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Interplay between the immune system and adipose tissue in obesity
Open accessAbstract
Obesity is a major risk factor for metabolic disease, with white adipose tissue (WAT) inflammation emerging as a key underlying pathology. Alongside its major role in energy storage, WAT is an important endocrine organ, producing many bioactive molecules, termed adipokines, which not only serve as regulators of systemic metabolism, but also possess immunoregulatory properties. Furthermore, WAT contains a unique immune cell repertoire, including an accumulation of leukocytes that are rare in other locations. These include alternatively activated macrophages, invariant natural killer T cells, and regulatory T cells. Disruption of resident adipose leukocyte homeostasis contributes to obesity-associated inflammation and consequent metabolic disorder. Despite many recent advances in this new field of immuno-metabolism, fundamental questions of why and how inflammation arises as obesity develops are not yet fully understood. Exploring the distinct immune system of adipose tissue is fundamental to our understanding of the endocrine as well as immune systems. In this review, we discuss the roles of adipose tissue leukocytes in the transition to obesity and progression of inflammation and highlight potential anti-inflammatory therapies for combating obesity-related pathology.
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“Obesity promotes inflammatory pathways in visceral fat through adipocyte hypertrophy and hyperplasia and the accumulation of immune cells including macrophages, mast cells, and T lymphocytes producing pro-inflammatory cytokines (148–150).”
From Health Consequences of Sarcopenic Obesity: A Narrative Review (2020) · cites this paper as [149]
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Juçara pulp supplementation improves glucose tolerance in mice
Oyama, L. M., da Silva, F. P., Carnier, J., de Miranda, D. A., Santamarina, A. B., Ribeiro, E. B., do Nascimento, C. M. O., & de Rosso, V. V. (2016) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-015-0122-4 · Cited by 37
Das, S., Mukhuty, A., Mullen, G. P., & Rudolph, M. C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126681 · Cited by 43
Kouidhi, S., Noman, M. Z., Kiéda, C., Elgaaïed, A. B., & Chouaïb, S. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00114 · Cited by 39
“The second group comprises anti-inflammatory cells [M2 macrophages, regulatory CD4 T cells (Tregs), Th2 CD4 T cells, eosinophils, Group 2 innate lymphoid cells (ILC2s), invariant natural killer T (iNKT) cells], which produce IL-10, IL-4, or IL-13, and drive Th2 response (15, 95).”
BackgroundA vicious circle in chronic lymphoedema pathophysiology? An adipocentric view
Cucchi, F., Rossmeislová, L., Simonsen, L., Jensen, M. R., & Bülow, J. (2017) · Obesity Reviews · doi:10.1111/obr.12565 · Cited by 37
“In obesity, hypertrophy of adipocytes results in their metabolic and subsequently immunological dysfunction (38,39) that is probably initiated by increased metabolite processing connected with higher reactive oxygen species production and chronic endoplasmic reticulum stress or by hypoxia (14,28,38,40).”
BackgroundMuscle-dependent regulation of adipose tissue function in long-lived growth hormone-mutant mice
Li, X., Frazier, J., Spahiu, E., McPherson, M., & Miller, R. A. (2020) · Aging · doi:10.18632/aging.103380 · Cited by 34
“Adipose tissue also plays an important role as an immuno-regulatory organ, influencing the activity of macrophages, T cells, B cells, mast cells, dendritic cells and neutrophils [24].”
Backgroundvan Eijkeren, R. J., Krabbe, O., Boes, M. L., Schipper, H. S., & Kalkhoven, E. (2017) · Immunology · doi:10.1111/imm.12839 · Cited by 35
Kim, J., Shin, S., & Kwon, E. (2023) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202200729 · Cited by 36
Cardiovascular disease predictors and adipose tissue macrophage polarization: Is there a link?
Lesná, I. K., Petráš, M., Čejková, S., Králová, A., Froněk, J., Janoušek, L., Thieme, F., Tyll, T., & Poledne, R. (2017) · European Journal of Preventive Cardiology · doi:10.1177/2047487317743355 · Cited by 34
Role of Circadian Transcription Factor Rev-Erb in Metabolism and Tissue Fibrosis
Raza, G. S., Sodum, N., Kaya, Y., & Herzig, K. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232112954 · Cited by 35
The association of non-alcoholic fatty liver disease and atrial fibrillation: a review
Käräjämäki, A. J., Hukkanen, J., & Ukkola, O. H. (2018) · Annals of Medicine · doi:10.1080/07853890.2018.1492147 · Cited by 33
Crosstalk between macrophages and innate lymphoid cells (ILCs) in diseases
Yin, G., Zhao, C., & Pei, W. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108937 · Cited by 33
Muscogiuri, G., Bettini, S., Boschetti, M., Barrea, L., Savastano, S., & Colao, A. (2022) · International Journal of Obesity · doi:10.1038/s41366-022-01111-5 · Cited by 33
“resulting in impaired immune response, defective chemotaxis, and deregulated immune cell differentiation [18].”
BackgroundLesná, I. K., Čejková, S., Králová, A., Froněk, J., Petráš, M., Sekerková, A., Thieme, F., Janoušek, L., & Poledne, R. (2017) · Nutrition and Diabetes · doi:10.1038/nutd.2017.15 · Cited by 30
Pecoraro, A., Nigro, E., Polito, R., Monaco, M. L., Scudiero, O., Mormile, I., Marcelli, A. C., Capasso, M., Habetswallner, F., Genovese, A., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00895 · Cited by 29
Do flavanols-rich natural products relieve obesity-related insulin resistance?
Engin, A. B., Tsatsakis, A. M., Tsoukalas, D., & Engin, A. (2017) · Food and Chemical Toxicology · doi:10.1016/j.fct.2017.12.055 · Cited by 30
“Impairment in the local leukocyte homeostasis takes part in the obesity-related inflammation and associated metabolic disorders (Exley et al., 2014).”
BackgroundAdipocytes harbor a glucosylceramide biosynthesis pathway involved in iNKT cell activation
Rakhshandehroo, M., van Eijkeren, R. J., Gabriel, T. L., de Haar, C. G., Gijzel, S. M. W., Hamers, N., Ferraz, M. J., Aerts, J. M. F. G., Schipper, H. S., van Eijk, M., et al. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2019.04.016 · Cited by 29
“Adipose tissue (AT), a site where the immune system and metabolic pathways intersect, undergoes marked changes during the progression of obesity [1,2].”
BackgroundSbierski‐Kind, J., Mai, K., Kath, J., Jurisch, A., Streitz, M., Kuchenbecker, L., Babel, N., Nienen, M., Jürchott, K., Spranger, L., et al. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000108 · Cited by 28
“mia, elevated triglycerides, and free fatty acids, seems to alter components of the immune system (9, 10).”
BackgroundT cell phenotypes associated with insulin resistance: results from the Berlin Aging Study II
Sbierski‐Kind, J., Goldeck, D., Buchmann, N., Spranger, J., Volk, H., Steinhagen‐Thiessen, E., Pawelec, G., Demuth, I., & Spira, D. (2020) · Immunity & Ageing · doi:10.1186/s12979-020-00211-y · Cited by 27
Inflammation and oxidative stress, the links between obesity and COVID-19: a narrative review
Moreno‐Fernández, J., Ochoa, J. J., Ojeda, M. L., Nogales, F., Carreras, O., & Díaz‐Castro, J. (2022) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-022-00887-4 · Cited by 32
“Lymphocytes present in AT could be the orchestrators of the inflammatory response of this tissue [26].”
BackgroundNutrient and immune sensing are obligate pathways in metabolism, immunity, and disease
Iyer, A., Brown, L., Whitehead, J. P., Prins, J. B., & Fairlie, D. P. (2015) · The FASEB Journal · doi:10.1096/fj.15-271155 · Cited by 25
“Inflammation is normally defined as an acute physiologic response to infection or injury, involving coordination of many complex signals in distinct cells and organ systems to identify and eliminate the source of infection and to repair tissue injury (6).”
BackgroundKyung, D. S., Sung, H., Kim, Y. J., Kim, K., Cho, S. Y., Choi, J., Lee, Y.-H., Kim, I. Y., & Seong, J. K. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.297 · Cited by 26
de Sant’Ana, L. P., Ribeiro, D. J. S., Martins, A. M. A., dos Santos, F. N., Corrêa, R., Almeida, R. D. N., Eberlin, M. N., Maurice, C. F., & Magalhães, K. G. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02926 · Cited by 26
“The characteristic inflammatory status in obesity triggers the release of pro-inflammatory cytokines, chemokines, and proinflammatory fatty acids (10).”
BackgroundSatoh, M., & Iwabuchi, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01314 · Cited by 26
“1+TCRβ+ population in AT was activated upon consumption of an HFD and contained more CD8+ but fewer CD4−CD8− subsets in Jα18 KO (referred here after as Jα281 KO) (25) mice, which differed from observations in either WT or CD1d KO mice; (2) WT mice harbored more noniNKT (=vNKT) cells in AT; and (3) hepatic mononuclea…”
BackgroundResultGermain, N., Viltart, O., Loyens, A., Bruchet, C., Nadin, K., Wolowczuk, I., Estour, B., & Galusca, B. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161890 · Cited by 26
“This result can be added within the complex immuno-metabolic profile characterizing obesity [38].”
Backgroundn-3 PUFA and obesity: from peripheral tissues to the central nervous system
de Mello, A. H., Uberti, M. F., de Farias, B. X., de Souza, N. A. R., & Rezin, G. T. (2018) · British Journal Of Nutrition · doi:10.1017/s0007114518000429 · Cited by 26
“This tissue produces many bioactive molecules, such as cytokines (when secreted by adipose tissue, the cytokines can be called adipokines or adipocytokines), which not only serve as regulators of systemic metabolism but also have immunoregulatory properties((3,56,57)).”
BackgroundRole of NKT cells in cancer immunotherapy—from bench to bed
Bayatipoor, H., Mehdizadeh, S., Jafarpour, R., Shojaei, Z., Pashangzadeh, S., & Motallebnezhad, M. (2022) · Medical Oncology · doi:10.1007/s12032-022-01888-5 · Cited by 24
“This subset secretes anti-inflammatory cytokines like IL-10 and does not have Plzf, unlike other mature iNKT cells [64, 65].”
BackgroundLatteri, S., Sofia, M., Puleo, S., Vincenzo, A. D., Cinti, S., & Castorina, S. (2023) · Langenbeck s Archives of Surgery · doi:10.1007/s00423-023-02821-8 · Cited by 25
“WAT, producing adipokines, growth factors, enzymes and active immune cells such as macrophages and T cells, takes part in the progression of inflammation in obesity [35].”
BackgroundBeckmann, P. J., & Largaespada, D. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031172 · Cited by 24
“Adipose tissue also hosts many immune cells which are significantly altered in the context of obesity [156,157].”
BackgroundAdipose tissue macrophage heterogeneity in the single-cell genomics era
Kang, H., & Lee, J. (2024) · Molecules and Cells · doi:10.1016/j.mocell.2024.100031 · Cited by 25
Willemsen, A. C. H., Moor, N. D., Dessel, J. V., Baijens, L. W. J., Bila, M., Hauben, E. I., van den Hout, M. F. C. M., Poorten, V. V., Hoeben, A., Clément, P. M., et al. (2022) · Cancer Medicine · doi:10.1002/cam4.5522 · Cited by 22
“First line palliative systemic therapy 40 (41) 28 (44) 12 (35) 0.”
Background
Metadata
- Authors
- Exley, M. A., Hand, L., O'Shea, D., & Lynch, L.
- Affiliations
- University College Dublin (IE)
- Venue
- Journal of Endocrinology
- Publisher
- Bioscientifica
- Published
- 2014-09-16
- Volume
- 223
- Issue
- 2
- Pages
- R41-R48
- ISSN
- 0022-0795 (ISSN-L)
- 1479-6805
- OpenAlex
- W2145456795
- Cited by
- 242
- References
- 66
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 12 · 2023: 26 · 2022: 25 · 2021: 20 · 2020: 24 · 2019: 18 · 2018: 20 · 2017: 22 · 2016: 24 · 2015: 35
- FWCI
- 3.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- Funders
- National Cancer Institute (P01CA017094, CA017094)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- obesity, white adipose tissue, adipose tissue inflammation, adipokines, M2 macrophages, invariant natural killer T cells, regulatory T cells, metabolic disorders, anti-inflammatory therapy
- MeSH terms
- Adipose Tissue, Animals, Eosinophils, Humans, Immune System, Inflammation, Lymphocytes, Macrophages, Obesity
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