Adan Chari Jirmo

Melanie Albrecht

Miguel Angel Alejandre Alcazar

Slaven Crnkovic

Frontiers in Immunology

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Frontiers in ImmunologyOPEN ACCESSEDITED AND REVIEWED BYPietro Ghezzi,University of Urbino Carlo Bo, Italy*CORRESPONDENCEAdan Chari JirmoJirmo.adan@mh-hannover.deMelanie Albrechtmelanie.albrecht@pei.deSlaven CrnkovicSlaven.Crnkovic@lvr.lbg.ac.atMiguel Angel Alejandre Alcazarmiguel.alejandre-alcazar@uk-koeln.deRECEIVED 07 December 2023ACCEPTED 13 December 2023PUBLISHED 17 January 2024CITATIONJirmo AC, Albrecht M, Crnkovic S andAlejandre Alcazar MA (2024) Editorial: Cellularand systemic interplay of metabolism andinflammation in the pathogenesis oflung diseases.Front. Immunol. 14:1352304.doi: 10.3389/fimmu.2023.1352304COPYRIGHT© 2024 Jirmo, Albrecht, Crnkovic andAlejandre Alcazar. This is an open-accessarticle distributed under the terms of theCreative Commons Attribution License (CC BY).The use, distribution or reproduction in otherforums is permitted, provided the originalauthor(s) and the copyright owner(s) arecredited and that the original publication inthis journal is cited, in accordance withaccepted academic practice. No use,distribution or reproduction is permittedwhich does not comply with these terms.TYPE EditorialPUBLISHED 17 January 2024DOI 10.3389/fimmu.2023.1352304Editorial: Cellular and systemicinterplay of metabolism andinflammation in the pathogenesisof lung diseasesAdan Chari Jirmo1,2*, Melanie Albrecht3*, Slaven Crnkovic4*and Miguel Angel Alejandre Alcazar5,6,7*1Department of Pediatric Pneumology, Allergology and Neonatology, Hannover MedicalSchool, Hannover, Germany, 2German Center for Lung Research (DZL), Hannover, Germany, 3Paul-Ehrlich Institute (PEI), Langen, Germany, 4Ludwig Boltzmann Institute (LBI) for Lung and VascularResearch, Otto Loewi Research Center Medical University of Graz, Graz, Austria, 5Department ofPediatric and Adolescent Medicine, Faculty of Medicine and University Hospital Cologne, University ofCologne, Cologne, Germany, 6Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD) and Center for Molecular Medicine Cologne (CMMC), Faculty ofMedicine and University Hospital Cologne, University of Cologne, Cologne, Germany, 7GermanCenter for Lung Research (DZL), Institute for Lung Health (ILH), University of Giessen and MarburgLung Center (UGMLC) and Cardiopulmonary Institute (CPI), Marburg, GermanyKEYWORDSmetabolism, metaflammation, inflammation, immuno-metabolism, lung pathologiesEditorial on the Research TopicCellular and systemic interplay of metabolism and inflammation in thepathogenesis of lung diseasesResearch in the last couple of years has generated ample evidence showing that cellularalterations of the metabolic machinery could be the underlying factor in multiple humandiseases. In this Research Topic, we have gathered scientific articles to underpin theinterplay between perturbed metabolism/triggering of inflammation that contributes topulmonary pathologies.In this Research Topic, Wang et al., through a literature review, clearly illustrate theimpact of various metabolic processes such as glycolysis, OXPHOS, FAO, and glutaminemetabolism in modulating phenotypic and functional changes in macrophages and howthese changes affect acute lung injury or acute respiratory distress syndrome. Moreover,through this review, Wang et al. reveal that metabolic reprogramming of macrophages isaccompanied by dramatic shifts in cell metabolism and that functional state-associatedunique metabolic signatures can be identified in various macrophage populations. Tanget al. have gone further in an original study to show that alveolar macrophages (AM)sensing of amino acid phenylalanine promotes pyroptosis, which causes the release ofinflammatory mediators and, thereby, exacerbates lung inflammation and acute respiratorydistress syndrome (ARDS) lethality in a murine model. This study is especially interestingsince it not only elucidates the entire process of how phenylalanine initiates pyroptosis inAMs and the resulting inflammation but also elucidates the subsequent effects of theinhibition of this process on ARDS. The article clearly shows the significance of small-molecule metabolites in pulmonary inflammation and how they may be useful not only asfrontiersin.org01Jirmo et al. 10.3389/fimmu.2023.1352304biomarkers but as potential therapeutic targets. In their work, Liet al. expand this Research Topic further by showing how sensitivityto ferroptosis influences the inflammatory and lung repaircapabilities of macrophages. They demonstrate that in chronicobstructive pulmonary disease (COPD), lipid peroxidation favorsthe differentiation of AM toward ferroptosis-sensitive M2-likemacrophages but not ferroptotic-resistant M1-like macrophages.The Ferroptotic M2-like AMs lose their anti-inflammatory andrepair functions but continue invoking inflammatory responses inCOPD. Due to persistent lipid peroxidation in a COPD lung, thispolarization toward M2-like AMs is speculated to be the cause ofconsistent inflammation and tissue damage. Importantly, the studyshows that this process is therapeutically targetable since theferroptotic phenotype can be ameliorated with anti-ferroptoticcompounds, iron chelators, and heme oxygenase (HO-1)inhibitors and thereby alleviate lung inflammation, destruction,and remodeling of COPD.More evidence of the impact of metabolic distortion on cellularhomeostasis and how it influences lung pathology was provided byBauer et al. They report that in severe cases of coronavirus disease-2019(COVID-19), hypoxia-sensitized toll-like receptor 4 (TLR4) signalingactivates SARS-CoV-2 spike protein in monocytes, ultimately leadingto systemic inflammation in severe cases of COVID-19 as a result ofenhanced chemokine ISG expression inmonocytes upon infection withSARS-CoV-2. The study by Bauer et al. shows the connection betweenhypoxia-evoked disturbances in cholesterol metabolism and alteredinterferon (IFN) responses in monocytes and how this concomitantlyaffects inflammatory responses in the lung. Furthermore, the studyprovides an explanation regarding the possible mechanism of systemicinflammation which has been observed in severe cases of COVID-19infections. In addition, Hasankhani et al. show in their review thatmetabolic perturbances are an underlying factor in the induction of theSARS-CoV-2-associated cytokine storm which is the main COVID-associated immunopathology that is related to disease severityand mortality.Finally, Lim and Templeton in their mini-review highlight theimportant immunomodulatory function of hormones on theexample of Adipokines exemplified through Adiponectin (APN).They speculate possible roles and mechanisms of AdiponectinFrontiers in Immunology 02(APN) pathway-induced protection in lung diseases, includingfungal, bacterial, and viral infection, which could result in noveltherapies that protect against infection, excessive inflammation,and other lung pathologies. This closes the potential circle andprovides “food for thought” on how potentially feeding behaviorand accompanying disturbances in hormones that regulatemetabolism might influence or be exploited in the managementof lung inflammatory conditions. Thus, with this Research Topic onCellular and Systemic Interplay of Metabolism and Inflammation inthe Pathogenesis of Lung Diseases, we provide an overview thoughnot exhaustive of how metaflammation influences pulmonaryimmunity and pathologies and the need for intensification ofresearch in this area.Author contributionsAJ: Conceptualization, Writing – original draft, Writing – review& editing. MA: Conceptualization,Writing – original draft, Writing –review & editing. SC: Conceptualization, Writing – original draft,Writing – review & editing. MA: Conceptualization, Writing –original draft, Writing – review & editing.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.Publisher’s noteAll claims expressed in this article are solely those of theauthors and do not necessarily represent those of their affiliatedorganizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.frontiersin.org

Editorial: Cellular and systemic interplay of metabolism and inflammation in the pathogenesis of lung diseases

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Editorial: Cellular and systemic interplay of metabolism and inflammation in the pathogenesis of lung diseases

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