Immunometabolism: new insights and lessons from antigen-directed cellular immune responses

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Abstract

Modulation of immune responses by nutrients is an important area of study in cellular biology and clinical sciences in the context of cancer therapies and anti-pathogen-directed immune responses in health and disease. We review metabolic pathways that influence immune cell function and cellular persistence in chronic infections. We also highlight the role of nutrients in altering the tissue microenvironment with lessons from the tumor microenvironment that shapes the quality and quantity of cellular immune responses. Multiple layers of biological networks, including the nature of nutritional supplements, the genetic background, previous exposures, and gut microbiota status have impact on cellular performance and immune competence against molecularly defined targets. We discuss how immune metabolism determines the differentiation pathway of antigen-specific immune cells and how these insights can be explored to devise better strategies to strengthen anti-pathogen-directed immune responses, while curbing unwanted, non-productive inflammation.

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Alan Saltiel, Shannon Reilly (2017)

Adipose tissue inflammation is an adaptive response to overnutrition in the early stages of obesity, but later becomes maladaptive. Here, Reilly and Saltiel review the cellular and molecular mechanisms of obesity-induced inflammation in adipose tissue and discuss potential therapeutic approaches.

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Cancer cachexia: mediators, signaling, and metabolic pathways.

Kenneth C.H. Fearon, David J. Glass, Denis C. Guttridge (2012)

Cancer cachexia is characterized by a significant reduction in body weight resulting predominantly from loss of adipose tissue and skeletal muscle. Cachexia causes reduced cancer treatment tolerance and reduced quality and length of life, and remains an unmet medical need. Therapeutic progress has been impeded, in part, by the marked heterogeneity of mediators, signaling, and metabolic pathways both within and between model systems and the clinical syndrome. Recent progress in understanding conserved, molecular mechanisms of skeletal muscle atrophy/hypertrophy has provided a downstream platform for circumventing the variations and redundancy in upstream mediators and may ultimately translate into new targeted therapies. Copyright © 2012 Elsevier Inc. All rights reserved.

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Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages.

Eva M. Pålsson-McDermott, Anne M Curtis, Gautam Goel … (2015)

Macrophages activated by the TLR4 agonist LPS undergo dramatic changes in their metabolic activity. We here show that LPS induces expression of the key metabolic regulator Pyruvate Kinase M2 (PKM2). Activation of PKM2 using two well-characterized small molecules, DASA-58 and TEPP-46, inhibited LPS-induced Hif-1α and IL-1β, as well as the expression of a range of other Hif-1α-dependent genes. Activation of PKM2 attenuated an LPS-induced proinflammatory M1 macrophage phenotype while promoting traits typical of an M2 macrophage. We show that LPS-induced PKM2 enters into a complex with Hif-1α, which can directly bind to the IL-1β promoter, an event that is inhibited by activation of PKM2. Both compounds inhibited LPS-induced glycolytic reprogramming and succinate production. Finally, activation of PKM2 by TEPP-46 in vivo inhibited LPS and Salmonella typhimurium-induced IL-1β production, while boosting production of IL-10. PKM2 is therefore a critical determinant of macrophage activation by LPS, promoting the inflammatory response.

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Author and article information

Contributors

Markus Maeurer: markus.maeurer@fundacaochampalimaud.pt

Journal

Journal ID (nlm-ta): Semin Immunopathol

Journal ID (iso-abbrev): Semin Immunopathol

Title: Seminars in Immunopathology

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 1863-2297

ISSN (Electronic): 1863-2300

Publication date (Electronic): 9 June 2020

Pages: 1-35

Affiliations

[1 ]Centro de Investigação Interdisciplinar Egas Moniz (CiiEM, U4585 FCT), Applied Nutrition Studies Group G.E.N.A.-IUEM), Instituto Universitário Egas Moniz, Egas Moniz Higher Education School, Monte de Caparica, Portugal

[2 ]GRID grid.421010.6, ISNI 0000 0004 0453 9636, ImmunoSurgery Unit, , Champalimaud Centre for the Unknown, ; Lisbon, Portugal

[3 ]GRID grid.488137.1, ISNI 0000 0001 2267 2324, Treatment and Research Center for Infectious Diseases, The Fifth Medical Center of PLA General Hospital, , National Clinical Research Center for Infectious Diseases, ; Beijing, China

[4 ]INMI L. Spallanzani, Rome, Italy

[5 ]GRID grid.52996.31, ISNI 0000 0000 8937 2257, Division of Infection and Immunity, University College London and NIHR Biomedical Research Centre, , UCL Hospitals NHS Foundation Trust, ; London, UK

[6 ]GRID grid.5802.f, ISNI 0000 0001 1941 7111, I Medizinische Klinik, , Johannes Gutenberg University Mainz, ; Mainz, Germany

Author notes

This article is a contribution to the special issue on: Immunopathology of unresolved tropical diseases - Guest Editor: Marcel Tanner

Article

Publisher ID: 798

DOI: 10.1007/s00281-020-00798-w

PMC ID: 7282544

PubMed ID: 32519148

SO-VID: 6a4eff62-fff4-4175-9ea4-b3b0a595873d

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This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

Immunometabolism: new insights and lessons from antigen-directed cellular immune responses

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Abstract

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Point-Of-Care Testing for Tuberculosis

Most cited references 284

Adapting to obesity with adipose tissue inflammation

Cancer cachexia: mediators, signaling, and metabolic pathways.

Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the warburg effect in LPS-activated macrophages.

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