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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| description | 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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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0158683</identifier><identifier>PMID: 27362522</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>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</subject><ispartof>PloS one, 2016-06, Vol.11 (6), p.e0158683</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Mackie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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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.</description><subject>Ablation</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Candida albicans</subject><subject>Candida albicans - genetics</subject><subject>Candidiasis - microbiology</subject><subject>Carbon</subject><subject>Copper</subject><subject>Copper - metabolism</subject><subject>Copper - poisoning</subject><subject>Disease Models, Animal</subject><subject>Disease Progression</subject><subject>Efflux</subject><subject>Fungal Proteins - genetics</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Gene mapping</subject><subject>Homeostasis</subject><subject>Immunity</subject><subject>Immunohistochemistry</subject><subject>Infections</subject><subject>Kidney - metabolism</subject><subject>Kidney diseases</subject><subject>Kidneys</subject><subject>Laboratories</subject><subject>Laser ablation</subject><subject>Liver - metabolism</subject><subject>Mass Spectrometry</subject><subject>Mass spectroscopy</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Micronutrients</subject><subject>Nutrition</subject><subject>Oxidation resistance</subject><subject>Oxidative Stress</subject><subject>Physical Sciences</subject><subject>Poisoning</subject><subject>Profiling</subject><subject>Research and Analysis Methods</subject><subject>Science</subject><subject>Spleen</subject><subject>Spleen - metabolism</subject><subject>Trace elements</subject><subject>Virulence</subject><subject>Yeast</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9Fu0zAUhiMEYqPwBggiISG4aIntxHZuJlUVY5WGhtjErWU7dusptTPbQeztcdpsatAuiC-S2N_5bf_nnCx7C4oFQAR8uXW9t7xddM6qRQEqiil6lp2CGsE5hgV6fvR9kr0K4bYoKkQxfpmdQIIwrCA8zfyFC3G-3nUuqCZfua5TPv_hTHDW2E2eFriMIT_v7Ya3-XcjvbN99EbZmC_lXW-CicbZvOn9wF_fh6h2RuYrbhvT8Jy3wkhuQ762WskBDa-zF5q3Qb0Z37Ps5vzrzepifnn1bb1aXs4lgVWcw1rgspKSNLLGigiU_gUEMj0UcwW0oBxqIAXGiDa10lRTWiHFAdRacDTL3h9ku9YFNroVGKBFQQpKkgWzbH0gGsdvWefNjvt75rhh-wnnN4z7aGSrGNI14LxGVBBaUoIFBk2FOEFF2QAhUNI6G3frxU41MvnjeTsRna5Ys2Ub95uVNaQUDYf5NAp4d9erENnOBKnallvl-v25KQEQVgP64R_06duNVEqcYsZql_aVgyhblgQUoAaEJmrxBJVGM6QxlZY2aX4S8HkSkJio_sQN70Ng6-uf_89e_ZqyH4_YreJt3AbX9vuSmYLlAUylGIJX-tFkULChMx7cYENnsLEzUti74wQ9Bj20AvoLhaALAQ</recordid><startdate>20160630</startdate><enddate>20160630</enddate><creator>Mackie, Joanna</creator><creator>Szabo, Edina K</creator><creator>Urgast, Dagmar S</creator><creator>Ballou, Elizabeth R</creator><creator>Childers, Delma S</creator><creator>MacCallum, Donna M</creator><creator>Feldmann, Joerg</creator><creator>Brown, Alistair J P</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160630</creationdate><title>Host-Imposed Copper Poisoning Impacts Fungal Micronutrient Acquisition during Systemic Candida albicans Infections</title><author>Mackie, Joanna ; Szabo, Edina K ; Urgast, Dagmar S ; Ballou, Elizabeth R ; Childers, Delma S ; MacCallum, Donna M ; Feldmann, Joerg ; Brown, Alistair J P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c725t-29b645cc7dc96e7b39b6b21cccc86ae1fb8a2f1cb6638d9ef8f8853ea12ffba3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Ablation</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Candida albicans</topic><topic>Candida albicans - 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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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27362522</pmid><doi>10.1371/journal.pone.0158683</doi><tpages>e0158683</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 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 |
| title | Host-Imposed Copper Poisoning Impacts Fungal Micronutrient Acquisition during Systemic Candida albicans Infections |
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