicri:level="2"><nlm:affiliation>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City, Missouri 64110.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Missouri (État)</region>
</placeName>
<wicri:cityArea>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Coccetti, Paola" sort="Coccetti, Paola" uniqKey="Coccetti P" first="Paola" last="Coccetti">Paola Coccetti</name>
<affiliation wicri:level="1"><nlm:affiliation>the Department of Biotechnology and Biosciences, University of Milano-Bicocca, 20126 Milan, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>the Department of Biotechnology and Biosciences, University of Milano-Bicocca, 20126 Milan</wicri:regionArea>
<placeName><settlement type="city">Milan</settlement>
<region nuts="2">Lombardie</region>
</placeName>
</affiliation>
<affiliation wicri:level="1"><nlm:affiliation>SYSBIO, Centre of Systems Biology, 20126 Milan, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>SYSBIO, Centre of Systems Biology, 20126 Milan</wicri:regionArea>
<placeName><settlement type="city">Milan</settlement>
<region nuts="2">Lombardie</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Singh, Ashutosh" sort="Singh, Ashutosh" uniqKey="Singh A" first="Ashutosh" last="Singh">Ashutosh Singh</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067</wicri:regionArea>
<wicri:noRegion>New Delhi 110067</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:affiliation>the Department of Biochemistry, Lucknow University, Lucknow 226024, Uttar Pradesh, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>the Department of Biochemistry, Lucknow University, Lucknow 226024, Uttar Pradesh</wicri:regionArea>
<wicri:noRegion>Uttar Pradesh</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Coste, Alix T" sort="Coste, Alix T" uniqKey="Coste A" first="Alix T" last="Coste">Alix T. Coste</name>
<affiliation wicri:level="1"><nlm:affiliation>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011, Switzerland.</nlm:affiliation>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011</wicri:regionArea>
<wicri:noRegion>CH-1011</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Gupta, Meghna" sort="Gupta, Meghna" uniqKey="Gupta M" first="Meghna" last="Gupta">Meghna Gupta</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067</wicri:regionArea>
<wicri:noRegion>New Delhi 110067</wicri:noRegion>
</affiliation>
<affiliation wicri:level="2"><nlm:affiliation>the Department of Biochemistry and Biophysics, University of California, San Francisco, California 94158.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>the Department of Biochemistry and Biophysics, University of California, San Francisco</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Sanglard, Dominique" sort="Sanglard, Dominique" uniqKey="Sanglard D" first="Dominique" last="Sanglard">Dominique Sanglard</name>
<affiliation wicri:level="1"><nlm:affiliation>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011, Switzerland.</nlm:affiliation>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011</wicri:regionArea>
<wicri:noRegion>CH-1011</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="White, Theodore C" sort="White, Theodore C" uniqKey="White T" first="Theodore C" last="White">Theodore C. White</name>
<affiliation wicri:level="2"><nlm:affiliation>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City, Missouri 64110.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Missouri (État)</region>
</placeName>
<wicri:cityArea>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Chauvel, Murielle" sort="Chauvel, Murielle" uniqKey="Chauvel M" first="Murielle" last="Chauvel">Murielle Chauvel</name>
<affiliation wicri:level="3"><nlm:affiliation>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris</wicri:regionArea>
<placeName><region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="D Enfert, Christophe" sort="D Enfert, Christophe" uniqKey="D Enfert C" first="Christophe" last="D'Enfert">Christophe D'Enfert</name>
<affiliation wicri:level="3"><nlm:affiliation>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris</wicri:regionArea>
<placeName><region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Chattopadhyay, Amitabha" sort="Chattopadhyay, Amitabha" uniqKey="Chattopadhyay A" first="Amitabha" last="Chattopadhyay">Amitabha Chattopadhyay</name>
<affiliation wicri:level="1"><nlm:affiliation>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007</wicri:regionArea>
<wicri:noRegion>Hyderabad 500007</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Gaur, Naseem A" sort="Gaur, Naseem A" uniqKey="Gaur N" first="Naseem A" last="Gaur">Naseem A. Gaur</name>
<affiliation><nlm:affiliation>the International Centre for Genetic Engineering and Biotechnology, New Delhi 110067, India, and.</nlm:affiliation>
<wicri:noCountry code="subField">and</wicri:noCountry>
</affiliation>
</author>
<author><name sortKey="Mondal, Alok Kumar" sort="Mondal, Alok Kumar" uniqKey="Mondal A" first="Alok Kumar" last="Mondal">Alok Kumar Mondal</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067</wicri:regionArea>
<wicri:noRegion>New Delhi 110067</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Prasad, Rajendra" sort="Prasad, Rajendra" uniqKey="Prasad R" first="Rajendra" last="Prasad">Rajendra Prasad</name>
<affiliation wicri:level="1"><nlm:affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India, rp47jnu@gmail.com.</nlm:affiliation>
<country wicri:rule="url">Oman</country>
<wicri:regionArea>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India</wicri:regionArea>
<wicri:noRegion>India</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:affiliation>the Amity Institute of Integrative Sciences and Health, Amity University Haryana, Amity Education Valley Gurgaon-122413, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>the Amity Institute of Integrative Sciences and Health, Amity University Haryana, Amity Education Valley Gurgaon-122413</wicri:regionArea>
<wicri:noRegion>Amity Education Valley Gurgaon-122413</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series><title level="j">The Journal of biological chemistry</title>
<idno type="eISSN">1083-351X</idno>
<imprint><date when="2018" type="published">2018</date>
</imprint>
</series>
</biblStruct>
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</fileDesc>
<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>ATP-Binding Cassette Transporters (genetics)</term>
<term>ATP-Binding Cassette Transporters (metabolism)</term>
<term>Antifungal Agents (pharmacology)</term>
<term>Azoles (pharmacology)</term>
<term>Biological Transport (drug effects)</term>
<term>Biological Transport (genetics)</term>
<term>Candida albicans (drug effects)</term>
<term>Candida albicans (genetics)</term>
<term>Candida albicans (metabolism)</term>
<term>Drug Resistance, Fungal (drug effects)</term>
<term>Drug Resistance, Fungal (genetics)</term>
<term>Fluconazole (pharmacology)</term>
<term>Fluorescence Recovery After Photobleaching (MeSH)</term>
<term>Fungal Proteins (genetics)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Membrane Transport Proteins (genetics)</term>
<term>Membrane Transport Proteins (metabolism)</term>
<term>Microbial Sensitivity Tests (MeSH)</term>
<term>TOR Serine-Threonine Kinases (genetics)</term>
<term>TOR Serine-Threonine Kinases (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Antifongiques (pharmacologie)</term>
<term>Azoles (pharmacologie)</term>
<term>Candida albicans (effets des médicaments et des substances chimiques)</term>
<term>Candida albicans (génétique)</term>
<term>Candida albicans (métabolisme)</term>
<term>Fluconazole (pharmacologie)</term>
<term>Protéines de transport membranaire (génétique)</term>
<term>Protéines de transport membranaire (métabolisme)</term>
<term>Protéines fongiques (génétique)</term>
<term>Protéines fongiques (métabolisme)</term>
<term>Redistribution de fluorescence après photoblanchiment (MeSH)</term>
<term>Résistance des champignons aux médicaments (effets des médicaments et des substances chimiques)</term>
<term>Résistance des champignons aux médicaments (génétique)</term>
<term>Sérine-thréonine kinases TOR (génétique)</term>
<term>Sérine-thréonine kinases TOR (métabolisme)</term>
<term>Tests de sensibilité microbienne (MeSH)</term>
<term>Transport biologique (effets des médicaments et des substances chimiques)</term>
<term>Transport biologique (génétique)</term>
<term>Transporteurs ABC (génétique)</term>
<term>Transporteurs ABC (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>ATP-Binding Cassette Transporters</term>
<term>Fungal Proteins</term>
<term>Membrane Transport Proteins</term>
<term>TOR Serine-Threonine Kinases</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>ATP-Binding Cassette Transporters</term>
<term>Fungal Proteins</term>
<term>Membrane Transport Proteins</term>
<term>TOR Serine-Threonine Kinases</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Antifungal Agents</term>
<term>Azoles</term>
<term>Fluconazole</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Biological Transport</term>
<term>Candida albicans</term>
<term>Drug Resistance, Fungal</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr"><term>Candida albicans</term>
<term>Résistance des champignons aux médicaments</term>
<term>Transport biologique</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Biological Transport</term>
<term>Candida albicans</term>
<term>Drug Resistance, Fungal</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Candida albicans</term>
<term>Protéines de transport membranaire</term>
<term>Protéines fongiques</term>
<term>Résistance des champignons aux médicaments</term>
<term>Sérine-thréonine kinases TOR</term>
<term>Transport biologique</term>
<term>Transporteurs ABC</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Candida albicans</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Candida albicans</term>
<term>Protéines de transport membranaire</term>
<term>Protéines fongiques</term>
<term>Sérine-thréonine kinases TOR</term>
<term>Transporteurs ABC</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr"><term>Antifongiques</term>
<term>Azoles</term>
<term>Fluconazole</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Fluorescence Recovery After Photobleaching</term>
<term>Microbial Sensitivity Tests</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Redistribution de fluorescence après photoblanchiment</term>
<term>Tests de sensibilité microbienne</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en">ATP-binding cassette (ABC) transporters help export various substrates across the cell membrane and significantly contribute to drug resistance. However, a recent study reported an unusual case in which the loss of an ABC transporter in <i>Candida albicans</i>
, orf19.4531 (previously named ROA1), increases resistance against antifungal azoles, which was attributed to an altered membrane potential in the mutant strain. To obtain further mechanistic insights into this phenomenon, here we confirmed that the plasma membrane-localized transporter (renamed <i>CDR6/ROA1</i>
 for consistency with <i>C. albicans</i>
 nomenclature) could efflux xenobiotics such as berberine, rhodamine 123, and paraquat. Moreover, a <i>CDR6/ROA1</i>
 null mutant, NKKY101, displayed increased susceptibility to these xenobiotics. Interestingly, fluorescence recovery after photobleaching (FRAP) results indicated that NKKY101 mutant cells exhibited increased plasma membrane rigidity, resulting in reduced azole accumulation and contributing to azole resistance. Transcriptional profiling revealed that ribosome biogenesis genes were significantly up-regulated in the NKKY101 mutant. As ribosome biogenesis is a well-known downstream phenomenon of target of rapamycin (TOR1) signaling, we suspected a link between ribosome biogenesis and TOR1 signaling in NKKY101. Therefore, we grew NKKY101 cells on rapamycin and observed TOR1 hyperactivation, which leads to Hsp90-dependent calcineurin stabilization and thereby increased azole resistance. This <i>in vitro</i>
 finding was supported by <i>in vivo</i>
 data from a mouse model of systemic infection in which NKKY101 cells led to higher fungal load after fluconazole challenge than wild-type cells. Taken together, our study uncovers a mechanism of azole resistance in <i>C. albicans</i>
, involving increased membrane rigidity and TOR signaling.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29158264</PMID>
<DateCompleted><Year>2018</Year>
<Month>11</Month>
<Day>26</Day>
</DateCompleted>
<DateRevised><Year>2019</Year>
<Month>01</Month>
<Day>12</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1083-351X</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>293</Volume>
<Issue>2</Issue>
<PubDate><Year>2018</Year>
<Month>01</Month>
<Day>12</Day>
</PubDate>
</JournalIssue>
<Title>The Journal of biological chemistry</Title>
<ISOAbbreviation>J Biol Chem</ISOAbbreviation>
</Journal>
<ArticleTitle>Azole resistance in a <i>Candida albicans</i>
 mutant lacking the ABC transporter <i>CDR6/ROA1</i>
 depends on TOR signaling.</ArticleTitle>
<Pagination><MedlinePgn>412-432</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1074/jbc.M117.807032</ELocationID>
<Abstract><AbstractText>ATP-binding cassette (ABC) transporters help export various substrates across the cell membrane and significantly contribute to drug resistance. However, a recent study reported an unusual case in which the loss of an ABC transporter in <i>Candida albicans</i>
, orf19.4531 (previously named ROA1), increases resistance against antifungal azoles, which was attributed to an altered membrane potential in the mutant strain. To obtain further mechanistic insights into this phenomenon, here we confirmed that the plasma membrane-localized transporter (renamed <i>CDR6/ROA1</i>
 for consistency with <i>C. albicans</i>
 nomenclature) could efflux xenobiotics such as berberine, rhodamine 123, and paraquat. Moreover, a <i>CDR6/ROA1</i>
 null mutant, NKKY101, displayed increased susceptibility to these xenobiotics. Interestingly, fluorescence recovery after photobleaching (FRAP) results indicated that NKKY101 mutant cells exhibited increased plasma membrane rigidity, resulting in reduced azole accumulation and contributing to azole resistance. Transcriptional profiling revealed that ribosome biogenesis genes were significantly up-regulated in the NKKY101 mutant. As ribosome biogenesis is a well-known downstream phenomenon of target of rapamycin (TOR1) signaling, we suspected a link between ribosome biogenesis and TOR1 signaling in NKKY101. Therefore, we grew NKKY101 cells on rapamycin and observed TOR1 hyperactivation, which leads to Hsp90-dependent calcineurin stabilization and thereby increased azole resistance. This <i>in vitro</i>
 finding was supported by <i>in vivo</i>
 data from a mouse model of systemic infection in which NKKY101 cells led to higher fungal load after fluconazole challenge than wild-type cells. Taken together, our study uncovers a mechanism of azole resistance in <i>C. albicans</i>
, involving increased membrane rigidity and TOR signaling.</AbstractText>
<CopyrightInformation>© 2018 by The American Society for Biochemistry and Molecular Biology, Inc.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Khandelwal</LastName>
<ForeName>Nitesh Kumar</ForeName>
<Initials>NK</Initials>
<AffiliationInfo><Affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>the International Centre for Genetic Engineering and Biotechnology, New Delhi 110067, India, and.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Chauhan</LastName>
<ForeName>Neeraj</ForeName>
<Initials>N</Initials>
<AffiliationInfo><Affiliation>Department of Microbiology, Biochemistry, and Molecular Genetics, New Jersey Medical School, Rutgers, The State University of New Jersey, Newark, New Jersey 07103.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Sarkar</LastName>
<ForeName>Parijat</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Esquivel</LastName>
<ForeName>Brooke D</ForeName>
<Initials>BD</Initials>
<AffiliationInfo><Affiliation>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City, Missouri 64110.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Coccetti</LastName>
<ForeName>Paola</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>the Department of Biotechnology and Biosciences, University of Milano-Bicocca, 20126 Milan, Italy.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>SYSBIO, Centre of Systems Biology, 20126 Milan, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Singh</LastName>
<ForeName>Ashutosh</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>the Department of Biochemistry, Lucknow University, Lucknow 226024, Uttar Pradesh, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Coste</LastName>
<ForeName>Alix T</ForeName>
<Initials>AT</Initials>
<AffiliationInfo><Affiliation>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Gupta</LastName>
<ForeName>Meghna</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>the Department of Biochemistry and Biophysics, University of California, San Francisco, California 94158.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Sanglard</LastName>
<ForeName>Dominique</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>the Institute of Microbiology, University of Lausanne and University Hospital Center, Rue du Bugnon 48, Lausanne, CH-1011, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>White</LastName>
<ForeName>Theodore C</ForeName>
<Initials>TC</Initials>
<AffiliationInfo><Affiliation>the School of Biological Sciences, Cell Biology, and Biophysics, University of Missouri, Kansas City, Missouri 64110.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Chauvel</LastName>
<ForeName>Murielle</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>d'Enfert</LastName>
<ForeName>Christophe</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>the Département Génomes et Génétique, Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, INRA, 75015 Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Chattopadhyay</LastName>
<ForeName>Amitabha</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>the CSIR-Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500007, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Gaur</LastName>
<ForeName>Naseem A</ForeName>
<Initials>NA</Initials>
<AffiliationInfo><Affiliation>the International Centre for Genetic Engineering and Biotechnology, New Delhi 110067, India, and.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Mondal</LastName>
<ForeName>Alok Kumar</ForeName>
<Initials>AK</Initials>
<AffiliationInfo><Affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Prasad</LastName>
<ForeName>Rajendra</ForeName>
<Initials>R</Initials>
<AffiliationInfo><Affiliation>From the School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India, rp47jnu@gmail.com.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>the Amity Institute of Integrative Sciences and Health, Amity University Haryana, Amity Education Valley Gurgaon-122413, India.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y"><Grant><GrantID>R01 AI124499</GrantID>
<Acronym>AI</Acronym>
<Agency>NIAID 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>2017</Year>
<Month>11</Month>
<Day>20</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>J Biol Chem</MedlineTA>
<NlmUniqueID>2985121R</NlmUniqueID>
<ISSNLinking>0021-9258</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D018528">ATP-Binding Cassette Transporters</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D000935">Antifungal Agents</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D001393">Azoles</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D026901">Membrane Transport Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>8VZV102JFY</RegistryNumber>
<NameOfSubstance UI="D015725">Fluconazole</NameOfSubstance>
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<Chemical><RegistryNumber>EC 2.7.1.1</RegistryNumber>
<NameOfSubstance UI="D058570">TOR Serine-Threonine Kinases</NameOfSubstance>
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</ChemicalList>
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<MeshHeadingList><MeshHeading><DescriptorName UI="D018528" MajorTopicYN="N">ATP-Binding Cassette Transporters</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000935" MajorTopicYN="N">Antifungal Agents</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001393" MajorTopicYN="N">Azoles</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001692" MajorTopicYN="N">Biological Transport</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002176" MajorTopicYN="N">Candida albicans</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D025141" MajorTopicYN="N">Drug Resistance, Fungal</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D015725" MajorTopicYN="N">Fluconazole</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D036681" MajorTopicYN="N">Fluorescence Recovery After Photobleaching</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D026901" MajorTopicYN="N">Membrane Transport Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008826" MajorTopicYN="N">Microbial Sensitivity Tests</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D058570" MajorTopicYN="N">TOR Serine-Threonine Kinases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">ABC transporter</Keyword>
<Keyword MajorTopicYN="Y">Azole resistance</Keyword>
<Keyword MajorTopicYN="Y">CDR6</Keyword>
<Keyword MajorTopicYN="Y">TOR signaling</Keyword>
<Keyword MajorTopicYN="Y">mTOR complex (mTORC)</Keyword>
<Keyword MajorTopicYN="Y">membrane transport</Keyword>
<Keyword MajorTopicYN="Y">multidrug transporter</Keyword>
<Keyword MajorTopicYN="Y">yeast</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2017</Year>
<Month>07</Month>
<Day>16</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised"><Year>2017</Year>
<Month>11</Month>
<Day>17</Day>
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Azole resistance in a Candida albicans mutant lacking the ABC transporter CDR6/ROA1 depends on TOR signaling.

Azole resistance in a Candida albicans mutant lacking the ABC transporter CDR6/ROA1 depends on TOR signaling.

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