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Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue
Open accessAbstract
Obesity elicits an immune response characterized by myeloid cell recruitment to key metabolic organs, including adipose tissue. However, the response of immune cells to nonpathologic metabolic stimuli has been less well studied, and the factors that regulate the metabolic-dependent accumulation of immune cells are incompletely understood. Here we characterized the response of adipose tissue macrophages (ATMs) to weight loss and fasting in mice and identified a role for lipolysis in ATM recruitment and accumulation. We found that the immune response to weight loss was dynamic; caloric restriction of high-fat diet-fed mice led to an initial increase in ATM recruitment, whereas ATM content decreased following an extended period of weight loss. The peak in ATM number coincided with the peak in the circulating concentrations of FFA and adipose tissue lipolysis, suggesting that lipolysis drives ATM accumulation. Indeed, fasting or pharmacologically induced lipolysis rapidly increased ATM accumulation, adipose tissue chemoattractant activity, and lipid uptake by ATMs. Conversely, dietary and genetic manipulations that reduced lipolysis decreased ATM accumulation. Depletion of macrophages in adipose tissue cultures increased expression of adipose triglyceride lipase and genes regulated by FFA, and increased lipolysis. These data suggest that local lipid fluxes are central regulators of ATM recruitment and that once recruited, ATMs form lipid-laden macrophages that can buffer local increases in lipid concentration.
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“Recently, Kosteli and colleagues demonstrated that acute weight loss is unexpectedly associated with a rapid -albeit transient -lipolytic-driven recruitment of macrophages into AT (39), thereby confirming similar reports by Granneman and colleagues (44).”
From Adipose tissue remodeling and obesity (2011) · cites this paper as [39]
In the citing paper
“This was indeed observed by Kosteli et al. during chronic weight loss, during which they report that a progressive decrease in lipolysis and ATMΦ content followed 21 days of caloric restriction (39);”
From Adipose tissue remodeling and obesity (2011) · cites this paper as [39]
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“Ironically, acute weight loss (days 0-7), a 24-hour fast, or pharmacological induction of adipocyte lipolysis using a β3-adrenergic agonist all resulted in a transient accumulation of lipid-laden ATMΦs (an increase of up to 65% of macrophage infiltration was observed).”
From Adipose tissue remodeling and obesity (2011) · cites this paper as [39]
In the citing paper
“We thus challenged animals with ADRB agonists and found that the ADRB3 agonist CL316,243, but not the ADRB1/2 agonist isoproterenol, was sufficient to induce IL6 (Figure 3E and F), consistent with previous reports (Kosteli et al., 2010; Zhang et al., 2014).”
From Origin and function of stress-induced IL-6 in murine models (2020) · cites this paper as Kosteli et al., 2010
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“https://doi.org/10.1038/s41590-023-01479-0 induced lipolysis is associated with ATM accumulation and lipid uptake by these cells 53 , whereas interference with the lysosomal function of macrophages abrogates whole-AT lipolysis 37 .”
BackgroundInfluentialSelf-citationThe β3-adrenergic receptor agonist mirabegron improves glucose homeostasis in obese humans
Finlin, B. S., Memetimin, H., Zhu, B., Confides, A. L., Vekaria, H. J., Khouli, R. H. E., Johnson, Z., Westgate, P. M., Chen, J., Morris, A. J., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci134892 · Cited by 261
“As part of our experimental protocol, we added BSA after the addition of FFAs to sequester the FFAs, which demonstrated the effects of FFAs on uncoupling.”
BackgroundInfluentialGlutamine Metabolism in Macrophages: A Novel Target for Obesity/Type 2 Diabetes
Ren, W., Xia, Y., Chen, S., Wu, G., Bazer, F. W., Zhou, B., Tan, B., Zhu, G., Deng, J., & Yin, Y. (2018) · Advances in Nutrition · doi:10.1093/advances/nmy084 · Cited by 261
“In the white adipose tissue of lean animals, macrophages have an M2 phenotype and have critical roles in adipose tissue homeostasis by clearing cellular debris and lipid buffering, whereas macrophages in the white adipose tissue of obese animals are M1 macrophages, producing proinflammatory cytokines to amplify inflam…”
BackgroundMacrophage functional diversity in NAFLD — more than inflammation
Barreby, E., Chen, P., & Aouadi, M. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00675-6 · Cited by 251
Defining macrophage phenotype and function in adipose tissue
Dalmas, É., Clément, K., & Guerre-Millo, M. (2011) · Trends in Immunology · doi:10.1016/j.it.2011.04.008 · Cited by 267
Ontogeny and Polarization of Macrophages in Inflammation: Blood Monocytes Versus Tissue Macrophages
Dey, A., Allen, J., & Hankey-Giblin, P. A. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00683 · Cited by 254
“However, despite transcriptional increases in both M1 and M2 genes, further studies by the authors demonstrated an overall decrease in the M2 populations in the DIO model as exhibited by flow cytometry analysis of eWAT cells expressing macrophage galactose type-C lectin-1 (MGL1, also known as CD301).”
BackgroundInfluentialVerboven, K., Wouters, K., Gaens, K. H. J., Hansen, D., Bijnen, M., Wetzels, S., Stehouwer, C. D. A., Goossens, G. H., Schalkwijk, C., Blaak, E. E., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-22962-x · Cited by 265
White adipose tissue dysfunction in obesity and aging
Reyes-Farias, M., Fos-Domenech, J., Serra, D., Herrero, L., & Sánchez-Infantes, D. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114723 · Cited by 250
Intermittent Fasting: Is the Wait Worth the Weight?
Stockman, M.-C., Thomas, D. D., Burke, J., & Apovian, C. M. (2018) · Current Obesity Reports · doi:10.1007/s13679-018-0308-9 · Cited by 248
Cottam, M. A., Caslin, H. L., Winn, N. C., & Hasty, A. H. (2022) · Nature Communications · doi:10.1038/s41467-022-30646-4 · Cited by 216
A decade of progress in adipose tissue macrophage biology
Hill, A. A., Bolus, W. R., & Hasty, A. H. (2014) · Immunological Reviews · doi:10.1111/imr.12216 · Cited by 227
“(78) have shown that lipolysis induced by caloric restriction or overnight fast results in a transient increase in ATMs.”
BackgroundInfluentialLipid signaling in adipose tissue: Connecting inflammation & metabolism
Masoodi, M., Kuda, O., Rossmeisl, M., Flachs, P., & Kopecký, J. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.09.023 · Cited by 229
Girousse, A., Tavernier, G., Valle, C., Moro, C., Mejhert, N., Dinel, A., Houssier, M., Roussel, B., Besse‐Patin, A., Combes, M., et al. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001485 · Cited by 240
“Since FA released from adipocytes may modulate WAT inflammation [8,17], we investigated WAT macrophages and inflammatory molecules.”
BackgroundCurrent understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease
Machado, F. S., Dutra, W. O., Esper, L., Gollob, K. J., Teixeira, M. M., Factor, S. M., Weiss, L. M., Nagajyothi, F., Tanowitz, H. B., & Garg, N. J. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-012-0351-7 · Cited by 232
“The reduction in adiponectin expression and local lipolysis has been linked to upregulation of inflammatory mediators, insulin resistance [46], and increase in the influx of macrophages into adipose tissue [47], as was demonstrated in experimental of Chagas disease.”
Adipose tissue plasticity from WAT to BAT and in between
Lee, Y., Mottillo, E. P., & Granneman, J. G. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.05.011 · Cited by 236
“15 activated macrophages may also prevent the adverse effects of excessive free fatty acid efflux during weight loss by suppressing lipolysis [98].”
BackgroundLoss of autophagy in hypothalamic POMC neurons impairs lipolysis
Kaushik, S., Arias, E., Kwon, H., Lopez, N. M., Athonvarangkul, D., Sahu, S., Schwartz, G. J., Pessin, J. E., & Singh, R. (2012) · The EMBO Reports · doi:10.1038/embor.2011.260 · Cited by 212
“…of PGC-1 a Although these results agree with a recent study showing a role for lipolysis in adipose tissue infiltrated macrophage recruitment, [16] our data showing an approximately threefold increase in the proportion of M1 macrophages in the lipolysis-deficient KO mice, suggest that…”
Macrophage function in obesity-induced inflammation and insulin resistance
Lauterbach, M., & Wunderlich, F. T. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-1955-5 · Cited by 216
“Under conditions of excessive lipolysis, they control release of fatty acids into the circulation by serving as buffer [55].”
BackgroundRecent advances in obesity-induced inflammation and insulin resistance
Tateya, S., Kim, F., & Tamori, Y. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00093 · Cited by 211
“showed that, although chronic weight loss reduced the macrophage content in adipose tissue, fasting or acute weight loss in turn elicited their accumulation (26).”
BackgroundHypothalamic Inflammation: Marker or Mechanism of Obesity Pathogenesis?
Thaler, J. P., Guyenet, S. J., Dorfman, M. D., Wisse, B. E., & Schwartz, M. W. (2013) · Diabetes · doi:10.2337/db12-1605 · Cited by 215
In Vivo Study of Spherical Gold Nanoparticles: Inflammatory Effects and Distribution in Mice
Chen, H., Dorrigan, A., Saad, S., Hare, D. J., Cortie, M. B., & Valenzuela, S. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058208 · Cited by 214
“The inhibition of ATM activity has been shown to increase lipolysis of the fat cells, thus reducing fat mass in obese mice [14,48].”
BackgroundInfluentialAdipose tissue and adipocyte dysregulation
Lafontan, M. (2013) · Diabetes & Metabolism · doi:10.1016/j.diabet.2013.08.002 · Cited by 218
“[101] Kosteli A, Sugaru E, Haemmerle G, Martin JF, Lei J, Zechner R, et al.”
BackgroundSchweiger, M., Romauch, M., Schreiber, R., Grabner, G. F., Hütter, S., Kotzbeck, P., Benedikt, P., Eichmann, T. O., Yamada, S., Knittelfelder, O. L., et al. (2017) · Nature Communications · doi:10.1038/ncomms14859 · Cited by 204
“This finding is consistent with previous observations that reduced lipolysis causes decreased macrophage infiltration in WAT 23 and reduced Il-6 production 24 .”
Self-citationAdipose tissue at single-cell resolution
Maniyadath, B., Zhang, Q., Gupta, R. K., & Mandrup, S. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.02.002 · Cited by 218
Mottillo, E. P., Bloch, A. E., Leff, T., & Granneman, J. G. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.374041 · Cited by 205
“This acute inflammatory response recruits macrophages that have anti-lipolytic properties, providing an additional mechanism to reduce lipolysis (13).”
BackgroundThe influence of perivascular adipose tissue on vascular homeostasis
Szasz, T., Bomfim, G. F., & Webb (2013) · Vascular Health and Risk Management · doi:10.2147/vhrm.s33760 · Cited by 205
“84 Besides oxidative stress and macrophage infiltration, another crucial element of PVAT dysfunction in obesity is the alteration in secretion of adipocytokines.”
The initiation of metabolic inflammation in childhood obesity
Singer, K., & Lumeng, C. N. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88882 · Cited by 194
“Subsequent production of chemoattractants such as CCL2 and lipolytic signals triggers the recruitment of monocytes from the circulation to form the CLS that engulfs the dying adipocytes and potentiates new adipocyte formation (132, 133).”
BackgroundThe Role of the Immune System in Obesity and Insulin Resistance
Patel, P., Buras, E. D., & Balasubramanyam, A. (2013) · Journal of Obesity · doi:10.1155/2013/616193 · Cited by 201
“Consistent with this hypothesis, visceral adipose tissue depots contain more ATMs than abdominal subcutaneous depots [8].”
BackgroundInfluentialInflammation links excess fat to insulin resistance: the role of the interleukin‐1 family
Tack, C. J., Stienstra, R., Joosten, L. A. B., & Netea, M. G. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01145.x · Cited by 199
“A highly dynamic influx of macrophages in adipose tissue during weight loss appears to facilitate adipocyte lipolysis without activating a proinflammatory state, suggesting that macrophages may also be crucial in the resolution of obesity (58).”
BackgroundAdipose Type One Innate Lymphoid Cells Regulate Macrophage Homeostasis through Targeted Cytotoxicity
Boulenouar, S., Michelet, X., Duquette, D., Álvarez, D., Hogan, A. E., Dold, C., O’Connor, D. B., Stutte, S., Tavakkoli, A., Winters, D., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.01.008 · Cited by 192
“Lipid-filled ATMs also accumulate during fasting, caloric restriction, and pharmacologically induced lipolysis, suggesting that ATMs are an important physiological response to perturbations in adipose tissue (Kosteli et al., 2010; Sun et al., 2011).”
Vitamin D Insufficiency in Overweight and Obese Children and Adolescents
Zakharova, I. N., Klimov, L., Kuryaninova, V. A., Nikitina, I. L., Malyavskaya, S. I., Dolbnya, S. V., Каsyanova, A. N., Atanesyan, R. A., Stoyan, M., Михайловна, Т. А., et al. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00103 · Cited by 195
“Macrophage migration occurs as a result of impaired functioning of adipose tissue and elevated free fatty acid concentrations (32), production by adipocytes of the proteins chemoattractant-1 and alpha-4 integrin promoting adhesion of macrophages to the endothelial wall, and their subsequent passage through the endothe…”
Background
Metadata
- Authors
- Kosteli, A., Sugaru, E., Haemmerle, G., Martin, J. F., Lei, J., Zechner, R., & Ferrante, A. W.
- Affiliations
- Columbia University Irving Medical Center (US)
- University of Graz (AT)
- Corresponding author
- Ferrante, Anthony W.
- Venue
- Journal of Clinical Investigation
- Published
- 2010-10-01
- Volume
- 120
- Issue
- 10
- Pages
- 3466-3479
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC2947229
- OpenAlex
- W2129973062
- Cited by
- 726
- References
- 54
- Citations by year
- 2026: 19 · 2025: 38 · 2024: 36 · 2023: 33 · 2022: 31 · 2021: 47 · 2020: 51 · 2019: 45 · 2018: 47 · 2017: 51 · 2016: 48 · 2015: 53 · 2014: 48 · 2013: 63 · 2012: 62
- FWCI
- 41.55
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Russell Berrie Foundation
- National Institutes of Health (DK026687, DK066525)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-063608, R56DK066525, DK026687, (DK066525, P30DK026687, P30DK063608, R01DK066525)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- adipose tissue macrophages, lipolysis, weight loss, fasting, caloric restriction, obesity, fatty acid uptake, adipose triglyceride lipase, myeloid cell recruitment, lipid metabolism, high-fat diet, macrophage lipid accumulation, chemoattraction
- MeSH terms
- Acyltransferases, Adipose Tissue, Animals, Carboxylic Ester Hydrolases, Cell Movement, Fatty Acids, Nonesterified, Lipase, Lipolysis, Macrophages, Male, Mice, Inbred C57BL, Weight Loss, Mice
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