Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells

Leire Aparicio-Fernandez; Aitziber Antoran; Maialen Areitio; Oier Rodriguez-Erenaga; Leire Martin-Souto; Idoia Buldain; Joana Márquez; Aitor Benedicto; Beatriz Arteta; Aize Pellon; David L. Moyes; Aitor Rementeria; Andoni Ramirez-Garcia

doi:10.1016/j.micinf.2024.105305

Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells

Leire Aparicio-Fernandez, Aitziber Antoran^*, Maialen Areitio, Oier Rodriguez-Erenaga, Leire Martin-Souto, Idoia Buldain, Joana Márquez, Aitor Benedicto, Beatriz Arteta, Aize Pellon, David L. Moyes, Aitor Rementeria, Andoni Ramirez-Garcia

^*Corresponding author for this work

Centre for Host Microbiome Interactions

Department of Plant Biology and Ecology University of the Basque Country UPV/EHU Bilbao Spain
Univ Basque Country UPV EHU, University of Basque Country, Dept Biochem & Mol Biol
Saarland University
Centre for Clinical, Oral and Translational Science, Faculty of Dental, Oral and Craniofacial Science, King's College London, United Kingdom.
1Department of Hepatology, Imperial College London, London, UK. 2Institute of Liver Studies at King's College School of Medicine at King's College Hospital, London, UK. 3Institute of Human Health and Performance, University College London, London, UK. 4Department of Asthma Allergy and Lung Biology, King's College London, London, UK. 5Division of Critical Care Medicine, University of Alberta, Edmonton, Canada.

Research output: Contribution to journal › Article › peer-review

4 Citations (Scopus)

Abstract

The liver, and more specifically, the liver sinusoidal endothelial cells, constitute the beginning of one of the most important responses for the elimination of hematogenously disseminated Candida albicans. Therefore, we aimed to study the mechanisms involved in the interaction between these cells and C. albicans. Transcriptomics-based analysis showed an increase in the expression of genes related to the immune response (including receptors, cytokines, and adhesion molecules), as well as to aerobic glycolysis. Further in vitro analyses showed that IL-6 production in response to C. albicans is controlled by MyD88- and SYK-pathways, suggesting an involvement of Toll-like and C-type lectin receptors and the subsequent activation of the MAP-kinases and c-Fos/AP-1 transcription factor. In addition, liver sinusoidal endothelial cells undergo metabolic reprogramming towards aerobic glycolysis induced by C. albicans, as confirmed by the increased Extracellular Acidification Rate and the overexpression of enolase (Eno2), hexonikase (Hk2) and glucose transporter 1 (Slc2a1). In conclusion, these results indicate that the hepatic endothelium responds to C. albicans by increasing aerobic glycolysis and promoting an inflammatory environment.

Original language	English
Article number	105305
Journal	MICROBES AND INFECTION
Volume	26
Issue number	4
Early online date	29 Jan 2024
DOIs	https://doi.org/10.1016/j.micinf.2024.105305
Publication status	Published - 1 May 2024

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10.1016/j.micinf.2024.105305Licence: CC BY-NC-ND

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Aparicio-Fernandez, L., Antoran, A., Areitio, M., Rodriguez-Erenaga, O., Martin-Souto, L., Buldain, I., Márquez, J., Benedicto, A., Arteta, B., Pellon, A., Moyes, D. L., Rementeria, A., & Ramirez-Garcia, A. (2024). Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells. MICROBES AND INFECTION, 26(4), Article 105305. https://doi.org/10.1016/j.micinf.2024.105305

@article{cd0232a4c6ac40e79b50f2bf24a998ba,

title = "Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells",

abstract = "The liver, and more specifically, the liver sinusoidal endothelial cells, constitute the beginning of one of the most important responses for the elimination of hematogenously disseminated Candida albicans. Therefore, we aimed to study the mechanisms involved in the interaction between these cells and C. albicans. Transcriptomics-based analysis showed an increase in the expression of genes related to the immune response (including receptors, cytokines, and adhesion molecules), as well as to aerobic glycolysis. Further in vitro analyses showed that IL-6 production in response to C. albicans is controlled by MyD88- and SYK-pathways, suggesting an involvement of Toll-like and C-type lectin receptors and the subsequent activation of the MAP-kinases and c-Fos/AP-1 transcription factor. In addition, liver sinusoidal endothelial cells undergo metabolic reprogramming towards aerobic glycolysis induced by C. albicans, as confirmed by the increased Extracellular Acidification Rate and the overexpression of enolase (Eno2), hexonikase (Hk2) and glucose transporter 1 (Slc2a1). In conclusion, these results indicate that the hepatic endothelium responds to C. albicans by increasing aerobic glycolysis and promoting an inflammatory environment.",

author = "Leire Aparicio-Fernandez and Aitziber Antoran and Maialen Areitio and Oier Rodriguez-Erenaga and Leire Martin-Souto and Idoia Buldain and Joana M{\'a}rquez and Aitor Benedicto and Beatriz Arteta and Aize Pellon and Moyes, {David L.} and Aitor Rementeria and Andoni Ramirez-Garcia",

note = "Funding Information: The authors thank for technical and human support provided by the Genomics and Proteomics service of SGIker at the University of the Basque Country (UPV/EHU) and PhD Maria del Toro in the Genomics and Bioinformatics platform of the Centro de Investigaci{\'o}n Biom{\'e}dica de la Rioja (CIBIR) (Logro{\~n}o, Spain). This research was funded by the Basque Government, grant numbers IT1362-19 and IT1657-22, and the Spanish Ministry of Science via FECYT, grant number PRECIPITA_PR251. L.M−S and M.A have received a predoctoral grant from the Basque Government and L.A-F from the University of the Basque Country (UPV/EHU). Funding Information: This research was funded by the Basque Government , grant numbers IT1362-19 and IT1657-22, and the Spanish Ministry of Science via FECYT, grant number PRECIPITA_PR251 . L.M−S and M.A have received a predoctoral grant from the Basque Government and L.A-F from the University of the Basque Country (UPV/EHU) . Publisher Copyright: {\textcopyright} 2024 The Authors",

year = "2024",

month = may,

day = "1",

doi = "10.1016/j.micinf.2024.105305",

language = "English",

volume = "26",

journal = "MICROBES AND INFECTION",

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Aparicio-Fernandez, L, Antoran, A, Areitio, M, Rodriguez-Erenaga, O, Martin-Souto, L, Buldain, I, Márquez, J, Benedicto, A, Arteta, B, Pellon, A , Moyes, DL, Rementeria, A & Ramirez-Garcia, A 2024, 'Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells', MICROBES AND INFECTION, vol. 26, no. 4, 105305. https://doi.org/10.1016/j.micinf.2024.105305

TY - JOUR

T1 - Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells

AU - Aparicio-Fernandez, Leire

AU - Antoran, Aitziber

AU - Areitio, Maialen

AU - Rodriguez-Erenaga, Oier

AU - Martin-Souto, Leire

AU - Buldain, Idoia

AU - Márquez, Joana

AU - Benedicto, Aitor

AU - Arteta, Beatriz

AU - Pellon, Aize

AU - Moyes, David L.

AU - Rementeria, Aitor

AU - Ramirez-Garcia, Andoni

N1 - Funding Information: The authors thank for technical and human support provided by the Genomics and Proteomics service of SGIker at the University of the Basque Country (UPV/EHU) and PhD Maria del Toro in the Genomics and Bioinformatics platform of the Centro de Investigación Biomédica de la Rioja (CIBIR) (Logroño, Spain). This research was funded by the Basque Government, grant numbers IT1362-19 and IT1657-22, and the Spanish Ministry of Science via FECYT, grant number PRECIPITA_PR251. L.M−S and M.A have received a predoctoral grant from the Basque Government and L.A-F from the University of the Basque Country (UPV/EHU). Funding Information: This research was funded by the Basque Government , grant numbers IT1362-19 and IT1657-22, and the Spanish Ministry of Science via FECYT, grant number PRECIPITA_PR251 . L.M−S and M.A have received a predoctoral grant from the Basque Government and L.A-F from the University of the Basque Country (UPV/EHU) . Publisher Copyright: © 2024 The Authors

PY - 2024/5/1

Y1 - 2024/5/1

N2 - The liver, and more specifically, the liver sinusoidal endothelial cells, constitute the beginning of one of the most important responses for the elimination of hematogenously disseminated Candida albicans. Therefore, we aimed to study the mechanisms involved in the interaction between these cells and C. albicans. Transcriptomics-based analysis showed an increase in the expression of genes related to the immune response (including receptors, cytokines, and adhesion molecules), as well as to aerobic glycolysis. Further in vitro analyses showed that IL-6 production in response to C. albicans is controlled by MyD88- and SYK-pathways, suggesting an involvement of Toll-like and C-type lectin receptors and the subsequent activation of the MAP-kinases and c-Fos/AP-1 transcription factor. In addition, liver sinusoidal endothelial cells undergo metabolic reprogramming towards aerobic glycolysis induced by C. albicans, as confirmed by the increased Extracellular Acidification Rate and the overexpression of enolase (Eno2), hexonikase (Hk2) and glucose transporter 1 (Slc2a1). In conclusion, these results indicate that the hepatic endothelium responds to C. albicans by increasing aerobic glycolysis and promoting an inflammatory environment.

AB - The liver, and more specifically, the liver sinusoidal endothelial cells, constitute the beginning of one of the most important responses for the elimination of hematogenously disseminated Candida albicans. Therefore, we aimed to study the mechanisms involved in the interaction between these cells and C. albicans. Transcriptomics-based analysis showed an increase in the expression of genes related to the immune response (including receptors, cytokines, and adhesion molecules), as well as to aerobic glycolysis. Further in vitro analyses showed that IL-6 production in response to C. albicans is controlled by MyD88- and SYK-pathways, suggesting an involvement of Toll-like and C-type lectin receptors and the subsequent activation of the MAP-kinases and c-Fos/AP-1 transcription factor. In addition, liver sinusoidal endothelial cells undergo metabolic reprogramming towards aerobic glycolysis induced by C. albicans, as confirmed by the increased Extracellular Acidification Rate and the overexpression of enolase (Eno2), hexonikase (Hk2) and glucose transporter 1 (Slc2a1). In conclusion, these results indicate that the hepatic endothelium responds to C. albicans by increasing aerobic glycolysis and promoting an inflammatory environment.

UR - http://www.scopus.com/inward/record.url?scp=85184762540&partnerID=8YFLogxK

U2 - 10.1016/j.micinf.2024.105305

DO - 10.1016/j.micinf.2024.105305

M3 - Article

C2 - 38296157

SN - 1286-4579

VL - 26

JO - MICROBES AND INFECTION

JF - MICROBES AND INFECTION

IS - 4

M1 - 105305

ER -

Candida albicans increases the aerobic glycolysis and activates MAPK-dependent inflammatory response of liver sinusoidal endothelial cells

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