Host-Imposed Copper Poisoning Impacts Fungal Micronutrient Acquisition during Systemic Candida albicans Infections
Nutritional immunity is a process whereby an infected host manipulates essential micronutrients to defend against an invading pathogen. We reveal a dynamic aspect of nutritional immunity during infection that involves copper assimilation. Using a combination of laser ablation inductively coupled mas...
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Published in | PloS one Vol. 11; no. 6; p. e0158683 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
30.06.2016
Public Library of Science (PLoS) |
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Abstract | Nutritional immunity is a process whereby an infected host manipulates essential micronutrients to defend against an invading pathogen. We reveal a dynamic aspect of nutritional immunity during infection that involves copper assimilation. Using a combination of laser ablation inductively coupled mass spectrometry (LA-ICP MS) and metal mapping, immunohistochemistry, and gene expression profiling from infected tissues, we show that readjustments in hepatic, splenic and renal copper homeostasis accompany disseminated Candida albicans infections in the mouse model. Localized host-imposed copper poisoning manifests itself as a transient increase in copper early in the kidney infection. Changes in renal copper are detected by the fungus, as revealed by gene expression profiling and fungal virulence studies. The fungus responds by differentially regulating the Crp1 copper efflux pump (higher expression during early infection and down-regulation late in infection) and the Ctr1 copper importer (lower expression during early infection, and subsequent up-regulation late in infection) to maintain copper homeostasis during disease progression. Both Crp1 and Ctr1 are required for full fungal virulence. Importantly, copper homeostasis influences other virulence traits-metabolic flexibility and oxidative stress resistance. Our study highlights the importance of copper homeostasis for host defence and fungal virulence during systemic disease. |
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AbstractList | Nutritional immunity is a process whereby an infected host manipulates essential micronutrients to defend against an invading pathogen. We reveal a dynamic aspect of nutritional immunity during infection that involves copper assimilation. Using a combination of laser ablation inductively coupled mass spectrometry (LA-ICP MS) and metal mapping, immunohistochemistry, and gene expression profiling from infected tissues, we show that readjustments in hepatic, splenic and renal copper homeostasis accompany disseminated Candida albicans infections in the mouse model. Localized host-imposed copper poisoning manifests itself as a transient increase in copper early in the kidney infection. Changes in renal copper are detected by the fungus, as revealed by gene expression profiling and fungal virulence studies. The fungus responds by differentially regulating the Crp1 copper efflux pump (higher expression during early infection and down-regulation late in infection) and the Ctr1 copper importer (lower expression during early infection, and subsequent up-regulation late in infection) to maintain copper homeostasis during disease progression. Both Crp1 and Ctr1 are required for full fungal virulence. Importantly, copper homeostasis influences other virulence traits-metabolic flexibility and oxidative stress resistance. Our study highlights the importance of copper homeostasis for host defence and fungal virulence during systemic disease. Nutritional immunity is a process whereby an infected host manipulates essential micronutrients to defend against an invading pathogen. We reveal a dynamic aspect of nutritional immunity during infection that involves copper assimilation. Using a combination of laser ablation inductively coupled mass spectrometry (LA-ICP MS) and metal mapping, immunohistochemistry, and gene expression profiling from infected tissues, we show that readjustments in hepatic, splenic and renal copper homeostasis accompany disseminated Candida albicans infections in the mouse model. Localized host-imposed copper poisoning manifests itself as a transient increase in copper early in the kidney infection. Changes in renal copper are detected by the fungus, as revealed by gene expression profiling and fungal virulence studies. The fungus responds by differentially regulating the Crp1 copper efflux pump (higher expression during early infection and down-regulation late in infection) and the Ctr1 copper importer (lower expression during early infection, and subsequent up-regulation late in infection) to maintain copper homeostasis during disease progression. Both Crp1 and Ctr1 are required for full fungal virulence. Importantly, copper homeostasis influences other virulence traits—metabolic flexibility and oxidative stress resistance. Our study highlights the importance of copper homeostasis for host defence and fungal virulence during systemic disease. |
Audience | Academic |
Author | Brown, Alistair J P MacCallum, Donna M Ballou, Elizabeth R Childers, Delma S Urgast, Dagmar S Feldmann, Joerg Mackie, Joanna Szabo, Edina K |
AuthorAffiliation | 2 Trace Element Speciation Laboratory, Department of Chemistry, College of Physical Science, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, United Kingdom Louisiana State University, UNITED STATES 1 Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom |
AuthorAffiliation_xml | – name: 1 Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom – name: Louisiana State University, UNITED STATES – name: 2 Trace Element Speciation Laboratory, Department of Chemistry, College of Physical Science, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, United Kingdom |
Author_xml | – sequence: 1 givenname: Joanna surname: Mackie fullname: Mackie, Joanna organization: Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom – sequence: 2 givenname: Edina K surname: Szabo fullname: Szabo, Edina K organization: Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom – sequence: 3 givenname: Dagmar S surname: Urgast fullname: Urgast, Dagmar S organization: Trace Element Speciation Laboratory, Department of Chemistry, College of Physical Science, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, United Kingdom – sequence: 4 givenname: Elizabeth R surname: Ballou fullname: Ballou, Elizabeth R organization: Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom – sequence: 5 givenname: Delma S surname: Childers fullname: Childers, Delma S organization: Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom – sequence: 6 givenname: Donna M surname: MacCallum fullname: MacCallum, Donna M organization: Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom – sequence: 7 givenname: Joerg surname: Feldmann fullname: Feldmann, Joerg organization: Trace Element Speciation Laboratory, Department of Chemistry, College of Physical Science, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, United Kingdom – sequence: 8 givenname: Alistair J P surname: Brown fullname: Brown, Alistair J P organization: Aberdeen Fungal Group, School of Medicine, Medical Sciences & Nutrition, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, United Kingdom |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27362522$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Biological Sciences, University of Calgary, 507 Campus Drive N.W., Calgary T2N 1N4, AB, Canada Conceived and designed the experiments: JM EKS DSU ERB DSC DMM JF AJPB. Performed the experiments: JM EKS DSU ERB DMM. Analyzed the data: JM EKS DSU ERB DSC DMM JF AJPB. Wrote the paper: JM AJPB. Competing Interests: The authors have declared that no competing interests exist. |
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Snippet | Nutritional immunity is a process whereby an infected host manipulates essential micronutrients to defend against an invading pathogen. We reveal a dynamic... |
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SubjectTerms | Ablation Animals Biology and Life Sciences Candida albicans Candida albicans - genetics Candidiasis - microbiology Carbon Copper Copper - metabolism Copper - poisoning Disease Models, Animal Disease Progression Efflux Fungal Proteins - genetics Fungi Gene expression Gene Expression Profiling Gene Expression Regulation, Fungal Gene mapping Homeostasis Immunity Immunohistochemistry Infections Kidney - metabolism Kidney diseases Kidneys Laboratories Laser ablation Liver - metabolism Mass Spectrometry Mass spectroscopy Medicine Medicine and Health Sciences Metabolism Mice Micronutrients Nutrition Oxidation resistance Oxidative Stress Physical Sciences Poisoning Profiling Research and Analysis Methods Science Spleen Spleen - metabolism Trace elements Virulence Yeast |
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Title | Host-Imposed Copper Poisoning Impacts Fungal Micronutrient Acquisition during Systemic Candida albicans Infections |
URI | https://www.ncbi.nlm.nih.gov/pubmed/27362522 https://www.proquest.com/docview/1800708727 https://search.proquest.com/docview/1808712257 https://pubmed.ncbi.nlm.nih.gov/PMC4928837 https://doaj.org/article/3f91aa938b784876b61d53a7304d1bb3 http://dx.doi.org/10.1371/journal.pone.0158683 |
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