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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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“(38)) may play an important role in mediating ATM recruitment to visceral fat, at least in mice models.”
BackgroundLysosomal Stress in Obese Adipose Tissue Macrophages Contributes to MITF-Dependent Gpnmb Induction
Gabriel, T. L., Tol, M. J., Ottenhoff, R., van Roomen, C. P. A. A., Aten, J., Claessen, N., Hooibrink, B., de Weijer, B. A., Serlie, M. J. M., Argmann, C., et al. (2014) · Diabetes · doi:10.2337/db13-1720 · Cited by 66
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“Similarly, release of FFA from adipose storage during fasting is acutely associated with accumulation of macrophages in visceral fat depots [41].”
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Engin, A. B., Engin, A., & Gönül, İ. I. (2019) · Journal of Molecular Endocrinology · doi:10.1530/jme-18-0252 · Cited by 64
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“Recently, it was proposed that macrophages recruited to adipose tissue during activation of lipolysis function to limit subsequent fatty acid mobilization (25).”
BackgroundIL-6 Strikes a Balance in Metabolic Inflammation
Covarrubias, A. J., & Horng, T. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.05.009 · Cited by 62
“…to increase circulating levels of IL-6, and M2 activation in these contexts may promote muscle regeneration, adaptive thermogenesis, and lipid scavenging, respectively (Kosteli et al., 2010; Nguyen et al., 2011; Pillon et al., 2013; Wernstedt Cell Metabolism et al., 2006; Wueest et al., 2014).”
BackgroundC/EBPα regulates macrophage activation and systemic metabolism
Lee, B., Qiao, L., Lu, M. M., Yoo, H. S., Cheung, W., MAK, R. H. K., Schaack, J. B., Feng, G., Chi, N., Olefsky, J. M., et al. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00002.2014 · Cited by 63
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“Recent studies implicate novel roles for immune cells, such as macrophages, in regulating lipolysis during diet-induced obesity (8).”
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“Excessive lipolysis in WAT causes accumulation of ectopic lipids and promotes a pro-inflammatory state [13–15], which can cause or worsen insulin resistance in muscle and liver [16–18].”
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Kohlgruber, A. C., LaMarche, N. M., & Lynch, L. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.09.005 · Cited by 60
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“ingly, the number of macrophages also increases during weight loss when adipocytes do not die, but shrink losing their lipid content.(11) Although there is a direct contact between adipocytes and”
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“after fasting or after initial weight loss in HFD-fed mice, suggesting that increased FFA may be an important cue for macrophage recruitment (38).”
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“In fact, lipolysis (pharmacologically-induced or through short-term fasting) is associated with increased macrophage recruitment to AT (62).”
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“When people or animals become obese, macrophages accumulate in adipose tissue and cytokine secretion significantly increases (Schenk et al., 2008; Kosteli et al., 2010).”
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Prolonged fasting drives a program of metabolic inflammation in human adipose tissue
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“In mice, contraction of AT mass over several weeks of caloric restriction drives a macrophage population that supports lipolysis [21].”
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Adipose tissue transcriptome changes during obesity development in female dogs
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“The exact role of adipose tissue macrophages is unclear; however, recent advances indicate they are involved in adipose tissue remodeling, phagocytosis of lipid droplets of dead adipocytes, and regulation of adipocyte lipolysis in the fasting state (65, 10, 31).”
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“Murine eWAT was removed and fixed in zinc-formalin (Anatech LTD, MI USA, 170) overnight at 4°C and prepared as previously described (Kosteli et al, 2010).”
MethodRedox Regulation of Lipid Mobilization in Adipose Tissues
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Macrophages, Metabolism and Heterophagy in the Heart
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“Considering that body weight and fat mass changes influence WAT inflammation and Mv infiltration, affecting glucose tolerance and insulin sensitivity (1,2,44), we chose short-term EPO treatment regimen (,3 weeks) after obesity induction.”
CCR7 Maintains Nonresolving Lymph Node and Adipose Inflammation in Obesity
Hellmann, J. L., Sansbury, B. E., Holden, C. R., Tang, Y., Wong, B. C. K., Wysoczynski, M., Rodríguez, J., Bhatnagar, A., Hill, B. G., & Spite, M. R. (2016) · Diabetes · doi:10.2337/db15-1689 · Cited by 52
“Because saturated fatty acids drive macrophage accumulation in adipose tissue and stimulate inflammatory signaling (1,43), it is likely that these fatty acids are a prominent stimulus for increased CCR7 expression in obesity.”
BackgroundMuir, L. A., Kiridena, S., Griffin, C. A., DelProposto, J. B., Geletka, L. M., Martinez-Santibañez, G., Zamarron, B. F., Lucas, H. R., Singer, K., O’Rourke, R. W., et al. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.3hi1017-422r · Cited by 56
Jak-TGFβ cross-talk links transient adipose tissue inflammation to beige adipogenesis
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Netrin-1 Alters Adipose Tissue Macrophage Fate and Function in Obesity
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“During the expansion of adipose tissue, inflammatory processes may be important for regulating adaptive responses, however the unresolved inflammation associated with obesity is thought to lead to metabolic dysfunction and insulin resistance [57,58].”
BackgroundSex hormones regulate metainflammation in diet-induced obesity in mice
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“However, there is strong evidence to implicate a shift in immune cell responses to a more chronic activated myeloid profile that contributes to sequelae of obesity in males (11, 12).”
Backgroundβ3-Adrenergic Receptor Stimulation Induces E-Selectin-mediated Adipose Tissue Inflammation
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IKKβ Is Essential for Adipocyte Survival and Adaptive Adipose Remodeling in Obesity
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“Increased ATM number has also been associated with elevated adipose lipolysis and circulating FFA levels (40).”
Kidney triglyceride accumulation in the fasted mouse is dependent upon serum free fatty acids
Scerbo, D. A., Son, N.-H., Sirwi, A., Zeng, L., Sas, K. M., Cifarelli, V., Schoiswohl, G., Huggins, L.-A., Gumaste, N., Hu, Y., et al. (2017) · Journal of Lipid Research · doi:10.1194/jlr.m074427 · Cited by 53
“3-adrenergic receptor agonist, CL 316,243 (Sigma), was dissolved in PBS and injected into C57BL/6 mice at 1 mg/kg at two time points (2:00 PM and 6:00 PM) (23).”
MethodRegulation of immunometabolism in adipose tissue
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Emamalipour, M., Seidi, K., Jahanban‐Esfahlan, A., & Jahanban‐Esfahlan, R. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28913 · Cited by 54
“…changes in cellular compositions and immune cell populations in WAT that may bring about M1 and M2 macrophages imbalance toward M1, and enhance M1 macrophages in WAT (Al Hannan & Culligan, 2015; Kosteli et al., 2010; Lumeng & Saltiel, 2011; Morris, Singer, & Lumeng, 2011; Weisberg et al., 2003).”
BackgroundLiu, B., Hutchison, A. T., Thompson, C. H., Lange, K. M., & Heilbronn, L. K. (2019) · Obesity Research & Clinical Practice · doi:10.1016/j.orcp.2019.07.001 · Cited by 54
Characterization of Eicosanoids Produced by Adipocyte Lipolysis
Gartung, A., Zhao, J., Chen, S., Mottillo, E. P., VanHecke, G. C., Ahn, Y., Maddipati, K. R., Sorokin, A., Granneman, J. G., & Lee, M.-J. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.725937 · Cited by 51
“Previous work has shown that excessive lipolysis is associated with adipose tissue inflammation and immune cell infiltration (15, 16, 33).”
BackgroundMacrophages protect against loss of adipose tissue during cancer cachexia
Erdem, M., Möckel, D., Jumpertz, S., John, C., Fragoulis, A., Rudolph, I., Wulfmeier, J., Springer, J., Horn, H., Koch, M., et al. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12450 · Cited by 51
Xiao, T., Langston, P. K., Muñoz-Rojas, A. R., Jayewickreme, T., Lazar, M. A., Benoist, C. O., & Mathis, D. J. (2022) · Science Immunology · doi:10.1126/sciimmunol.abl7641 · Cited by 54
“NE-induced lipolysis is an important mechanism for providing nutrients during states of energy deprivation (59), but excessive lipolysis recruits inflammatory infiltrates to the adipose tissue (60, 61).”
BackgroundMartinez-Santibañez, G., Singer, K., Cho, K. W., DelProposto, J. L., Mergian, T. A., & Lumeng, C. N.-K. (2015) · Adipocyte · doi:10.1080/21623945.2015.1027848 · Cited by 52
“Lipolytic remodeling activatesMmp12 expression To observe rapid adipose tissue remodeling in a different context, we employed the use of an acute lipolysis model.(24) To examine the regulation of Mmp12 gene expression in this setting, we assessed age-matched lean (ND) and obese (16-week HFD) mice after 3 days of treat…”
MethodCole, B. K., Morris, M. A., Grzesik, W. J., Leone, K. A., & Nadler, J. L. (2012) · Mediators of Inflammation · doi:10.1155/2012/851798 · Cited by 51
“promotes a phenotypic proinflammatory switch in the macrophages that is detrimental to local adipocyte health and metabolism [36, 37].”
BackgroundHuman CD206+ macrophages associate with diabetes and adipose tissue lymphoid clusters
Muir, L. A., Cho, K. W., Geletka, L. M., Baker, N. A., Flesher, C. G., Ehlers, A. P., Kaciroti, N., Lindsly, S., Ronquist, S., Rajapakse, I., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.146563 · Cited by 52
Adipocyte CAMK2 deficiency improves obesity-associated glucose intolerance
Dai, W., Choubey, M., Patel, S., Singer, H. A., & Özcan, L. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101300 · Cited by 49
“Although the underlying molecular mechanisms that initiate and sustain WAT inflammation are complex, growing evidence indicates that high circulating plasma insulin and FFA levels as well as disrupted calcium homeostasis and insulin signaling are involved in this regulation [3,50,62,69].”
BackgroundPeriparturient lipolysis and oxylipid biosynthesis in bovine adipose tissues
Contreras, G. A., Strieder‐Barboza, C., de Souza, J., Gandy, J. C., Mavangira, V., Lock, A. L., & Sordillo, L. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188621 · Cited by 48
Nanomaterials for the theranostics of obesity
Li, J., Cha, R., Luo, H., Hao, W., Zhang, Y., & Jiang, X. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119474 · Cited by 48
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Singh, M., & Benencia, F. (2019) · International Reviews of Immunology · doi:10.1080/08830185.2019.1638921 · Cited by 48
Involvements of long noncoding RNAs in obesity‐associated inflammatory diseases
Wijesinghe, S. N., Nicholson, T. A., Tsintzas, K., & Jones, S. W. (2020) · Obesity Reviews · doi:10.1111/obr.13156 · Cited by 48
“transient changes in body fat mass, these specialized immune cells or AT resident macrophages function to regulate tissue homeostasis and are involved in energy production, adipogenesis and lipid metabolism.(60,61) With obesity, the chronic expansion in AT mass”
BackgroundChalla, T. D., Straub, L. G., Baláž, M., Kiehlmann, E., Donzé, O., Rudofsky, G., Ukropec, J., Ukropcová, B., & Wolfrum, C. (2015) · Diabetes · doi:10.2337/db14-1932 · Cited by 45
“Conversely, hyperplasia is followed by a reduction in M1-type markers and an increase in anti-inflammatory “alternatively activated” M2 macrophages (11).”
BackgroundGarcia, Z. M., Oliveira, M. C., Lima, R. L., Soriani, F. M., Cisalpino, D., Botion, L. M., Teixeira, M. M., Souza, D. G., & Ferreira, A. V. M. (2013) · Obesity · doi:10.1002/oby.20142 · Cited by 46
“However, in such cases, there are concomitant reductions in body mass and adipose tissue weight (8,9,28).”
BackgroundAdipocytes Modulate the Phenotype of Human Macrophages through Secreted Lipids
Klein‐Wieringa, I. R., Andersen, S. N., Kwekkeboom, J. C., Giera, M. A., de Lange-Brokaar, B. J. E., van Osch, G. J. V. M., Zuurmond, A., Stojanovic-Susulic, V., Nelissen, R. G. H. H., Pijl, H., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1203074 · Cited by 48
“This could be relevant in the light of a recent publication indicating that variation in nutrient availability, rather than BMI alone, are important regulators of ATM recruitment and proinflammatory changes (41).”
BackgroundMolli, A. E. I., Steinhardt, A. P., López, A. P., González, C. D., Vilarino, J. F., Frechtel, G. D., & Cerrone, G. E. (2017) · PLoS ONE · doi:10.1371/journal.pone.0190528 · Cited by 49
Macrophages modulate cardiac function in lipotoxic cardiomyopathy
Schilling, J. D., Machkovech, H. M., Kim, A. H. J., Schwedwener, R., & Schaffer, J. E. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00111.2012 · Cited by 48
“It is also possible that myocyte cell death or free fatty acids themselves contribute to the influx of macrophages (14).”
BackgroundExploring the activated adipogenic niche: Interactions of macrophages and adipocyte progenitors
Lee, Y., Thacker, R. I., Hall, B. K., Kong, R., & Granneman, J. G. (2014) · Cell Cycle · doi:10.4161/cc.27647 · Cited by 46
“, fasting, calorie restriction, adrenergic remodeling).(15,19) A cell-isolation strategy based on CD44 expression and lipid content may allow more precise isolation of the relevant subpopulations.”
BackgroundLack of “immunological fitness” during fasting in metabolically challenged animals
Asterholm, I. W., McDonald, J. L., Blanchard, P.-G., Sinha, M. K., Xiao, Q., Mistry, J., Rutkowski, J. M., Deshaies, Y., Brekken, R. A., & Scherer, P. E. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m021725 · Cited by 45
“Kosteli et al. ( 10 ) have recently observed that fasting and weight loss is associated with a transient expected, fasting caused increased PEPCK and reduced SREBP1c levels in both adipose and liver (see supplementary Fig.”
BackgroundResultAutophagy Is Dispensable for Macrophage-Mediated Lipid Homeostasis in Adipose Tissue
Grijalva, A., Xu, X., & Ferrante, A. W. (2016) · Diabetes · doi:10.2337/db15-1219 · Cited by 46
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Caspar‐Bauguil, S., Kolditz, C.-I., Lefort, C., Vila, I. K., Mouisel, É., Beuzelin, D., Tavernier, G., Marqués, M.-A., Zakaroff‐Girard, A., Pécher, C., et al. (2015) · Diabetologia · doi:10.1007/s00125-015-3719-0 · Cited by 45
“Accordingly, mouse ATMs accumulate lipids in response to lipolysis during fasting [42].”
BackgroundSpontaneous hypertension occurs with adipose tissue dysfunction in perilipin-1 null mice
Zou, L., Wang, W., Liu, S., Zhao, X., Lyv, Y., Du, C., Su, X., Geng, B., & Xu, G. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.024 · Cited by 44
Adipose tissue signaling by nuclear receptors in metabolic complications of obesity
Jacobi, D., Stanya, K. J., & Lee, C. (2012) · Adipocyte · doi:10.4161/adip.19036 · Cited by 45
“While it is known that visceral WAT has higher levels of lipolysis and contains more ATMs than abdominal subcutaneous WAT,(41-43) recent studies have characterized the effects of weight loss and fasting on ATMs in mice and identified a role for lipolysis in macrophage recruitment.(44) First, increases in ATM number co…”
BackgroundMacrophage Rewiring by Nutrient Associated PI3K Dependent Pathways
Sharif, O., Brunner, J. S., Vogel, A., & Schabbauer, G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02002 · Cited by 47
“Together, ATMs respond to their environment by upregulating lipid/lysosomal programs, which is likely heighted during obesity, allowing them to fulfill their main function of clearing up dying adipocytes, buffering lipids, preventing ectopic lipid spill over, and ensuing insulin resistance (25, 26, 33, 34).”
BackgroundBrunner, J. S., Vogel, A., Lercher, A., Caldera, M., Korosec, A., Pühringer, M., Hofmann, M., Hajto, A., Kieler, M., Garrido, L. Q., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00311-5 · Cited by 45
The SCN Clock Governs Circadian Transcription Rhythms in Murine Epididymal White Adipose Tissue
Kolbe, I., Husse, J., Salinas, G., Lingner, T., Astiz, M., & Oster, H. (2016) · Journal of Biological Rhythms · doi:10.1177/0748730416666170 · Cited by 45
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Dyslipidemia: Obese or Not Obese—That Is Not the Question
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Regulation of metabolism by cGMP
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Macrophage ontogeny in the control of adipose tissue biology
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“Mice were sacrificed 14 h after the second injection [25, 59].”
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An anti-inflammatory phenotype in visceral adipose tissue of old lean mice, augmented by exercise
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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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