The DOI matches its Crossref record; 43 of the 43 references it cites were found in a registry or an index.
Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice
Open accessAbstract
C57BL/6 (B6) mice subjected to a high-fat diet develop metabolic syndrome with obesity, hyperglycemia, and insulin resistance, whereas 129S6/SvEvTac (129) mice are relatively protected from this disorder because of differences in higher basal energy expenditure in 129 mice, leading to lower weight gain. At a molecular level, this difference correlates with a marked higher expression of uncoupling protein 1 (UCP1) and a higher degree of uncoupling in vitro in mitochondria isolated from muscle of 129 versus B6 mice. Detailed histological examination, however, reveals that this UCP1 is in mitochondria of brown adipocytes interspersed between muscle bundles. Indeed, the number of UCP1-positive brown fat cells in intermuscular fat in 129 mice is >700-fold higher than in B6 mice. These brown fat cells are subject to further up-regulation of UCP1 after stimulation with a β 3 -adrenergic receptor agonist. Thus, ectopic deposits of brown adipose tissue in intermuscular depots with regulatable expression of UCP1 provide a genetically based mechanism of protection from weight gain and metabolic syndrome between strains of mice.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In rodents, small collections of physiologically relevant BAT have been found in the hindlimb in intermuscular adipose tissue and mixed with white fat 86,87.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [86]
In the citing paper
“These systemic brown adipocytes are often found admixed with white fat cells; are more sensitive to β3-adrenergic stimulation and cold exposure; and their thermogenic capacity appears to be regulated by genetic background 86,87,74.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [86]
In the citing paper
“However, the recent identification of brown adipocytes interspersed between muscle bundles in mice 86 opens up the question whether some of the measured NST energy expenditure in skeletal muscle comes from these interspersed brown adipocytes.”
From Cellular bioenergetics as a target for obesity therapy (2010) · cites this paper as [86]
Citations
Cites
Leptin and the regulation of body weight in mammals
Friedman, J. M., & Halaas, J. L. (1998) · Nature · doi:10.1038/27376 · Cited by 5,405
Yamauchi, T., Kamon, J., Waki, H., Terauchi, Y., Kubota, N., Hara, K., Mori, Y., Ide, T., Murakami, K., Tsuboyama-Kasaoka, N., et al. (2001) · Nature Medicine · doi:10.1038/90984 · Cited by 4,915
Obesity and the regulation of energy balance
Spiegelman, B. M., & Flier, J. S. (2001) · Cell · doi:10.1016/s0092-8674(01)00240-9 · Cited by 2,398
Towards a molecular understanding of adaptive thermogenesis
Lowell, B. B., & Spiegelman, B. M. (2000) · Nature · doi:10.1038/35007527 · Cited by 1,630
Thermogenic mechanisms in brown fat.
Nicholls, D. G., & Locke, R. M. (1984) · Physiological Reviews · doi:10.1152/physrev.1984.64.1.1 · Cited by 1,602
Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese
Enerbäck, S., Jacobsson, A., Simpson, E. M., Guerra, C., Yamashita, H., Harper, M.-E., & Kozak, L. P. (1997) · Nature · doi:10.1038/387090a0 · Cited by 1,379
Reduced Rate of Energy Expenditure as a Risk Factor for Body-Weight Gain
Ravussin, E., Lillioja, S., Knowler, W. C., Christin, L., Freymond, D., Abbott, W. G. H., Boyce, V., Howard, B. V., & Bogardus, C. (1988) · New England Journal of Medicine · doi:10.1056/nejm198802253180802 · Cited by 1,215
Development of obesity in transgenic mice after genetic ablation of brown adipose tissue
Lowell, B. B., S-Susulic, V., Hamann, A., Lawitts, J. A., Himms-Hagen, J., Boyer, B. B., Kozak, L. P., & Flier, J. S. (1993) · Nature · doi:10.1038/366740a0 · Cited by 1,075
Hotamışlıgil, G. S., Johnson, R. S., Distel, R. J., Ellis, R., Papaioannou, V. E., & Spiegelman, B. M. (1996) · Science · doi:10.1126/science.274.5291.1377 · Cited by 915
Parental transmission of type 2 diabetes: the Framingham Offspring Study
Meigs, J. B., Cupples, L. A., & Wilson, P. W. (2000) · Diabetes · doi:10.2337/diabetes.49.12.2201 · Cited by 666
Research works printed but not linked: 1
- G Garruti, D Ricquier Int J Obes Relat Metab Disord 16, 383–390 (1992).
Cited by
Sorted by citations
Items 201–284 of 284
Cre Recombinase Strains Used for the Study of Adipose Tissues and Adipocyte Progenitors
Liu, J., Xu, Z., Wu, W.-C., Wang, Y., & Shan, T. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25675 · Cited by 14
Effects of the light–dark cycle on diurnal rhythms of diet-induced thermogenesis in humans
Fukuda, Y., & Morita, T. (2017) · Chronobiology International · doi:10.1080/07420528.2017.1362422 · Cited by 14
Intramuscular adipose tissue: from progenitor to pathology
Jones, H. G., Kopinke, D., & Meyer, G. A. (2025) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00613.2025 · Cited by 16
Pervin, S., Singh, V., Tucker, A., Collazo, J., & Singh, R. (2017) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2017-0036 · Cited by 13
Zhou, H., Chen, C., Hu, H., Jiang, B., Yin, Y., Zhang, K., Shen, M., Wu, S. J., & Wang, Z. (2023) · Bone and Joint Research · doi:10.1302/2046-3758.128.bjr-2022-0309.r2 · Cited by 12
Pani, S., Dey, S., Pati, B., Senapati, U., & Bal, N. C. (2022) · Journal of the Endocrine Society · doi:10.1210/jendso/bvac151 · Cited by 12
Gesta, S., & Kahn, C. R. (2011) · Springer eBooks · doi:10.1007/978-1-4614-0965-6_4 · Cited by 12
Self-citationYang, G., Forrest, R. H.-J., Zhou, H., Hodge, S., & Hickford, J. G. H. (2014) · Journal of Animal Breeding and Genetics · doi:10.1111/jbg.12097 · Cited by 12
Gadéa, É., Thivat, É., Merlin, C., Paulon, R., Kwiatkowski, F., Chadeyras, J. B., Coudert, B. P., Boirie, Y., Morio, B., & Durando, X. (2014) · Nutrition and Cancer · doi:10.1080/01635581.2014.948212 · Cited by 12
Kanamori, Y., Yamada, T., Asano, H., Kida, R., Qiao, Y., Eldaim, M. A. A., Tomonaga, S., Matsui, T., & Funaba, M. (2014) · Journal of Veterinary Medical Science · doi:10.1292/jvms.14-0137 · Cited by 11
Miao, Y., Warner, M. N., & Gustafsson, J.-Α. (2016) · Adipocyte · doi:10.1080/21623945.2016.1142634 · Cited by 11
Molecular physiopathology of obesity-related diseases: multi-organ integration by GRK2
Lucas, E., Cruces‐Sande, M., Briones, A. M., Salaíces, M., Mayor, F., Murga, C., & Vila‐Bedmar, R. (2015) · Archives of Physiology and Biochemistry · doi:10.3109/13813455.2015.1107589 · Cited by 11
Hossin, A. Y., Inafuku, M., & Oku, H. (2019) · Nutrients · doi:10.3390/nu11123053 · Cited by 11
Preconditioning improves muscle regeneration after ischemia–reperfusion injury
Zhang, H., Liu, M., Kim, H. T., Feeley, B. T., & Liu, X. (2020) · Journal of Orthopaedic Research® · doi:10.1002/jor.24909 · Cited by 10
Fink, B. D., Rauckhorst, A. J., Taylor, E. B., Yu, L. P., & Sivitz, W. I. (2021) · FASEB BioAdvances · doi:10.1096/fba.2021-00137 · Cited by 9
Self-citationReversible transdifferentiation in the adipose organ
Cinti, S. (2008) · International Journal of Pediatric Obesity · doi:10.1080/17477160802404665 · Cited by 9
Self-citationParinandi, N. L., & Magalang, U. J. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00022.2013 · Cited by 10
Transcriptional Diversity in Response to Aging Across Skeletal Muscles
Liu, C., Zheng, D., Zhang, R., Li, H., Tong, X., Wu, Y., Zhang, G., Wang, S., Chen, H., Ren, Z., et al. (2025) · Aging Cell · doi:10.1111/acel.70164 · Cited by 9
Liu, Y., Fu, W., Seese, K., Yin, A., & Yin, H. (2019) · The FASEB Journal · doi:10.1096/fj.201802162rr · Cited by 9
Lau, A.-M., Tseng, Y., & Schulz, T. J. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1453-1_19 · Cited by 9
Mechanisms and metabolic consequences of adipocyte progenitor replicative senescence
Lin, T., Mohammad, A., Kolonin, M. G., & Eckel‐Mahan, K. L. (2024) · Immunometabolism · doi:10.1097/in9.0000000000000046 · Cited by 8
Gao, Z., Yu, Y., Eckel‐Mahan, K. L., & Kolonin, M. G. (2025) · Aging Cell · doi:10.1111/acel.14499 · Cited by 7
Sudeep, H., Gouthamchandra, K., Ramanaiah, I., Raj, A., & Shyamprasad, K. (2021) · Pharmacognosy Magazine · doi:10.4103/pm.pm_175_20 · Cited by 7
Parson, J. C., Zhang, X., Craft, C. S., Magee, K. L., Scheller, E. L., & Meyer, G. A. (2023) · Journal of Orthopaedic Research® · doi:10.1002/jor.25627 · Cited by 7
A new era for brown adipose tissue: New insights into brown adipocyte function and differentiation*
Vila‐Bedmar, R., & Fernández‐Veledo, S. (2011) · Archives of Physiology and Biochemistry · doi:10.3109/13813455.2011.560951 · Cited by 7
Gesta, S., & Kahn, C. R. (2017) · Springer eBooks · doi:10.1007/978-3-319-52031-5_5 · Cited by 11
Self-citationNg, D. S. (2013) · Vitamins and hormones · doi:10.1016/b978-0-12-407766-9.00011-0 · Cited by 7
Liver injury after small bowel resection is prevented in obesity-resistant 129S1/SvImJ mice
Onufer, E. J., Han, Y., Courtney, C. M., Steinberger, A. E., Tecos, M. E., Sutton, S., Sescleifer, A. M., Ou, J., Czepielewski, R. S., Randolph, G. J., et al. (2021) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00284.2020 · Cited by 6
Wargent, E. T., Ahmad, S. J. S., Lu, Q. R., Kostenis, E., Arch, J. R. S., & Stocker, C. J. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.698115 · Cited by 7
How brown is brown fat that we can see?
Kolonin, M. G. (2014) · Adipocyte · doi:10.4161/adip.27747 · Cited by 5
Burly1 is a mouse QTL for lean body mass that maps to a 0.8-Mb region of chromosome 2
Lin, C., Fesi, B. D., Marquis, M., Bosak, N. P., Lysenko, A., Koshnevisan, M. A., Duke, F. F., Theodorides, M. L., Nelson, T. M., McDaniel, A. H., et al. (2018) · Mammalian Genome · doi:10.1007/s00335-018-9746-7 · Cited by 5
Role of adipocyte browning in prostate and breast tumor microenvironment
Ku, H., & Cheng, C. (2022) · Tzu Chi Medical Journal · doi:10.4103/tcmj.tcmj_62_22 · Cited by 5
Chu, D., Truong, D. T., Thị, H. V., & Hương, N. T. L. (2022) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-021-04350-8 · Cited by 5
Plasticity of the Adipose Organ
Cinti, S. (2010) · Wiley eBooks · doi:10.1002/9783527629527.ch3 · Cited by 4
Self-citationZhou, Z., Darwal, M. A., Cheng, E. A., Taylor, S. R., Duan, E., & Harding, P. A. (2013) · Growth Factors · doi:10.3109/08977194.2013.840297 · Cited by 4
Asano, H., Kida, R., Muto, K., Nara, T., Kato, K., Hashimoto, O., Kawada, T., Matsui, T., & Funaba, M. (2016) · Cell Biochemistry and Function · doi:10.1002/cbf.3241 · Cited by 4
Hu, Q., Chen, X., Liu, J., Di, W., Lv, S., Tang, L., & Ding, G. (2018) · BioMed Research International · doi:10.1155/2018/3619548 · Cited by 4
Animal Models for Manipulation of Thermogenesis
Fuller‐Jackson, J., Clarke, I. J., & Henry, B. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809468-6.00012-7 · Cited by 4
Regulatory Factors that Reveal Three Distinct Adipocytes : The Brown, the White and the Brite
Waldén, T. B. (2010) · KTH Publication Database DiVA (KTH Royal Institute of Technology) · Cited by 4
Nebivolol in the treatment of metabolic syndrome: Making the fat more brownish
Solak, Y., & Atalay, H. (2009) · Medical Hypotheses · doi:10.1016/j.mehy.2009.10.011 · Cited by 3
Brown and Beige Fat: Therapeutic Potential in Obesity
Meiliana, A., & Wijaya, A. (2014) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v6i2.32 · Cited by 3
Moreno‐Fernández, J., Díaz‐Castro, J., Pulido‐Moran, M., Alférez, M. J. M., Nestares, T., & López‐Aliaga, I. (2016) · European Journal of Nutrition · doi:10.1007/s00394-016-1268-z · Cited by 3
Zhou, H., Wang, Z., Chen, C., Hu, H., Jiang, B., Yin, Y., Zhang, K., Shen, M., & Wu, S. J. (2023) · Orthopaedic Journal of Sports Medicine · doi:10.1177/23259671231170192 · Cited by 2
BMP Signaling in Skeletogenesis
Estrada, K. D., & Lyons, K. M. (2010) · Springer eBooks · doi:10.1007/978-1-84882-822-3_8 · Cited by 2
The effects of early under-nutrition on the development of wBAT and obesity
Kozak, L. P. (2012) · Adipocyte · doi:10.4161/adip.21555 · Cited by 2
Brown Adipose Tissue: A New Target for Antiobesity Therapy
Meiliana, A., & Wijaya, A. (2010) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v2i2.115 · Cited by 2
Sengupta, S., & Avtanski, D. B. (2023) · Contemporary Endocrinology · doi:10.1007/978-3-031-39721-9_2 · Cited by 3
Animal Models for Manipulation of Thermogenesis
Henry, B. A., & Clarke, I. J. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-415894-8.00014-2 · Cited by 2
Tecido Adiposo Marrom e Obesidade em Humanos
Broetto, F. N., & Brito, M. (2012) · Saúde e Pesquisa · Cited by 2
Krase, A. A., Giannaki, C. D., Flouris, A. D., Liakos, D., Stefanidis, I., Karatzaferi, C., & Sakkas, G. K. (2024) · ASAIO Journal · doi:10.1097/mat.0000000000002117 · Cited by 1
Insights into intramuscular adipose–muscle signaling in the diabetic lower extremity
Gui, C., Kamm, D. R., Ferey, J. L. A., Bohnert, K. L., McCormick, J. J., Hastings, M. K., & Meyer, G. A. (2025) · Journal of Clinical & Translational Endocrinology · doi:10.1016/j.jcte.2025.100422 · Cited by 1
Thermogenic brown adipocytes as new targets for the treatment of obesity in humans
Giacobino, J., & Casteilla, L. (2010) · Clinical Lipidology · doi:10.2217/clp.10.5 · Cited by 1
Gómez‐Hernández, A., Perdomo, L., Escribano, Ó., & Benito, M. (2013) · Clínica e Investigación en Arteriosclerosis · doi:10.1016/j.arteri.2012.11.002 · Cited by 1
Adipose Tissue Development, Structure and Function
Sethi, J. K., & Vidal‐Puig, A. (2010) · Springer eBooks · doi:10.1007/978-1-4419-1607-5_3 · Cited by 1
Ballasy, N., Patel, V. B., Hussien, N. I., El-Gohary, O. A., & El, A. (2020) · Benha Medical Journal · doi:10.21608/bmfj.2020.120413 · Cited by 1
Adipocyte Development and Experimental Obesity
ISGANAITIS, E. M., & Patti, M. (2010) · Endocrine updates · doi:10.1007/978-1-4419-7034-3_16 · Cited by 1
Utility of transplantation in studying adipocyte biogenesis and function
Zhang, Y. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.08.022 · Cited by 1
Efeitos da ingestão de capsinóides sobre a adiposidade corporal em ratos Wistar
Cansian, A. C. C. (2017) · doi:10.11606/d.17.2017.tde-30032017-100952 · Cited by 1
Cold and diet induced thermogenesis in humans; Implications for obesity
Wijers, S. L. J. (2011) · Research Publications (Maastricht University) · doi:10.26481/dis.20110407sw
Cinti, S. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1203-2_6
Self-citationNrg4 and Gpr120 signalling in brown fat
Okolo, A. (2015) · doi:10.25560/26287
Cinti, S. (2011)
Self-citationPericardial fat is a nutritionally regulated depot of brown adipose tissue
Ojha, S. (2015) · Nottingham ePrints (University of Nottingham)
Estudo dos efeitos metabólicos e redox de dietas intermitentes
de Freitas, B. C. (2015) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.46.2015.tde-22092015-081157
adipocytes mRNA induction via ERK activation in 10T1/2 UCP1induced by RAW macrophages suppresses
Goto, T., Kawada, T., Sakamoto, T., Takahashi, N., Sawaragi, Y., Naknukool, S., & Yu, R. (2013)
Body composition and metabolic profile of children with end stage liver disease
Kyrana, E. (2017) · Research Portal (King's College London)
Pathways that regulate renal development, fibrosis, and metabolic disease in mouse models
Soofi, A. (2026) · Warwick Research Archive Portal (University of Warwick) · doi:10.82444/warw.33757513
Miyata, T., & Ichimura, A. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.718167526.793488225
(2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3282c3a898
Vettor, R., & Cinti, S. (2009) · Oxidative stress and disease · doi:10.1201/9781420091311.ch1
Self-citationMetabolic Implications of Birth via Cesarean Section in Prairie Vole ( Microtus ochrogaster )Preprint
Starr, A., Ahmed, S., Partie, M. E., & Kenkel, W. M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.21.492929
Salej, L., Camara, H., Chaves, N., Kodani, S. D., Monahan-Earley, R. A., Huntington, S., Cypess, A. M., Asara, J. M., Tseng, Y., James, B. C., et al. (2025) · Journal of the Endocrine Society · doi:10.1210/jendso/bvaf178
Lu, Y., Zhao, M., Peng, Y., He, S., Zhu, X., Hu, C., Xia, G., Zuo, T., Zhang, X., Yun, Y., et al. (2022) · Figshare · doi:10.6084/m9.figshare.21202053
Norris, A. M., Fierman, K. E., Campbell, J., Pitale, R., Shahraj, M., & Kopinke, D. (2024) · Figshare · doi:10.6084/m9.figshare.25929164
Ocobock, C. J., Niclou, A. M., Stenbäck, V., & McElreavy, D. (2025) · Lipids in Health and Disease · doi:10.1186/s12944-025-02838-6
Herrera, C. L. (2015) · theses.fr (ABES) · doi:10.70675/d09d7e9cz079fz4faaz985aza9cd4fc18f18
Implications du microbiote intestinal et de la pectine dans la stéato-hépatite non-alcoolique
Houron, C. (2020) · theses.fr (ABES) · doi:10.70675/282e9d85z4f3dz4f5bz9045zd1ce6da72037
Role of Inflammation in Diet-Induced Obesity: A Dissertation
Kogan, S. (2013) · The Journal of the American Medical Association (JAMA) Network (American Medical Association) · doi:10.13028/m2760c
Metadata
- Authors
- Almind, K., Manieri, M., Sivitz, W. I., Cinti, S., & Kahn, C. R.
- Affiliations
- Joslin Diabetes Center (US)
- Institute of Normal Human Morphology and Anatomy, University of Ancona, 6013 Ancona, Italy; and
- University of Iowa (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-02-13
- Volume
- 104
- Issue
- 7
- Pages
- 2366-2371
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1892979
- OpenAlex
- W2038657829
- Cited by
- 286
- References
- 43
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 4 · 2023: 6 · 2022: 11 · 2021: 10 · 2020: 11 · 2019: 7 · 2018: 16 · 2017: 17 · 2016: 11 · 2015: 18 · 2014: 21 · 2013: 35 · 2012: 20
- FWCI
- 16.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
- Funders
- National Institutes of Health (DK31036)
- National Institute of Diabetes and Digestive and Kidney Diseases (R37DK031036, DK 30136, R01DK031036, DK45935, DK-60837, R01DK045935, R01DK060837)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- intermuscular fat, UCP1, metabolic syndrome, high-fat diet, obesity, insulin resistance, hyperglycemia, energy expenditure, beta3-adrenergic agonists, brown adipocytes, C57BL/6 mice, strain differences, mitochondrial uncoupling
- MeSH terms
- Uncoupling Protein 1, Animals, Adipose Tissue, Brown, Dietary Fats, Energy Metabolism, Ion Channels, Mice, Inbred C57BL, Mice, Inbred Strains, Mitochondria, Muscles, Risk, Weight Gain, Up-Regulation, Mitochondrial Proteins, Metabolic Syndrome, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review