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Metabolic pathways in immune senescence and inflammaging : Novel therapeutic strategy for chronic inflammatory lung diseases. An EAACI position paper from the Task Force for Immunopharmacology

Roth-Walter, F. ; Adcock, I. M. ; Benito-Villalvilla, C. ; Bianchini, R. ; Bjermer, L. LU ; Caramori, G. ; Cari, L. ; Chung, K. F. ; Diamant, Z. LU and Eguiluz-Gracia, I. , et al. (2023) In Allergy: European Journal of Allergy and Clinical Immunology
Abstract

The accumulation of senescent cells drives inflammaging and increases morbidity of chronic inflammatory lung diseases. Immune responses are built upon dynamic changes in cell metabolism that supply energy and substrates for cell proliferation, differentiation, and activation. Metabolic changes imposed by environmental stress and inflammation on immune cells and tissue microenvironment are thus chiefly involved in the pathophysiology of allergic and other immune-driven diseases. Altered cell metabolism is also a hallmark of cell senescence, a condition characterized by loss of proliferative activity in cells that remain metabolically active. Accelerated senescence can be triggered by acute or chronic stress and inflammatory responses. In... (More)

The accumulation of senescent cells drives inflammaging and increases morbidity of chronic inflammatory lung diseases. Immune responses are built upon dynamic changes in cell metabolism that supply energy and substrates for cell proliferation, differentiation, and activation. Metabolic changes imposed by environmental stress and inflammation on immune cells and tissue microenvironment are thus chiefly involved in the pathophysiology of allergic and other immune-driven diseases. Altered cell metabolism is also a hallmark of cell senescence, a condition characterized by loss of proliferative activity in cells that remain metabolically active. Accelerated senescence can be triggered by acute or chronic stress and inflammatory responses. In contrast, replicative senescence occurs as part of the physiological aging process and has protective roles in cancer surveillance and wound healing. Importantly, cell senescence can also change or hamper response to diverse therapeutic treatments. Understanding the metabolic pathways of senescence in immune and structural cells is therefore critical to detect, prevent, or revert detrimental aspects of senescence-related immunopathology, by developing specific diagnostics and targeted therapies. In this paper, we review the main changes and metabolic alterations occurring in senescent immune cells (macrophages, B cells, T cells). Subsequently, we present the metabolic footprints described in translational studies in patients with chronic asthma and chronic obstructive pulmonary disease (COPD), and review the ongoing preclinical studies and clinical trials of therapeutic approaches aiming at targeting metabolic pathways to antagonize pathological senescence. Because this is a recently emerging field in allergy and clinical immunology, a better understanding of the metabolic profile of the complex landscape of cell senescence is needed. The progress achieved so far is already providing opportunities for new therapies, as well as for strategies aimed at disease prevention and supporting healthy aging.

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organization
publishing date
type
Contribution to journal
publication status
epub
subject
keywords
cell metabolism, immune senescence, immunometabolism, inflammaging, senolytic drugs, senomorphic drugs
in
Allergy: European Journal of Allergy and Clinical Immunology
publisher
Wiley-Blackwell
external identifiers
  • pmid:38108546
  • scopus:85180002830
ISSN
0105-4538
DOI
10.1111/all.15977
language
English
LU publication?
yes
id
b13b6a65-d08d-42ad-9a25-b46096402b36
date added to LUP
2024-01-10 14:35:06
date last changed
2024-04-25 10:34:32
@article{b13b6a65-d08d-42ad-9a25-b46096402b36,
  abstract     = {{<p>The accumulation of senescent cells drives inflammaging and increases morbidity of chronic inflammatory lung diseases. Immune responses are built upon dynamic changes in cell metabolism that supply energy and substrates for cell proliferation, differentiation, and activation. Metabolic changes imposed by environmental stress and inflammation on immune cells and tissue microenvironment are thus chiefly involved in the pathophysiology of allergic and other immune-driven diseases. Altered cell metabolism is also a hallmark of cell senescence, a condition characterized by loss of proliferative activity in cells that remain metabolically active. Accelerated senescence can be triggered by acute or chronic stress and inflammatory responses. In contrast, replicative senescence occurs as part of the physiological aging process and has protective roles in cancer surveillance and wound healing. Importantly, cell senescence can also change or hamper response to diverse therapeutic treatments. Understanding the metabolic pathways of senescence in immune and structural cells is therefore critical to detect, prevent, or revert detrimental aspects of senescence-related immunopathology, by developing specific diagnostics and targeted therapies. In this paper, we review the main changes and metabolic alterations occurring in senescent immune cells (macrophages, B cells, T cells). Subsequently, we present the metabolic footprints described in translational studies in patients with chronic asthma and chronic obstructive pulmonary disease (COPD), and review the ongoing preclinical studies and clinical trials of therapeutic approaches aiming at targeting metabolic pathways to antagonize pathological senescence. Because this is a recently emerging field in allergy and clinical immunology, a better understanding of the metabolic profile of the complex landscape of cell senescence is needed. The progress achieved so far is already providing opportunities for new therapies, as well as for strategies aimed at disease prevention and supporting healthy aging.</p>}},
  author       = {{Roth-Walter, F. and Adcock, I. M. and Benito-Villalvilla, C. and Bianchini, R. and Bjermer, L. and Caramori, G. and Cari, L. and Chung, K. F. and Diamant, Z. and Eguiluz-Gracia, I. and Knol, E. F. and Jesenak, M. and Levi-Schaffer, F. and Nocentini, G. and O'Mahony, L. and Palomares, O. and Redegeld, F. and Sokolowska, M. and Van Esch, B. C.A.M. and Stellato, C.}},
  issn         = {{0105-4538}},
  keywords     = {{cell metabolism; immune senescence; immunometabolism; inflammaging; senolytic drugs; senomorphic drugs}},
  language     = {{eng}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Allergy: European Journal of Allergy and Clinical Immunology}},
  title        = {{Metabolic pathways in immune senescence and inflammaging : Novel therapeutic strategy for chronic inflammatory lung diseases. An EAACI position paper from the Task Force for Immunopharmacology}},
  url          = {{http://dx.doi.org/10.1111/all.15977}},
  doi          = {{10.1111/all.15977}},
  year         = {{2023}},
}