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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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Citations
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Adipose Tissue Inflammation: Linking Physiological Stressors to Disease Susceptibility
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“In addition, M1 macrophages are associated with the development of insulin resistance and hypertension (23, 37, 41), whereas M2 macrophages play a role in adipose tissue homeostasis, in particular through their role in adipocyte turnover and lipid buffering (16, 27).”
BackgroundSirT1: A Guardian at the Gates of Adipose Tissue Inflammation
Cho, K. W., & Lumeng, C. N.-K. (2011) · Diabetes · doi:10.2337/db11-1308 · Cited by 21
“Besides chemokines, physiological stimuli such as lipolysis and fasting are sufficient to trigger macrophage recruitment to fat (13), and it is possible that metabolic cues lead to the increase in ATMs.”
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“On the other hand, the NEFA in weight loss is a dynamic change that rises first then decreases (32).”
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“org 7 tumor presence reduced the proportion of M2-type macrophages [Ftumor (1, 6)=11.”
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“Recent data indicate that lipolysis and circulating lipids can trigger macrophage recruitment to the fat depot (40).”
Reduction of IL‐6 gene expression in human adipose tissue after sleeve gastrectomy surgery
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“ing weight loss, likely because of an increase in adipose tissue lipolysis.(23) Although inflammation may drive metabolic dysfunction in obesity, macrophages involved in controlled inflammation may play a”
BackgroundInfluentialMetabolic Reprogramming of Macrophages in Atherosclerosis: Is It All about Cholesterol?
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BackgroundLoss of Sirt6 in adipocytes impairs the ability of adipose tissue to adapt to intermittent fasting
Wu, D., Bang, I. H., Park, B., & Bae, E. J. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00664-1 · Cited by 20
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“It has been reported that the infiltration of macrophages in adipose tissue is controlled by the adipose tissue weight and the volume of lipid metabolism [29].”
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“Increased expression of macrophage markers during VLCD might be associated with enhanced fatty acids release from adipocytes as a possible trigger of macrophage activation and infiltration mediated by TLR4 signaling as shown before ( Kosteli et al. 2010, Suganami et al. 2005 ) .”
Harmon, D. B., Wu, C., Dedousis, N. L., SIPULA, I. J., Stefanović-Račić, M., Schoiswohl, G., O'Donnell, C. P., Alonso, L. C., Kershaw, E. E., Kelley, E. E., et al. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00172.2018 · Cited by 18
“(21) used immunohistochemistry and quantitative PCR for their analysis, and previous findings from our group using similar techniques also demonstrated that fasting increases AT crown-like structure formation and elevates AT Cd11c and F4/80 mRNA (35).”
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ResultObesity and Fibrosis: Setting the Stage for Breast Cancer
Kuziel, G. M., Moore, B. N., & Arendt, L. M. (2023) · Cancers · doi:10.3390/cancers15112929 · Cited by 16
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“Furthermore, in a recent study in mice, it was shown that the adipose tissue lipolysis also depended on the phase of the diet (15).”
BackgroundMyocardial Insulin Resistance: An Overview of Its Causes, Effects, and Potential Therapy
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“MCP-1 is also known to regulate recruitment of macrophages to sites of inflammation and may be involved in the recruitment and differentiation of monocytes to macrophages that produce pro-inflammatory cytokines in conditions such as obesity and dyslipidaemia [97, 104].”
BackgroundThe Ups and Downs of Insulin Resistance and Type 2 Diabetes: Lessons from Genomic Analyses in Humans
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“With continued nutrient excess, the capacity for lipid storage is overwhelmed, unrestrained lipolysis ensues, and proinflammatory cascades are engaged [123].”
BackgroundHuman Congenital Perilipin Deficiency and Insulin Resistance
Kozusko, K., Patel, S., & Savage, D. B. (2013) · Endocrine development · doi:10.1159/000342511 · Cited by 17
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“Manipulations that reduce lipolysis in these mice also decrease the recruitment of ATMs, suggesting that FFA drives ATM accumulation [60,61].”
BackgroundA Critical Assessment of Fasting to Promote Metabolic Health and Longevity
Fazeli, P. K., & Steinhauser, M. L. (2025) · Endocrine Reviews · doi:10.1210/endrev/bnaf021 · Cited by 19
“When the contraction of fat mass and weight loss is protracted over several weeks in a model of chronic caloric restriction in obese mice, an influx of macrophages is detectable (224).”
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“For example, the induction of lipolysis and release of FFAs through pharmacological intervention or over-night fasting leads to an increase in adipose tissue macrophages [41,42].”
Adipokines and their Involvement as a Target of New Drugs
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“The metabolically dysfunctional adipose tissue is also characterized by higher number of adipocytes undergoing necrosis, and by macrophages distributed around these dead cells in a crown-like structure [7,24,25].”
BackgroundMagnetic resonance assessment of the cerebral alterations associated with obesity development
Lizarbe, B., Campillo, B. W., Guadilla, I., López‐Larrubia, P., & Cerdán, S. (2020) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x20941263 · Cited by 16
“Moreover, HFD models allow to investigate feeding/fasting paradigms superimposed to the dietary manipulations, an acute nutritional intervention currently considered to promote activation of the neuro-inflammatory profile.(75)”
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Glycoprotein Non-Metastatic Protein B (GPNMB): The Missing Link Between Lysosomes and Obesity
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“This review aims to summarize and clarify the role of GPNMB in the progression of obesity and to highlight its potential use as a biomarker for lipid-associated disorders.”
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“bolic regulation, adipose tissue modulates the immune system by recruiting and activating lymphoid and myeloid cells (Kosteli et al., 2010).”
BackgroundCharacterization and Treatment of Inflammation and Insulin Resistance in Obese Adipose Tissue
Lu, Z., Li, Y., & Song, J. (2020) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s271509 · Cited by 16
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“Monocytes recruited during weight loss are another source of M2 macrophages, which help with the processing of fatty acids in adipose tissue during this phase; the numbers of these cells drop once weight loss is achieved.(68) The loss of anti-inflammatory actions of M2 macrophages and augmented inflammatory responses…”
BackgroundLoft, A., Rydbirk, R., Gammelmark, E., Hauwaert, E. L. V., Wernberg, C. W., Møller, A. F., Dam, T. V., Hassan, M. N., Maniyadath, B., Nielsen, R., et al. (2026) · Nature Metabolism · doi:10.1038/s42255-025-01433-4 · Cited by 17
“…we found that the proportions of macrophage subpopulations remained relatively stable following the moderate lifestyle-induced weight loss, suggesting that macrophage lipid handling continued to have a role in supporting healthy AT remodelling during the early stages of weight loss 10,11,13,14,67 .”
Importance of temperature on immuno‐metabolic regulation and cancer progression
Wang, H., Çolakoğlu, M., & Trajkovski, M. (2022) · FEBS Journal · doi:10.1111/febs.16632 · Cited by 14
“…potential metabolic signals, such as fatty acids, amino acids, hypoxia and adipocyte stress, have been proposed to contribute to the interaction between immune cells and adipocytes at different temperatures [82,83]; however, more efforts are needed to better understand their importance (Table 1).”
BackgroundReciprocal signaling between adipose tissue depots and the central nervous system
Puente-Ruiz, S. C., & Jaïs, A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.979251 · Cited by 17
“ATMs help maintain adipose tissue homeostasis by controlling key signaling pathways involved in adipogenesis, lipogenesis, lipolysis, and lipid uptake (Kosteli et al., 2010; Bilkovski et al., 2011; Nguyen et al., 2011; Brunner et al., 2020; Chen et al., 2021).”
BackgroundZhu, Y.-N., Gu, X.-L., Wang, L.-Y., Guan, N., & Li, C.-G. (2023) · Immunological Investigations · doi:10.1080/08820139.2023.2173077 · Cited by 14
“(Continued). production of secondary damage and resists plaque formation in atherosclerosis (Kosteli et al. 2010).”
BackgroundZhang, M. Q., Heirbaut, S., Jing, X., Stefańska, B., Vandaele, L., Neve, N. D., & Fievez, V. (2024) · Journal of Dairy Science · doi:10.3168/jds.2023-24156 · Cited by 14
Zhao, H., Li, L., Tan, J., Wang, Y., Zhang, A., Zhao, Y., & Jiang, L. (2024) · Antioxidants · doi:10.3390/antiox13050614 · Cited by 14
“Lipolysis partly induces adipose tissue macrophage (ATM) infiltration by excessive release of NEFA from adipocytes [65].”
BackgroundAdipose tissue microenvironments during aging: Effects on stimulated lipolysis
Camell, C. D. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2022.159118 · Cited by 16
Influence of Weight Loss and Weight Regain on Adipose Tissue Inflammation
Cáceres, L., Ray, A. G., Emont, M. P., & Weinstock, A. (2025) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.125.322196 · Cited by 16
Role of Nrf2 in Oxidative and Inflammatory Processes in Obesity and Metabolic Diseases
Bayliak, M. M., & Abrat, O. (2020) · Progress in inflammation research · doi:10.1007/978-3-030-44599-7_7 · Cited by 14
Macrophages play a nutritive role in post-metamorphic maturation in Drosophila
Krejčová, G., Danielová, A., Sehadová, H., Dyčka, F., Kubásek, J., Moos, M., & Bajgar, A. (2024) · Development · doi:10.1242/dev.202492 · Cited by 13
Komaravolu, R. K., Mehta-D’souza, P., Conner, T., Allen, M. T., Lumry, J., Batushansky, A., Pezant, N. P., Montgomery, C. G., & Griffin, T. M. (2024) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2024.03.109 · Cited by 13
“These features of β AR stimulation are biologically coupled, as lipolysis increases trafficking of M2-like macrophages to adipose tissue 15 .”
BackgroundDynamic Roles and Expanding Diversity of Adipose Tissue Macrophages in Obesity
Soedono, S., Julietta, V., Nawaz, H., & Cho, K. W. (2024) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes24030 · Cited by 16
“73,75,76 76-78 These lipid-laden ATMs surround dead adipocytes, forming CLS that facilitate the clearance of dead fat cells.”
BackgroundHoulahan, K. E., Prokopec, S. D., Sun, R., Moffat, I. D., Lindén, J., Lensu, S., Okey, A. B., Pohjanvirta, R., & Boutros, P. C. (2015) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2015.07.018 · Cited by 12
Pandey, R., Bakay, M. A., Strenkowski, B. P., Hain, H. S., & Hakonarson, H. H. (2021) · Scientific Reports · doi:10.1038/s41598-021-86493-8 · Cited by 13
Adipose tissue metabolism and inflammation in obesity
van Meijel, R. L. J., Blaak, E. E., & Goossens, G. H. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813553-2.00001-4 · Cited by 13
Murray, S. A., Dalbøge, L. S., Baquero, K., Sanford, C. A., Misquith, A., Mercer, A. J., Meek, T. H., Guldbrandt, M., Andersen, B., Kievit, P., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-64170-6 · Cited by 12
Zhou, C., Ruiz, H. H., Li, L., Maurizi, G., Sakamoto, K., Liberini, C. G., Wang, L., Stanley, A. T., EĞRİTAĞ, H. E., Sanz, S., et al. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101813 · Cited by 12
“As the increased ef fl ux of nonesteri fi ed fatty acids (NEFA) released through adipose lipolysis can be pro-in fl ammatory [15], we hypothesized that unrestrained lipolysis may account for the alcohol induced in fl ammation in adipose tissue and the hypothalamus.”
BackgroundScolaro, B., Krautter, F., Brown, E. J., Ray, A. G., Kalev‐Altman, R., Petitjean, M., Delbare, S., Donahoe, C., Pena, S., Garabedian, M. L., et al. (2025) · Journal of Clinical Investigation · doi:10.1172/jci172198 · Cited by 16
“…in atherosclerotic plaques; (b) enrichment in both plaques and eWAT of a macrophage subpopulation distinguished by high expression of Fcgr4 ; and (c) loss of these features when mice were allowed to regain weight after stCR, likely through reprogramming of myeloid progenitors in the bone marrow.”
Kristensen, M. D., Lund, M. T., Hansen, M., Poulsen, S. S., Ploug, T., Dela, F., Helge, J. W., & Prats, C. (2017) · Obesity · doi:10.1002/oby.21964 · Cited by 12
“This is in line with other findings (30) that have shown that acute energy restriction increases ATM content in mice, whereas a continuing weight loss leads to decreased ATM infiltration.”
BackgroundResultJohns, D. G., Wang, S., Rosa, R. L., Hubert, J. A., Xu, S. S., Chen, Y., Bateman, T. J., & Blaustein, R. O. (2019) · Pharmacology Research & Perspectives · doi:10.1002/prp2.543 · Cited by 12
de Boer, J. F., Dikkers, A., Jurdzinski, A., von Felden, J., Gaestel, M., Bavendiek, U., & Tietge, U. J. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106300 · Cited by 12
“This property of adipose tissue macrophages was recently described [36].”
BackgroundCaslin, H. L., & Hasty, A. H. (2019) · Current Obesity Reports · doi:10.1007/s13679-019-00344-2 · Cited by 13
Expansion and inflammation of white adipose tissue - focusing on adipocyte progenitors
Liu, W., Li, D., Cao, H., Li, H., & Wang, Y. (2020) · Biological Chemistry · doi:10.1515/hsz-2019-0451 · Cited by 12
Šiklová, M., Simonsen, L., Polak, J., Štich, V., & Bülow, J. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3846 · Cited by 12
“It was suggested that a higher proinflammatory profile during acute calorie restriction could be dependent on AT lipolysis and an associated release of fatty acids that may attract immune cells into AT or directly influence proinflammatory cytokines production (7).”
BackgroundMacrophages expressing uncoupling protein 1 increase in adipose tissue in response to cold in humans
Finlin, B. S., Memetimin, H., Confides, A. L., Zhu, B., Westgate, P. M., Dupont‐Versteegden, E. E., & Kern, P. A. (2021) · Scientific Reports · doi:10.1038/s41598-021-03014-3 · Cited by 11
A detective story of intermittent fasting effect on immunity
Ma, R. (2024) · Immunology · doi:10.1111/imm.13829 · Cited by 14
“FFA released by lipolysis, play an important role in obesity-induced adipose tissue inflammation [28], immunomodulation [29], and stimulation of hepatic very low-density lipoprotein (VLDL) production [30].”
Liu, D., Morales, F. E., IglayReger, H. B., Treutelaar, M. K., Rothberg, A. E., Hubal, M. J., Nadler, E. P., Robidoux, J., Barakat, H. A., Horowitz, J. F., et al. (2017) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2017-0228 · Cited by 11
“The non-significant change of macrophage gene expression in both skeletal and adipose tissues in response to weight loss might be due to increased lipolysis induced by the low-calorie diet, as it has been suggested that augmentation lipolysis can drive macrophage infiltration (Kosteli et al. 2010).”
BackgroundManaging complexity: Dealing with systemic crosstalk in bovine physiology
Bradford, B. J., Yuan, K., & Ylioja, C. M. (2015) · Journal of Dairy Science · doi:10.3168/jds.2015-10271 · Cited by 11
“…if this extreme physiological state is excluded, there is strong evidence that adipose tissue macrophages regulate both lipolysis during fasting (Kosteli et al., 2010) and thermogenesis in brown adipose tissue during cold exposure (Nguyen et al., 2011), that immune cells (likely liver T cells)…”
BackgroundA possible secondary immune response in adipose tissue during weight cycling
Anderson‐Baucum, E. K., Major, A. S., & Hasty, A. H. (2014) · Adipocyte · doi:10.4161/adip.27556 · Cited by 11
“Weight loss decreases pathologies associated with obesity, including adipose tissue inflammation and IR.(17,18) However, weight loss is difficult to maintain, leading to weight regain or weight cycling.”
BackgroundLinks between Immunologic Memory and Metabolic Cycling
Cottam, M. A., Itani, H. A., Beasley, A. A., & Hasty, A. H. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701713 · Cited by 13
Dalmas, É., Tordjman, J., Guerre-Millo, M., & Clément, K. (2011) · médecine/sciences · doi:10.1051/medsci/20112711016 · Cited by 17
Radwan, M. M., Radwan, B. M., Nandipati, K. C., Hunter, W. J., & Agrawal, D. K. (2013) · Expert Review of Clinical Immunology · doi:10.1586/1744666x.2013.816484 · Cited by 11
Immune activation induced by dysregulated lipid metabolism in the pathogenesis of type 2 diabetes
Yang, H., Yu, W., Mao, Q., & Zhao, L. (2025) · World Journal of Diabetes · doi:10.4239/wjd.v16.i12.114395 · Cited by 11
Keshvari, S., Masson, J. J. R., Ferrari-Cestari, M., Bodea, L., Nooru‐Mohamed, F., Tse, B. W.-C., Sokolowski, K. A., Batoon, L., Patkar, O. L., Sullivan, M. A., et al. (2023) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00347.2023 · Cited by 10
Schaftenaar, F. H., van Dam, A. D., de Bruin, G., Depuydt, M. A. C., de Mol, J., Amersfoort, J., Douna, H., Meijer, M., Kröner, M. J., van Santbrink, P. J., et al. (2024) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.123.319701 · Cited by 10
Ahn, C., Divoux, A., Zhou, M., Seldin, M. M., Sparks, L. M., & Whytock, K. L. (2025) · Obesity · doi:10.1002/oby.24264 · Cited by 10
“Weight loss induces extensive morphological and functional remodeling of adipocytes, which includes reduced adipocyte size and restoration of lipid metabolism in obesity [11,40,60].”
Chen, S., Fu, J., Yan, J., Zhao, R., Qian, C., Yisimayili, Z., & Wu, J. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00071.2025 · Cited by 10
Weight Loss‐Associated Remodeling of Adipose Tissue Immunometabolism
Basso, P. J., Schcolnik‐Cabrera, A., Zhu, M., Strachan, E. R., Clemente‐Casares, X., & Tsai, S. J. (2025) · Obesity Reviews · doi:10.1111/obr.13975 · Cited by 13
“In a HFD model, short-term CR led to increased recruitment of ATMS, whereas prolonged CR resulted in a reduction in ATM numbers [204].”
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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