The pesticide chlorpyrifos promotes obesity by inhibiting diet-induced thermogenesis in brown adipose tissue

Wang, Bo; Tsakiridis, Evangelia E.; Zhang, Shuman; Llanos, Andrea; Desjardins, Eric M.; Yabut, Julian M.; Green, Alexander E.; Day, Emily A.; Smith, Brennan K.; Lally, James S. V.; Wu, Jianhan; Raphenya, Amogelang R.; Srinivasan, Krishna A.; McArthur, Andrew G.; Kajimura, Shingo; Patel, Jagdish Suresh; Wade, Michael G.; Morrison, Katherine M.; Holloway, Alison C.; Steinberg, Gregory R.

doi:10.1038/s41467-021-25384-y

The pesticide chlorpyrifos promotes obesity by inhibiting diet-induced thermogenesis in brown adipose tissue

Journal Article · Fri Aug 27 00:00:00 EDT 2021 · Nature Communications

DOI:https://doi.org/10.1038/s41467-021-25384-y· OSTI ID:2469593

Wang, Bo ^[1]; Tsakiridis, Evangelia E. ^[2]; Zhang, Shuman ^[2]; Llanos, Andrea ^[2]; Desjardins, Eric M. ^[2]; Yabut, Julian M. ^[2]; ^[2]; ^[2]; Smith, Brennan K. ^[2]; Lally, James S. V. ^[2]; Wu, Jianhan ^[2]; ^[2]; Srinivasan, Krishna A. ^[2]; ^[2]; ^[3]; ^[4]; Wade, Michael G. ^[5]; ^[2]; ^[2]; ^[2]

McMaster University, Hamilton, ON (Canada); China Agricultural University, Beijing (China)
McMaster University, Hamilton, ON (Canada)
Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA (United States)
University of Idaho, Moscow, ID (United States)
Health Canada, Ottawa, ON (Canada)

Obesity results from a caloric imbalance between energy intake, absorption and expenditure. In both rodents and humans, diet-induced thermogenesis contributes to energy expenditure and involves the activation of brown adipose tissue (BAT). We hypothesize that environmental toxicants commonly used as food additives or pesticides might reduce BAT thermogenesis through suppression of uncoupling protein 1 (UCP1) and this may contribute to the development of obesity. Using a step-wise screening approach, we discover that the organophosphate insecticide chlorpyrifos suppresses UCP1 and mitochondrial respiration in BAT at concentrations as low as 1 pM. In mice housed at thermoneutrality and fed a high-fat diet, chlorpyrifos impairs BAT mitochondrial function and diet-induced thermogenesis, promoting greater obesity, non-alcoholic fatty liver disease (NAFLD) and insulin resistance. This is associated with reductions in cAMP; activation of p38MAPK and AMPK; protein kinases critical for maintaining UCP1 and mitophagy, respectively in BAT. These data indicate that the commonly used pesticide chlorpyrifos, suppresses diet-induced thermogenesis and the activation of BAT, suggesting its use may contribute to the obesity epidemic.

View Accepted Manuscript (DOE)

Research Organization:: Idaho National Laboratory (INL), Idaho Falls, ID (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC07-05ID14517

OSTI ID:: 2469593

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 12; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (81)

GROMACS: Fast, flexible, and free Van Der Spoel, David; Lindahl, Erik; Hess, Berk Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20291	journal	January 2005
AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading Trott, Oleg; Olson, Arthur J. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21334	journal	January 2009
Women have more potential to induce browning of perirenal adipose tissue than men van den Beukel, Johanna C.; Grefhorst, Aldo; Hoogduijn, Martin J. Obesity, Vol. 23, Issue 8 https://doi.org/10.1002/oby.21166	journal	July 2015
Difference in Housing Temperature‐Induced Energy Expenditure Elicits Sex‐Specific Diet‐Induced Metabolic Adaptations in Mice Morris, E. Matthew; Noland, Roberto D.; Allen, Julie A. Obesity, Vol. 28, Issue 10 https://doi.org/10.1002/oby.22925	journal	August 2020
Weight gain associated with chronic exposure to chlorpyrifos in rats Meggs, William J.; Brewer, Kori L. Journal of Medical Toxicology, Vol. 3, Issue 3 https://doi.org/10.1007/BF03160916	journal	September 2007
Effects of sub-chronic in vivo chlorpyrifos exposure on muscarinic receptors and adenylate cyclase of rat striatum Huff, Robin; Abu-Qare, Aqel; Abou-Donia, Mohamed Archives of Toxicology, Vol. 75, Issue 8 https://doi.org/10.1007/s002040100269	journal	October 2001
The polymorphisms of UCP1 genes associated with fat metabolism, obesity and diabetes Jia, Jun-jing; Tian, Yun-bo; Cao, Zhen-hui Molecular Biology Reports, Vol. 37, Issue 3 https://doi.org/10.1007/s11033-009-9550-2	journal	May 2009
Endocrine disruption: molecular interactions of chlorpyrifos and its degradation products with estrogen receptor Hazarika, Jnyandeep; Ganguly, Mausumi; Borgohain, Gargi Structural Chemistry, Vol. 31, Issue 5 https://doi.org/10.1007/s11224-020-01562-4	journal	June 2020
Low doses of chlorpyrifos interfere with spermatogenesis of rats through reduction of sex hormones Peiris, Dinithi Champika; Dhanushka, Thamali Environmental Science and Pollution Research, Vol. 24, Issue 26 https://doi.org/10.1007/s11356-017-9617-x	journal	July 2017
Emerging Role of AMPK in Brown and Beige Adipose Tissue (BAT): Implications for Obesity, Insulin Resistance, and Type 2 Diabetes Desjardins, Eric M.; Steinberg, Gregory R. Current Diabetes Reports, Vol. 18, Issue 10 https://doi.org/10.1007/s11892-018-1049-6	journal	August 2018
Sex-Specific Neurotoxic Effects of Organophosphate Pesticides Across the Life Course Comfort, Nicole; Re, Diane B. Current Environmental Health Reports, Vol. 4, Issue 4 https://doi.org/10.1007/s40572-017-0171-y	journal	October 2017
ThermoMouse: An In Vivo Model to Identify Modulators of UCP1 Expression in Brown Adipose Tissue Galmozzi, Andrea; Sonne, Si B.; Altshuler-Keylin, Svetlana Cell Reports, Vol. 9, Issue 5 https://doi.org/10.1016/j.celrep.2014.10.066	journal	December 2014
Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation Uldry, Marc; Yang, Wenli; St-Pierre, Julie Cell Metabolism, Vol. 3, Issue 5 https://doi.org/10.1016/j.cmet.2006.04.002	journal	May 2006
UCP1 Ablation Induces Obesity and Abolishes Diet-Induced Thermogenesis in Mice Exempt from Thermal Stress by Living at Thermoneutrality Feldmann, Helena M.; Golozoubova, Valeria; Cannon, Barbara Cell Metabolism, Vol. 9, Issue 2 https://doi.org/10.1016/j.cmet.2008.12.014	journal	February 2009
Thermoneutral Housing Accelerates Metabolic Inflammation to Potentiate Atherosclerosis but Not Insulin Resistance Tian, Xiao Yu; Ganeshan, Kirthana; Hong, Cynthia Cell Metabolism, Vol. 23, Issue 1 https://doi.org/10.1016/j.cmet.2015.10.003	journal	January 2016
Lack of Adipocyte AMPK Exacerbates Insulin Resistance and Hepatic Steatosis through Brown and Beige Adipose Tissue Function Mottillo, Emilio P.; Desjardins, Eric M.; Crane, Justin D. Cell Metabolism, Vol. 24, Issue 1 https://doi.org/10.1016/j.cmet.2016.06.006	journal	July 2016
Postprandial Oxidative Metabolism of Human Brown Fat Indicates Thermogenesis U. Din, Mueez; Saari, Teemu; Raiko, Juho Cell Metabolism, Vol. 28, Issue 2 https://doi.org/10.1016/j.cmet.2018.05.020	journal	August 2018
Persistent organic pollutants and diabetes among Inuit in the Canadian Arctic Singh, Kavita; Chan, Hing Man Environment International, Vol. 101 https://doi.org/10.1016/j.envint.2017.02.002	journal	April 2017
Adulthood dietary exposure to a common pesticide leads to an obese-like phenotype and a diabetic profile in apoE3 mice Peris-Sampedro, Fiona; Cabré, Maria; Basaure, Pia Environmental Research, Vol. 142 https://doi.org/10.1016/j.envres.2015.06.036	journal	October 2015
Chlorpyrifos exposure in farmers and urban adults: Metabolic characteristic, exposure estimation, and potential effect of oxidative damage Wang, Lei; Liu, Zhen; Zhang, Junjie Environmental Research, Vol. 149 https://doi.org/10.1016/j.envres.2016.05.011	journal	August 2016
Concentrations of organochlorine pesticides in pooled human serum by age and gender Thomas, Aleysha; Toms, Leisa-Maree Leontjew; Harden, Fiona A. Environmental Research, Vol. 154 https://doi.org/10.1016/j.envres.2016.12.009	journal	April 2017
Joint toxicity of chlorpyrifos and cadmium on the oxidative stress and mitochondrial damage in neuronal cells Xu, Ming-Yuan; Wang, Pan; Sun, Ying-Jian Food and Chemical Toxicology, Vol. 103 https://doi.org/10.1016/j.fct.2017.03.013	journal	May 2017
Chronic chlorpyrifos exposure elicits diet-specific effects on metabolism and the gut microbiome in rats Fang, Bing; Li, Jin Wang; Zhang, Ming Food and Chemical Toxicology, Vol. 111 https://doi.org/10.1016/j.fct.2017.11.001	journal	January 2018
Cold-Inducible Zfp516 Activates UCP1 Transcription to Promote Browning of White Fat and Development of Brown Fat Dempersmier, Jon; Sambeat, Audrey; Gulyaeva, Olga Molecular Cell, Vol. 57, Issue 2 https://doi.org/10.1016/j.molcel.2014.12.005	journal	January 2015
Optimal housing temperatures for mice to mimic the thermal environment of humans: An experimental study Fischer, Alexander W.; Cannon, Barbara; Nedergaard, Jan Molecular Metabolism, Vol. 7 https://doi.org/10.1016/j.molmet.2017.10.009	journal	January 2018
Chronic exposure to chlorpyrifos triggered body weight increase and memory impairment depending on human apoE polymorphisms in a targeted replacement mouse model Peris-Sampedro, Fiona; Basaure, Pia; Reverte, Ingrid Physiology & Behavior, Vol. 144 https://doi.org/10.1016/j.physbeh.2015.03.006	journal	May 2015
Prolonged inorganic arsenic exposure via drinking water impairs brown adipose tissue function in mice Zuo, Zhuo; Liu, Zhiyuan; Gao, Tianchang Science of The Total Environment, Vol. 668 https://doi.org/10.1016/j.scitotenv.2019.03.008	journal	June 2019
Pyrethroid and Organophosphorus Pesticides in Composite Diet Samples from Atlanta, USA Adults Riederer, Anne M.; Hunter Jr., Ronald E.; Hayden, Steven W. Environmental Science & Technology, Vol. 44, Issue 1 https://doi.org/10.1021/es902479h	journal	December 2009
Conserved Binding Mode of Human β ₂ Adrenergic Receptor Inverse Agonists and Antagonist Revealed by X-ray Crystallography Wacker, Daniel; Fenalti, Gustavo; Brown, Monica A. Journal of the American Chemical Society, Vol. 132, Issue 33 https://doi.org/10.1021/ja105108q	journal	August 2010
A role for brown adipose tissue in diet-induced thermogenesis Rothwell, Nancy J.; Stock, Michael J. Nature, Vol. 281, Issue 5726 https://doi.org/10.1038/281031a0	journal	September 1979
Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis Shih, Diana M.; Gu, Lingjie; Xia, Yu-Rong Nature, Vol. 394, Issue 6690 https://doi.org/10.1038/28406	journal	July 1998
Impact of UCP1 and β3AR gene polymorphisms on age-related changes in brown adipose tissue and adiposity in humans Yoneshiro, T.; Ogawa, T.; Okamoto, N. International Journal of Obesity, Vol. 37, Issue 7 https://doi.org/10.1038/ijo.2012.161	journal	October 2012
Aryl hydrocarbon receptor deficiency protects mice from diet-induced adiposity and metabolic disorders through increased energy expenditure Xu, C-X; Wang, C.; Zhang, Z-M International Journal of Obesity, Vol. 39, Issue 8 https://doi.org/10.1038/ijo.2015.63	journal	April 2015
Brown adipose tissue is involved in diet-induced thermogenesis and whole-body fat utilization in healthy humans Hibi, M.; Oishi, S.; Matsushita, M. International Journal of Obesity, Vol. 40, Issue 11 https://doi.org/10.1038/ijo.2016.124	journal	July 2016
PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes Mootha, Vamsi K.; Lindgren, Cecilia M.; Eriksson, Karl-Fredrik Nature Genetics, Vol. 34, Issue 3 https://doi.org/10.1038/ng1180	journal	June 2003
Brown and beige fat: development, function and therapeutic potential Harms, Matthew; Seale, Patrick Nature Medicine, Vol. 19, Issue 10 https://doi.org/10.1038/nm.3361	journal	September 2013
Thermoneutral housing exacerbates nonalcoholic fatty liver disease in mice and allows for sex-independent disease modeling Giles, Daniel A.; Moreno-Fernandez, Maria E.; Stankiewicz, Traci E. Nature Medicine, Vol. 23, Issue 7 https://doi.org/10.1038/nm.4346	journal	June 2017
Global obesity: trends, risk factors and policy implications Malik, Vasanti S.; Willett, Walter C.; Hu, Frank B. Nature Reviews Endocrinology, Vol. 9, Issue 1 https://doi.org/10.1038/nrendo.2012.199	journal	November 2012
Adipose tissue browning and metabolic health Bartelt, Alexander; Heeren, Joerg Nature Reviews Endocrinology, Vol. 10, Issue 1 https://doi.org/10.1038/nrendo.2013.204	journal	October 2013
Warming the mouse to model human diseases Ganeshan, Kirthana; Chawla, Ajay Nature Reviews Endocrinology, Vol. 13, Issue 8 https://doi.org/10.1038/nrendo.2017.48	journal	May 2017
Sex‐Dependent Dietary Obesity, Induction of UCPs, and Leptin Expression in Rat Adipose Tissues Rodríguez, Ana M.; Quevedo‐Coli, Santiago; Roca, Pilar Obesity Research, Vol. 9, Issue 9 https://doi.org/10.1038/oby.2001.75	journal	September 2001
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0201-4	journal	August 2019
Arsenite exposure suppresses adipogenesis, mitochondrial biogenesis and thermogenesis via autophagy inhibition in brown adipose tissue Bae, Jiyoung; Jang, Yura; Kim, Heejeong Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-50965-9	journal	October 2019
Impact of pesticide exposure on adipose tissue development and function Gutgesell, Robert M.; Tsakiridis, Evangelia E.; Jamshed, Shanza Biochemical Journal, Vol. 477, Issue 14 https://doi.org/10.1042/BCJ20200324	journal	July 2020
The UCP1 Gene Polymorphism A-3826G in Relation to DM2 and Body Composition in Czech Population Sramkova, D.; Krejbichova, S.; Vcelak, J. Experimental and Clinical Endocrinology & Diabetes, Vol. 115, Issue 05 https://doi.org/10.1055/s-2007-977732	journal	May 2007
Functional Brown Adipose Tissue in Healthy Adults Virtanen, Kirsi A.; Lidell, Martin E.; Orava, Janne New England Journal of Medicine, Vol. 360, Issue 15 https://doi.org/10.1056/NEJMoa0808949	journal	April 2009
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles Subramanian, A.; Tamayo, P.; Mootha, V. K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 43, p. 15545-15550 https://doi.org/10.1073/pnas.0506580102	journal	September 2005
Mapping of human brown adipose tissue in lean and obese young men Leitner, Brooks P.; Huang, Shan; Brychta, Robert J. Proceedings of the National Academy of Sciences, Vol. 114, Issue 32 https://doi.org/10.1073/pnas.1705287114	journal	July 2017
UCP1 deficiency causes brown fat respiratory chain depletion and sensitizes mitochondria to calcium overload-induced dysfunction Kazak, Lawrence; Chouchani, Edward T.; Stavrovskaya, Irina G. Proceedings of the National Academy of Sciences, Vol. 114, Issue 30 https://doi.org/10.1073/pnas.1705406114	journal	June 2017
Are Women More Vulnerable to Environmental Pollution? Butter, Maureen E. Journal of Human Ecology, Vol. 20, Issue 3 https://doi.org/10.1080/09709274.2006.11905931	journal	November 2006
Chemical Toxins: A Hypothesis to Explain the Global Obesity Epidemic Baillie-Hamilton, Paula F. The Journal of Alternative and Complementary Medicine, Vol. 8, Issue 2 https://doi.org/10.1089/107555302317371479	journal	April 2002
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Mice Treated with Chlorpyrifos or Chlorpyrifos Oxon Have Organophosphorylated Tubulin in the Brain and Disrupted Microtubule Structures, Suggesting a Role for Tubulin in Neurotoxicity Associated with Exposure to Organophosphorus Agents Jiang, Wei; Duysen, Ellen G.; Hansen, Heidi Toxicological Sciences, Vol. 115, Issue 1 https://doi.org/10.1093/toxsci/kfq032	journal	February 2010
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Developmental neurotoxicity of the organophosphorus insecticide chlorpyrifos: from clinical findings to preclinical models and potential mechanisms Burke, Richard D.; Todd, Spencer W.; Lumsden, Eric Journal of Neurochemistry, Vol. 142, Issue S2 https://doi.org/10.1111/jnc.14077	journal	August 2017
βAR Signaling Required for Diet-Induced Thermogenesis and Obesity Resistance Bachman, Eric S.; Dhillon, Harveen; Zhang, Chen-Yu Science, Vol. 297, Issue 5582 https://doi.org/10.1126/science.1073160	journal	August 2002
Systemic pan-AMPK activator MK-8722 improves glucose homeostasis but induces cardiac hypertrophy Myers, Robert W.; Guan, Hong-Ping; Ehrhart, Juliann Science, Vol. 357, Issue 6350 https://doi.org/10.1126/science.aah5582	journal	July 2017
Molecular basis for high-affinity agonist binding in GPCRs Warne, Tony; Edwards, Patricia C.; Doré, Andrew S. Science, Vol. 364, Issue 6442 https://doi.org/10.1126/science.aau5595	journal	May 2019
Chronic arsenic exposure impairs adaptive thermogenesis in male C57BL/6J mice Castriota, Felicia; Zushin, Peter-James H.; Sanchez, Sylvia S. American Journal of Physiology-Endocrinology and Metabolism, Vol. 318, Issue 5 https://doi.org/10.1152/ajpendo.00282.2019	journal	May 2020
Intact innervation is essential for diet-induced recruitment of brown adipose tissue Fischer, Alexander W.; Schlein, Christian; Cannon, Barbara American Journal of Physiology-Endocrinology and Metabolism, Vol. 316, Issue 3 https://doi.org/10.1152/ajpendo.00443.2018	journal	March 2019
Adrenergic control of lipolysis in women compared with men Schmidt, Stacy L.; Bessesen, Daniel H.; Stotz, Sarah Journal of Applied Physiology, Vol. 117, Issue 9 https://doi.org/10.1152/japplphysiol.00003.2014	journal	November 2014
Cold acclimation recruits human brown fat and increases nonshivering thermogenesis van der Lans, Anouk A. J. J.; Hoeks, Joris; Brans, Boudewijn Journal of Clinical Investigation, Vol. 123, Issue 8 https://doi.org/10.1172/JCI68993	journal	July 2013
A model of chlorpyrifos distribution and its biochemical effects on the liver and kidneys of rats Tanvir, Em; Afroz, R.; Chowdhury, Maz Human & Experimental Toxicology, Vol. 35, Issue 9 https://doi.org/10.1177/0960327115614384	journal	July 2016
Meta-analyses between 18 candidate genetic markers and overweight/obesity Tang, Linlin; Ye, Huadan; Hong, Qingxiao Diagnostic Pathology, Vol. 9, Issue 1 https://doi.org/10.1186/1746-1596-9-56	journal	March 2014
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Organophosphorus pesticide chlorpyrifos intake promotes obesity and insulin resistance through impacting gut and gut microbiota Liang, Yiran; Zhan, Jing; Liu, Donghui Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0635-4	journal	February 2019
The −3826 A→G Variant of the Uncoupling Protein-1 Gene Diminishes Postprandial Thermogenesis after a High Fat Meal in Healthy Boys Nagai, Narumi; Sakane, Naoki; Ueno, Linda Massako The Journal of Clinical Endocrinology & Metabolism, Vol. 88, Issue 12 https://doi.org/10.1210/jc.2003-030672	journal	December 2003
Outdoor Temperature, Age, Sex, Body Mass Index, and Diabetic Status Determine the Prevalence, Mass, and Glucose-Uptake Activity of 18F-FDG-Detected BAT in Humans Ouellet, Veronique; Routhier-Labadie, Annick; Bellemare, William The Journal of Clinical Endocrinology & Metabolism, Vol. 96, Issue 1 https://doi.org/10.1210/jc.2010-0989	journal	January 2011
Critical periods for chlorpyrifos-induced developmental neurotoxicity: alterations in adenylyl cyclase signaling in adult rat brain regions after gestational or neonatal exposure. Meyer, Armando; Seidler, Frederic J.; Aldridge, Justin E. Environmental Health Perspectives, Vol. 112, Issue 3 https://doi.org/10.1289/ehp.6755	journal	March 2004
Predicting peak spectral sensitivities of vertebrate cone visual pigments using atomistic molecular simulations Patel, Jagdish Suresh; Brown, Celeste J.; Ytreberg, F. Marty PLOS Computational Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pcbi.1005974	journal	January 2018
Perinatal Exposure of Mice to the Pesticide DDT Impairs Energy Expenditure and Metabolism in Adult Female Offspring La Merrill, Michele; Karey, Emma; Moshier, Erin PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0103337	journal	July 2014
Uncoupling protein-1 deficiency promotes brown adipose tissue inflammation and ER stress Bond, Laura M.; Burhans, Maggie S.; Ntambi, James M. PLOS ONE, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pone.0205726	journal	November 2018
Thermoneutrality decreases thermogenic program and promotes adiposity in high-fat diet-fed mice Cui, Xin; Nguyen, Ngoc Ly T.; Zarebidaki, Eleen Physiological Reports, Vol. 4, Issue 10 https://doi.org/10.14814/phy2.12799	journal	May 2016
High Incidence of Metabolically Active Brown Adipose Tissue in Healthy Adult Humans Saito, Masayuki; Okamatsu-Ogura, Yuko; Matsushita, Mami Diabetes, Vol. 58, Issue 7 https://doi.org/10.2337/db09-0530	journal	April 2009
Cellular Energy Sensing and Metabolism—Implications for Treating Diabetes: The 2017 Outstanding Scientific Achievement Award Lecture Steinberg, Gregory R. Diabetes, Vol. 67, Issue 2 https://doi.org/10.2337/dbi17-0039	journal	January 2018
History of the Obesogen Field: Looking Back to Look Forward Heindel, Jerrold J. Frontiers in Endocrinology, Vol. 10 https://doi.org/10.3389/fendo.2019.00014	journal	January 2019
Endocrine-Mediated Mechanisms of Metabolic Disruption and New Approaches to Examine the Public Health Threat Kassotis, Christopher D.; Stapleton, Heather M. Frontiers in Endocrinology, Vol. 10 https://doi.org/10.3389/fendo.2019.00039	journal	February 2019
Environmental Pollutants Effect on Brown Adipose Tissue Di Gregorio, Ilaria; Busiello, Rosa Anna; Burgos Aceves, Mario Alberto Frontiers in Physiology, Vol. 9 https://doi.org/10.3389/fphys.2018.01891	journal	January 2019
Brown adipose tissue activity after a high-calorie meal in humans Vosselman, Maarten J.; Brans, Boudewijn; van der Lans, Anouk AJJ The American Journal of Clinical Nutrition, Vol. 98, Issue 1 https://doi.org/10.3945/ajcn.113.059022	journal	July 2013
Can a small-changes approach help address the obesity epidemic? A report of the Joint Task Force of the American Society for Nutrition, Institute of Food Technologists, and International Food Information Council Hill, James O. The American Journal of Clinical Nutrition, Vol. 89, Issue 2 https://doi.org/10.3945/ajcn.2008.26566	journal	February 2009
Organophosphorus pesticide chlorpyrifos intake promotes obesity and insulin resistance through impacting gut and gut microbiota Liang, Yiran; Zhan, Jing; Liu, Donghui figshare https://doi.org/10.6084/m9.figshare.c.4397441	collection	January 2019

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