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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]
In the citing paper
“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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“ATMs have been defined almost exclusively using the markers F4/80CD11b by our group and others (8, 34, 37).”
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“Consequently, adipose tissue macrophage (ATM) infiltration and accumulation into the fat tissue 82 is also increased, which promotes inflammatory responses in the adipose tissue by directly engaging 83 toll-like receptors (TLR) to induce production of cytokines, such as TNFα (9).”
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“These include lipolytic signals, chemokines, chemoattractants, cytokines, and pathogen associated molecular proteins (PAMPs) such as lipopolysaccharide [4,8,9].”
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“In addition, we blocked macrophage infiltration and adipose tissue inflammation by pharmacologic treatment with liposome-clodronate (36).”
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“The increased stress and hypoxia (24) resulting in the release of free fatty acids and reactive oxygen species to initiate inflammation in adipose tissue can recruit more inflammatory monocytes to differentiate into classically activated macrophages (M1) (25,26).”
BackgroundImmunological contributions to adipose tissue homeostasis
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“Rather, they functioned to suppress further adipocyte lipolysis [71].”
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“It has been well established that M2 macrophages predominate in insulin-sensitive adipose tissue in lean subjects, whereas M1 macrophages accumulate commensurate with adipose tissue mass in the obese state (Lumeng et al. 2007; Kosteli et al. 2010; Weisberg et al. 2003).”
IL-33 causes thermogenic failure in aging by expanding dysfunctional adipose ILC2
Goldberg, E. L., Shchukina, I., Youm, Y., Ryu, S., Tsusaka, T., Young, K. C., Camell, C. D., Dlugos, T., Artyomov, M. N., & Dixit, V. D. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.08.004 · Cited by 89
“The adiposeresident immune compartment controls inflammation in visceral adipose tissue (VAT) and regulates fasting-induced lipolysis (Camell et al., 2017; Kosteli et al., 2010), cold-induced thermogenesis (Brestoff et al.”
BackgroundLipid storage by adipose tissue macrophages regulates systemic glucose tolerance
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“Nutrients 2015, 7 732 Alterations in free fatty acid (FFA) concentrations could provide a chemotactic stimulus for macrophage infiltration through arachidonic acid products or the release of chemokines, such as monocyte chemoattractant protein-1 (MCP-1) [11,12].”
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Macrophages in epididymal adipose tissue secrete osteopontin to regulate bone homeostasis
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“It was recently observed that M2 macrophages were increased in animals during weight loss [42].”
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“Firstly, by buffering fluctuations in tissue lipid levels, adipose tissue- and liver-resident macrophages help to maintain metabolic homeostasis (5, 10, 11).”
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“In turn, TNF-α promotes lipolysis through a variety of mechanisms; the injection of recombinant TNF-α in cattle reduced feed intake (Kushibiki et al., 2003) and insulin sensitivity (Kushibiki et al., 2001), and directly stimulated lipolysis (Kushibiki et al., 2002).”
BackgroundSex Differences in Inflammatory Responses to Adipose Tissue Lipolysis in Diet-Induced Obesity
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“Moreover, the conditioned medium from ox-LDL–treated released from enlarged adipocytes and augmented by increased lipolysis in obesity (Landin et al., 1990; Tsujita et al., 1995; Lafontan and Langin, 2009; Kosteli et al., 2010).”
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“In a model of weight loss, lipolysis is a forced process to reduce fat mass; by triggering a negative energy balance lipolysis is increased to provide FFAs that will be transported from the AT to the skeletal muscle to be used as energy substrate [31].”
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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