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Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice
Open accessAbstract
Obesity is accompanied by adipocyte death and accumulation of macrophages and mast cells in expanding adipose tissues. Considering the differences in biological behavior of fat found in different anatomical locations, we explored the distribution of mast cells, solitary macrophages, and crown-like structures (CLS), the surrogates for dead adipocytes, in subcutaneous and abdominal visceral fat of lean and diet-induced obese C57BL/6 mice. In fat depots of lean mice, mast cells were far less prevalent than solitary macrophages. Subcutaneous fat contained more mast cells, but fewer solitary macrophages and CLS, than visceral fat. Whereas no significant change in mast cell density of subcutaneous fat was observed, obesity was accompanied by a substantial increase in mast cells in visceral fat. CLS became prevalent in visceral fat of obese mice, and the distribution paralleled mast cells. Adipose tissue mast cells contained and released preformed TNF-α, the cytokine implicated in the pathogenesis of obesity-linked insulin resistance. In summary, subcutaneous fat differed from visceral fat by immune cell composition and a lower prevalence of CLS both in lean and obese mice. The increase in mast cells in visceral fat of obese mice suggests their role in the pathogenesis of obesity and insulin resistance.
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“Consistent with previous reports, our data confirm a more pronounced accumulation of large Cd68-eGFP+ clusters in the visceral fat compared with in the subcutaneous fat38.”
From A deep-learning framework reveals whole-body perturbations at cell level (2026) · cites this paper as [38]
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Yamada, T., KAMIYA, M., & HIGUCHI, M. (2020) · Animal Science Journal · doi:10.1111/asj.13449 · Cited by 30
Obesity, Inflammation, and Insulin Resistance
Ellies, L. G., Johnson, A., & Olefsky, J. M. (2013) · Springer eBooks · doi:10.1007/978-1-4614-6819-6_1 · Cited by 31
Rodríguez-Mortera, R., Caccavello, R. J., Hermo, R., Garay‐Sevilla, M. E., & Gugliucci, A. (2021) · Antioxidants · doi:10.3390/antiox10050751 · Cited by 30
“These results could be attributed to several factors, including (a) greater chronic inflammation in adolescents with obesity as evidenced by higher levels of IL-6 [17]; (b) greater visceral adipose tissue mass, which has 4-fold more crown-like structures [18] that participate in the expression of IL-6 and in the expre…”
BackgroundAltintas, M. M., Nayer, B., Walford, E. C., Johnson, K. B., Gaidosh, G., Reiser, J., Cruz-Munoz, N. F. D. L., Ortega, L. M., & Nayer, A. (2012) · Lipids in Health and Disease · doi:10.1186/1476-511x-11-21 · Cited by 29
“We also showed that dietinduced obesity in mice is associated with a marked increase in mast cells in the visceral, but not in the subcutaneous, fat depots [11].”
BackgroundMethodInfluentialSelf-citationEller, O. C., Morris, E. M., Thyfault, J. P., & Christianson, J. A. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113000 · Cited by 27
Politis‐Barber, V., Brunetta, H. S., Paglialunga, S., Petrick, H. L., & Holloway, G. P. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00028.2020 · Cited by 28
Thatcher, S. E., Gupte, M., Hatch, N. W., & Cassis, L. A. (2012) · International Journal of Hypertension · doi:10.1155/2012/762094 · Cited by 27
“This finding is consistent with results from studies demonstrating that obesity is associated with more pronounced infiltration of macrophages in visceral compared to subcutaneous adipose tissue [21].”
Dietary cholesterol is essential to mast cell activation and associated obesity and diabetes in mice
Zhang, X., Huang, Q. M., Wang, X., Deng, Z., Li, J., Yan, X., Jauhiainen, M., Metso, J., Libby, P., Liu, J., et al. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.04.006 · Cited by 26
Sphingosine 1-Phosphate Regulates Obesity and Glucose Homeostasis
Kajita, K., Ishii, I., Mori, I., Asano, M., Fuwa, M., & Morita, H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25020932 · Cited by 31
“In obese humans and mice, macrophages accumulate more in VAT than in SAT [37,38,53].”
BackgroundBrunetta, H. S., Politis‐Barber, V., Petrick, H. L., Dennis, K. M. J. H., Kirsh, A. J., Barbeau, P., Nunes, E. A., & Holloway, G. P. (2020) · The Journal of Physiology · doi:10.1113/jp279455 · Cited by 25
“The average of these four sections was taken as the number of CLS/field (Altintas et al. 2011).”
BackgroundImmune cells and metabolic dysfunction
Eheim, A. L., Medříková, D., & Herzig, S. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0403-7 · Cited by 27
“Counts of mast cells in lean adipose tissue are relatively low, but increase with fat accumulation in humans as well as in animal models [36, 37], which suggest a contribution to diet-induced obesity and insulin resistance.”
Mouse model of the adipose organ: the heterogeneous anatomical characteristics
Chun, K. (2021) · Archives of Pharmacal Research · doi:10.1007/s12272-021-01350-6 · Cited by 27
Immunometabolism in Obese Asthmatics: Are We There Yet?
Periyalil, H., Gibson, P. G., & Wood, L. G. (2013) · Nutrients · doi:10.3390/nu5093506 · Cited by 24
“Since mast cells have been implicated in obesity [209] and are a crucial link for expression of”
BackgroundSouza‐Smith, F. M., Siggins, R. W., & Molina, P. E. (2015) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12796 · Cited by 24
“Increased visceral fat mast cells, neutrophil, and macrophage infiltration has been shown to be associated with insulin resistance in rodents (Altintas et al., 2011; Elgazar-Carmon et al., 2008).”
BackgroundImmune and Inflammatory Signaling Pathways in Exercise and Obesity
Krüger, K., Mooren, F. C., Eder, K., & Ringseis, R. (2014) · American Journal of Lifestyle Medicine · doi:10.1177/1559827614552986 · Cited by 26
A macrophage-collagen fragment axis mediates subcutaneous adipose tissue remodeling in mice
Vujičić, M., Broderick, I., Salmantabar, P., Perian, C., Nilsson, J., Sihlbom, C., & Asterholm, I. W. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2313185121 · Cited by 21
“S1 N ), in line with their proposed role in adipose tissue remodeling (18–20).”
BackgroundMacPherson, R. E. K., Gamu, D., Frendo‐Cumbo, S., Castellani, L. N., Kwon, F., Tupling, A. R., & Wright, D. C. (2016) · Obesity · doi:10.1002/oby.21521 · Cited by 23
“percentage of total adipocytes in each image (29).”
BackgroundMast cell deficiency exacerbates inflammatory bowel symptoms in interleukin-10-deficient mice.
Zhang, H., Xue, Y., Wang, H., Huang, Y., Du, ., Yang, Q., & Zhu, M. J. (2014) · PubMed Central · doi:10.3748/wjg.v20.i27.9106 · Cited by 22
Differential Hematopoietic Activity in White Adipose Tissue Depending on its Localization
Luche, É., Sengenès, C., Arnaud, E., Laharrague, P. F., Casteilla, L., & Cousin, B. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.25045 · Cited by 21
Obesity reduces methionine sulphoxide reductase activity in visceral adipose tissue
Uthus, E. O., & Picklo, M. J. (2011) · Free Radical Research · doi:10.3109/10715762.2011.591793 · Cited by 21
“Adipose tissue is a combination of cell types that include stromal vascular cells, adipocytes, mesenchymal stem cells, and in the obese state, elevated levels of macrophages [40,45,46].”
BackgroundYamada, T., KAMIYA, M., HIGUCHI, M., & NAKANISHI, N. (2018) · Journal of Veterinary Medical Science · doi:10.1292/jvms.18-0324 · Cited by 22
“Crown-like structures (CLS), which consist of macrophages surrounding dead adipocytes [2, 7, 31], were also found only in visceral adipose tissue (Fig.”
BackgroundRodríguez-Mortera, R., Caccavello, R. J., Garay‐Sevilla, M. E., & Gugliucci, A. (2020) · Clinica Chimica Acta · doi:10.1016/j.cca.2020.05.014 · Cited by 21
Ishijima, Y., Ohmori, S., & Ohneda, K. (2013) · FEBS Open Bio · doi:10.1016/j.fob.2013.11.004 · Cited by 20
Review of various molecular targets on mast cells and its relation to obesity: A future perspective
Bais, S., Kumari, R., Prashar, Y., & Gill, N. S. (2017) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2017.07.029 · Cited by 20
Aravindhan, V., & Anand, G. (2017) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.17-0236 · Cited by 22
The role of orexin in controlling the activity of the adipo-pancreatic axis
Skrzypski, M., Billert, M., Nowak, K. W., & Strowski, M. Z. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0122 · Cited by 19
Goldstein, N., Kezerle, Y., Gepner, Y., Haim, Y., Pecht, T., Gazit, R., Polischuk, V., Liberty, I. F., Kirshtein, B., Shaco‐Levy, R., et al. (2020) · Cells · doi:10.3390/cells9061508 · Cited by 19
“Interestingly, obesity is associated with increases in MC numbers in all white AT depots besides SAT [7].”
BackgroundObesity, Body Image Dissatisfaction, and Sexual Dysfunction: A Narrative Review
McNabney, S. M. (2022) · Sexes · doi:10.3390/sexes3010002 · Cited by 22
Metadata
- Authors
- Altintas, M. M., Azad, A., Nayer, B., Contreras, G., Zaias, J., Faul, C., Reiser, J., & Nayer, A.
- Affiliations
- University of Miami (US)
- Corresponding author
- Nayer, Ali
- Venue
- Journal of Lipid Research
- Publisher
- Elsevier BV
- Published
- 2011-03
- Volume
- 52
- Issue
- 3
- Pages
- 480-488
- ISSN
- 0022-2275 (ISSN-L)
- PMC
- PMC3035684
- OpenAlex
- W2089000416
- Cited by
- 198
- References
- 48
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 14 · 2023: 6 · 2022: 14 · 2021: 10 · 2020: 17 · 2019: 12 · 2018: 14 · 2017: 19 · 2016: 12 · 2015: 19 · 2014: 13 · 2013: 21 · 2012: 9
- FWCI
- 7.91
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Lipid Research (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- 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
- mast cells, macrophages, crown-like structures, subcutaneous adipose tissue, visceral fat, obesity, adipocyte death, TNF-α, insulin resistance, adipose tissue inflammation, diet-induced obesity, C57BL/6 mice
- MeSH terms
- Animals, Diet, Epididymis, Macrophages, Male, Mast Cells, Mice, Inbred C57BL, Obesity, Thinness, Subcutaneous Fat, Intra-Abdominal Fat, Mice
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