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CCE and EODF as two distinct non-shivering thermogenesis models inducing weight loss

  • Integrative Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Increasing energy expenditure and reducing energy intake are considered two classical methods to induce weight loss. Weight loss through physical methods instead of drugs has been a popular research topic nowadays, but how these methods function in adipose and cause weight loss in body remains unclear. In this study, we set up chronic cold exposure (CCE) and every-other-day fasting (EODF) as two distinct models in long-term treatment to induce weight loss, recording their own characteristics in changes of body temperature and metabolism. We investigated the different types of non-shivering thermogenesis induced by CCE and EODF in white and brown adipose tissue through sympathetic nervous system (SNS), creatine-driven pathway, and fibroblast growth factor 21 (FGF21)–adiponectin axis. CCE and EODF could reduce body weight, lipid composition, increase insulin sensitivity, promote the browning of white fat, and increase the expression of endogenous FGF21 in adipose tissue. CCE stimulated the SNS and increased the thermogenic function of brown fat, and EODF increased the activity of protein kinase in white fat. In this study, we further explained the thermogenic mechanism function in adipose and metabolic benefits of the stable phenotype through physical treatments used for weight loss, providing more details for the literature on weight loss models.

Graphical Abstract

The influence on metabolism, non-shivering thermogenesis, endogenous FGF21, and ADPN changes in the long-term treatment of distinct methods (increasing energy expenditure and decreasing energy intake) to induce weight loss

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Data Availability

The data are available from the corresponding author on reasonable request

Abbreviations

CCE:

Chronic cold exposure

EODF:

Every-other-day fasting

UCP-1:

Uncoupling protein-1

iBAT:

Interscapular brown adipose tissue

eWAT:

Epididymal white adipose tissue

NADR:

Noradrenaline

SNS:

Sympathetic nervous system

FGF21:

Fibroblast growth factor 21

ADPN:

Adiponectin

TC:

Total cholesterol

TG:

Triglycerides

CK:

Creatine kinase

FFA:

Free fatty acids

References

  1. Abu-Odeh M, Zhang Y, Reilly SM, Ebadat N, Keinan O, Valentine JM, Hafezi-Bakhtiari M, Ashayer H, Mamoun L, Zhou X, Zhang J, Yu RT, Dai Y, Liddle C, Downes M, Evans RM, Kliewer SA, Mangelsdorf DJ, Saltiel AR (2021) FGF21 promotes thermogenic gene expression as an autocrine factor in adipocytes. Cell Rep 35:109331. https://doi.org/10.1016/j.celrep.2021.109331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Anson RM, Guo Z, de Cabo R, Iyun T, Rios M, Hagepanos A, Ingram DK, Lane MA, Mattson MP (2003) Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci U S A 100:6216–6220. https://doi.org/10.1073/pnas.1035720100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bal NC, Maurya SK, Pani S, Sethy C, Banerjee A, Das S, Patnaik S, Kundu CN (2017) Mild cold induced thermogenesis: are BAT and skeletal muscle synergistic partners? Biosci Rep 37:BSR20171087. https://doi.org/10.1042/BSR20171087

  4. Bray GA, Fruhbeck G, Ryan DH, Wilding JPH (2016) Management of obesity. Lancet 387:1947–1956. https://doi.org/10.1016/s0140-6736(16)00271-3

    Article  PubMed  Google Scholar 

  5. Byun S, Seok S, Kim Y-C, Zhang Y, Yau P, Iwamori N, Xu HE, Ma J, Kemper B, Kemper JK (2020) Fasting-induced FGF21 signaling activates hepatic autophagy and lipid degradation via JMJD3 histone demethylase. Nat Commun 11:807. https://doi.org/10.1038/s41467-020-14384-z

  6. Camilleri M, Acosta A (2018) Combination Therapies for Obesity. Metab Syndr Relat Disord 16:390–394. https://doi.org/10.1089/met.2018.0075

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chang SH, Song NJ, Choi JH, Yun UJ, Park KW (2019) Mechanisms underlying UCP1 dependent and independent adipocyte thermogenesis. Obes Rev 20:241–251. https://doi.org/10.1111/obr.12796

    Article  CAS  PubMed  Google Scholar 

  8. Chao AM, Quigley KM, Wadden TA (2021) Dietary interventions for obesity: clinical and mechanistic findings. J Clin Investig 131:e140065. https://doi.org/10.1172/jci140065

  9. Chartoumpekis DV, Habeos IG, Ziros PG, Psyrogiannis AI, Kyriazopoulou VE, Papavassiliou AG (2011) Brown adipose tissue responds to cold and adrenergic stimulation by induction of FGF21. Mol Med 17:736–740. https://doi.org/10.2119/molmed.2011.00075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chatterjee S, Khunti K, Davies MJ (2017) Type 2 diabetes. Lancet 389:2239–2251. https://doi.org/10.1016/s0140-6736(17)30058-2

    Article  CAS  PubMed  Google Scholar 

  11. Chen YC, Yu YH (2018) The potential of brown adipogenesis and browning in porcine bone marrow-derived mesenchymal stem cells. J Anim Sci 96:3635–3644. https://doi.org/10.1093/jas/sky230

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chen M, Chen H, Nguyen A, Gupta D, Wang J, Lai EW, Pacak K, Gavrilova O, Quon MJ, Weinstein LS (2010) G(s)alpha deficiency in adipose tissue leads to a lean phenotype with divergent effects on cold tolerance and diet-induced thermogenesis. Cell Metab 11:320–330. https://doi.org/10.1016/j.cmet.2010.02.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chouchani ET, Kazak L, Spiegelman BM (2019) New Advances in Adaptive Thermogenesis: UCP1 and Beyond. Cell Metab 29:27–37. https://doi.org/10.1016/j.cmet.2018.11.002

    Article  CAS  PubMed  Google Scholar 

  14. Cohen P, Kajimura S (2021) The cellular and functional complexity of thermogenic fat. Nat Rev Mol Cell Biol 22:393–409. https://doi.org/10.1038/s41580-021-00350-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Conway B, Rene A (2004) Obesity as a disease: no lightweight matter. Obes Rev 5:145–151. https://doi.org/10.1111/j.1467-789X.2004.00144.x

    Article  CAS  PubMed  Google Scholar 

  16. Desautels M, Dulos RA (1988) Effects of repeated cycles of fasting-refeeding on brown adipose tissue composition in mice. Am J Physiol 255:E120–E128. https://doi.org/10.1152/ajpendo.1988.255.2.E120

    Article  CAS  PubMed  Google Scholar 

  17. Dickson LM, Gandhi S, Layden BT, Cohen RN, Wicksteed B (2016) Protein kinase A induces UCP1 expression in specific adipose depots to increase energy expenditure and improve metabolic health. Am J Physiol Regul Integr Comp Physiol 311:R79-88. https://doi.org/10.1152/ajpregu.00114.2016

    Article  PubMed  PubMed Central  Google Scholar 

  18. Divakaruni AS, Humphrey DM, Brand MD (2012) Fatty acids change the conformation of uncoupling protein 1 (UCP1). J Biol Chem 287:36845–36853. https://doi.org/10.1074/jbc.M112.381780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fanti M, Mishra A, Longo VD, Brandhorst S (2021) Time-restricted eating, intermittent fasting, and fasting-mimicking diets in weight loss. Curr Obes Rep 10:70–80. https://doi.org/10.1007/s13679-021-00424-2

    Article  PubMed  Google Scholar 

  20. Fedorenko A, Lishko PV, Kirichok Y (2012) Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151:400–413. https://doi.org/10.1016/j.cell.2012.09.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fisher FM, Maratos-Flier E (2016) Understanding the physiology of FGF21. Annu Rev Physiol 78:223–241. https://doi.org/10.1146/annurev-physiol-021115-105339

    Article  CAS  PubMed  Google Scholar 

  22. Fisher FM, Kleiner S, Douris N, Fox EC, Mepani RJ, Verdeguer F, Wu J, Kharitonenkov A, Flier JS, Maratos-Flier E, Spiegelman BM (2012) FGF21 regulates PGC-1alpha and browning of white adipose tissues in adaptive thermogenesis. Genes Dev 26:271–281. https://doi.org/10.1101/gad.177857.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gao Y, Qimuge NR, Qin J, Cai R, Li X, Chu GY, Pang WJ, Yang GS (2018) Acute and chronic cold exposure differentially affects the browning of porcine white adipose tissue. Animal 12:1435–1441. https://doi.org/10.1017/s1751731117002981

    Article  CAS  PubMed  Google Scholar 

  24. Golozoubova V, Cannon B, Nedergaard J (2006) UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. American journal of physiology. Endocrinol Metab 291:E350–E357. https://doi.org/10.1152/ajpendo.00387.2005

    Article  CAS  Google Scholar 

  25. Gotthardt JD, Verpeut JL, Yeomans BL, Yang JA, Yasrebi A, Roepke TA, Bello NT (2016) Intermittent fasting promotes fat loss with lean mass retention, increased hypothalamic norepinephrine content, and increased neuropeptide Y gene expression in diet-induced obese male mice. Endocrinology 157:679–691. https://doi.org/10.1210/en.2015-1622

    Article  CAS  PubMed  Google Scholar 

  26. Grigg G, Nowack J, Bicudo J, Bal NC, Woodward HN, Seymour RS (2022) Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians. Biol Rev Camb Philos Soc 97:766–801. https://doi.org/10.1111/brv.12822

    Article  CAS  PubMed  Google Scholar 

  27. Harms M, Seale P (2013) Brown and beige fat: development, function and therapeutic potential. Nat Med 19:1252–1263. https://doi.org/10.1038/nm.3361

    Article  CAS  PubMed  Google Scholar 

  28. Hayashi M, Nagasaka T (1983) Suppression of norepinephrine-induced thermogenesis in brown adipose tissue by fasting. Am J Physiol 245:E582–E586. https://doi.org/10.1152/ajpendo.1983.245.6.E582

    Article  CAS  PubMed  Google Scholar 

  29. Holland WL, Adams AC, Brozinick JT, Bui HH, Miyauchi Y, Kusminski CM, Bauer SM, Wade M, Singhal E, Cheng CC, Volk K, Kuo MS, Gordillo R, Kharitonenkov A, Scherer PE (2013) An FGF21-adiponectin-ceramide axis controls energy expenditure and insulin action in mice. Cell Metab 17:790–797. https://doi.org/10.1016/j.cmet.2013.03.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Hondares E, Rosell M, Gonzalez FJ, Giralt M, Iglesias R, Villarroya F (2010) Hepatic FGF21 expression is induced at birth via PPAR alpha in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab 11:206–212. https://doi.org/10.1016/j.cmet.2010.02.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hondares E, Iglesias R, Giralt A, Gonzalez FJ, Giralt M, Mampel T, Villarroya F (2011) Thermogenic activation induces FGF21 expression and release in brown adipose tissue. J Biol Chem 286:12983–12990. https://doi.org/10.1074/jbc.M110.215889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ivanova YM (1985) Blondin DP (2021) Examining the benefits of cold exposure as a therapeutic strategy for obesity and type 2 diabetes. J Appl Physiol 130:1448–1459. https://doi.org/10.1152/japplphysiol.00934.2020

    Article  CAS  Google Scholar 

  33. Izumiya Y, Bina HA, Ouchi N, Akasaki Y, Kharitonenkov A, Walsh K (2008) FGF21 is an Akt-regulated myokine. FEBS Lett 582:3805–3810. https://doi.org/10.1016/j.febslet.2008.10.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Joslin PMN, Bell RK, Swoap SJ (2017) Obese mice on a high-fat alternate-day fasting regimen lose weight and improve glucose tolerance. J Anim Physiol Anim Nutr 101:1036–1045. https://doi.org/10.1111/jpn.12546

    Article  CAS  Google Scholar 

  35. Kazak L, Chouchani ET, Jedrychowski MP, Erickson BK, Shinoda K, Cohen P, Vetrivelan R, Lu GZ, Laznik-Bogoslavski D, Hasenfuss SC, Kajimura S, Gygi SP, Spiegelman BM (2015) A creatine-driven substrate cycle enhances energy expenditure and thermogenesis in beige fat. Cell 163:643–655. https://doi.org/10.1016/j.cell.2015.09.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kazak L, Rahbani JF, Samborska B, Lu GZ, Jedrychowski MP, Lajoie M, Zhang S, Ramsay L, Dou FY, Tenen D, Chouchani ET, Dzeja P, Watson IR, Tsai L, Rosen ED, Spiegelman BM (2019) Ablation of adipocyte creatine transport impairs thermogenesis and causes diet-induced obesity. Nat Metab 1:360–370. https://doi.org/10.1038/s42255-019-0035-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kliewer SA, Mangelsdorf DJ (2019) A dozen years of discovery: insights into the physiology and pharmacology of FGF21. Cell Metab 29:246–253. https://doi.org/10.1016/j.cmet.2019.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Koenen M, Hill MA, Cohen P, Sowers JR (2021) Obesity, adipose tissue and vascular dysfunction. Circ Res 128:951–968. https://doi.org/10.1161/circresaha.121.318093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Krentz AJ, Fujioka K, Hompesch M (2016) Evolution of pharmacological obesity treatments: focus on adverse side-effect profiles. Diabetes Obes Metab 18:558–570. https://doi.org/10.1111/dom.12657

    Article  CAS  PubMed  Google Scholar 

  40. Lee P, Brychta RJ, Linderman J, Smith S, Chen KY, Celi FS (2013) Mild cold exposure modulates fibroblast growth factor 21 (FGF21) diurnal rhythm in humans: relationship between FGF21 levels, lipolysis, and cold-induced thermogenesis. J Clin Endocrinol Metab 98:E98–E102. https://doi.org/10.1210/jc.2012-3107

    Article  CAS  PubMed  Google Scholar 

  41. Lee P, Linderman JD, Smith S, Brychta RJ, Wang J, Idelson C, Perron RM, Werner CD, Phan GQ, Kammula US, Kebebew E, Pacak K, Chen KY, Celi FS (2014) Irisin and FGF21 Are cold-induced endocrine activators of brown fat function in humans. Cell Metab 19:302–309. https://doi.org/10.1016/j.cmet.2013.12.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Li G, Xie C, Lu S, Nichols RG, Tian Y, Li L, Patel D, Ma Y, Brocker CN, Yan T, Krausz KW, Xiang R, Gavrilova O, Patterson AD, Gonzalez FJ (2017) Intermittent fasting promotes white adipose browning and decreases obesity by shaping the gut microbiota. Cell Metab 26:672–685. https://doi.org/10.1016/j.cmet.2017.08.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. MacPherson REK, Gamu D, Frendo-Cumbo S, Castellani L, Kwon F, Tupling AR, Wright DC (2016) Sarcolipin Knockout Mice Fed a High-Fat Diet Exhibit Altered Indices of Adipose Tissue Inflammation and Remodeling. Obesity 24:1499–1505. https://doi.org/10.1002/oby.21521

    Article  CAS  PubMed  Google Scholar 

  44. Marlatt KL, Ravussin E (2017) Brown adipose tissue: an update on recent findings. Curr Obes Rep 6:389–396. https://doi.org/10.1007/s13679-017-0283-6

    Article  PubMed  PubMed Central  Google Scholar 

  45. Maurya SK, Periasamy M (2015) Sarcolipin is a novel regulator of muscle metabolism and obesity. Pharmacol Res 102:270–275. https://doi.org/10.1016/j.phrs.2015.10.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Meizoso-Huesca A, Pearce L, Barclay CJ, Launikonis BS (2022) Ca(2+) leak through ryanodine receptor 1 regulates thermogenesis in resting skeletal muscle. Proc Natl Acad Sci U S A 119. https://doi.org/10.1073/pnas.2119203119

  47. Oishi K, Sakamoto K, Konishi M, Murata Y, Itoh N, Sei H (2010) FGF21 is dispensable for hypothermia induced by fasting in mice. Neuro Endocrinol Lett 31:198–202

    CAS  PubMed  Google Scholar 

  48. Olsen MK, Johannessen H, Ramracheya R, Zhao CM, Chen D (2018) New approaches for weight loss: experiments using animal models. Curr Pharm Des 24:1926–1935. https://doi.org/10.2174/1381612824666180614075412

    Article  CAS  PubMed  Google Scholar 

  49. Pani S, Dey S, Pati B, Senapati U, Bal NC (2022) Brown to white fat transition overlap with skeletal muscle during development of larger mammals: is it a coincidence? J Endocr Soc 6:bvac151. https://doi.org/10.1210/jendso/bvac151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Periasamy M, Herrera JL, Reis FCG (2017) Skeletal muscle thermogenesis and its role in whole body energy metabolism. Diabetes Metab J 41:327–336. https://doi.org/10.4093/dmj.2017.41.5.327

    Article  PubMed  PubMed Central  Google Scholar 

  51. Periasamy M, Maurya SK, Sahoo SK, Singh S, Reis FCG, Bal NC (2017) Role of SERCA pump in muscle thermogenesis and metabolism. Compr Physiol 7:879–890. https://doi.org/10.1002/cphy.c160030

    Article  PubMed  Google Scholar 

  52. Raschke S, Eckel J (2013) Adipo-myokines: two sides of the same coin–mediators of inflammation and mediators of exercise. Mediators Inflamm 2013:320724. https://doi.org/10.1155/2013/320724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Reinisch I, Schreiber R, Prokesch A (2020) Regulation of thermogenic adipocytes during fasting and cold. Mol Cell Endocrinol 512:110869. https://doi.org/10.1016/j.mce.2020.110869

    Article  CAS  PubMed  Google Scholar 

  54. Rosen ED, Spiegelman BM (2014) What we talk about when we talk about fat. Cell 156:20–44. https://doi.org/10.1016/j.cell.2013.12.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rowland LA, Bal NC, Kozak LP, Periasamy M (2015) Uncoupling protein 1 and sarcolipin are required to maintain optimal thermogenesis, and loss of both systems compromises survival of mice under cold stress. J Biol Chem 290:12282–12289. https://doi.org/10.1074/jbc.M115.637603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Saito M, Matsushita M, Yoneshiro T, Okamatsu-Ogura Y (2020) Brown Adipose Tissue, Diet-Induced Thermogenesis, and Thermogenic Food Ingredients: From Mice to Men. Front Endocrinol (Lausanne) 11:222. https://doi.org/10.3389/fendo.2020.00222

  57. Scheja L, Heeren J (2019) The endocrine function of adipose tissues in health and cardiometabolic disease. Nat Rev Endocrinol 15:507–524. https://doi.org/10.1038/s41574-019-0230-6

    Article  CAS  PubMed  Google Scholar 

  58. Shapiro B, Wertheimer E (1948) The synthesis of fatty acids in adipose tissue in vitro. J Biol Chem 173:725–8

    Article  CAS  PubMed  Google Scholar 

  59. Sivitz WI, Fink BD, Donohoue PA (1999) Fasting and leptin modulate adipose and muscle uncoupling protein: divergent effects between messenger ribonucleic acid and protein expression. Endocrinology 140:1511–1519. https://doi.org/10.1210/en.140.4.1511

    Article  CAS  PubMed  Google Scholar 

  60. Stanford KI, Goodyear LJ (2018) Muscle-adipose tissue cross talk. Cold Spring Harb Perspect Med 8:a029801. https://doi.org/10.1101/cshperspect.a029801

  61. Sveidahl Johansen O, Ma T, Hansen JB, Markussen LK, Schreiber R, Reverte-Salisa L, Dong H, Christensen DP, Sun W, Gnad T, Karavaeva I, Nielsen TS, Kooijman S, Cero C, Dmytriyeva O, Shen Y, Razzoli M, O’Brien SL, Kuipers EN, Nielsen CH, Orchard W, Willemsen N, Jespersen NZ, Lundh M, Sustarsic EG, Hallgren CM, Frost M, McGonigle S, Isidor MS, Broholm C, Pedersen O, Hansen JB, Grarup N, Hansen T, Kjaer A, Granneman JG, Babu MM, Calebiro D, Nielsen S, Ryden M, Soccio R, Rensen PCN, Treebak JT, Schwartz TW, Emanuelli B, Bartolomucci A, Pfeifer A, Zechner R, Scheele C, Mandrup S, Gerhart-Hines Z (2021) Lipolysis drives expression of the constitutively active receptor GPR3 to induce adipose thermogenesis. Cell 184:3502-3518 e33. https://doi.org/10.1016/j.cell.2021.04.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wang S, Gopinath T, Larsen EK, Weber DK, Walker C, Uddigiri VR, Mote KR, Sahoo SK, Periasamy M, Veglia G (2021) Structural basis for sarcolipin’s regulation of muscle thermogenesis by the sarcoplasmic reticulum Ca2+-ATPase. Sci Adv 7:eabi7154. https://doi.org/10.1126/sciadv.abi7154

  63. Willoughby D, Hewlings S, Kalman D (2018) Body Composition Changes in Weight Loss: Strategies and Supplementation for Maintaining Lean Body Mass, a Brief Review. Nutrients 10:1876. https://doi.org/10.3390/nu10121876

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Funding

This study was supported by the National Natural Science Foundation of China (No. 82170751, 32102634), the Fund for Shanxi “1331 Project” (No. 20211331–16, 20211331–13, 20211331–12), the “Six New” Project of Agriculture and Rural Department of Shanxi Province, the Young Science Foundation of Shanxi province, China (Grant No. 201901D211368, No.20210302124700), the Start-Up Fund for doctoral research, Shanxi Agricultural University (Grant No. 2018YJ46, 2021BQ08), the Shanxi Province Excellent Doctoral Work Award-Scientific Research Project (Grant No. SXYBKY2019001, SXBYKY2021043), and the Innovation Projects of College of Veterinary Medicine, Shanxi Agricultural University (Grant No. DY-M007).

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Haidong Wang and Tianyi Xu conceived and designed the experiments. Tianyi Xu and Shiting Lu drafted the manuscript. Tianyi Xu and Juan Wang performed the experiments. Tianyi Xu, Huiling Zhang, Xiaofan Wei, Hongwei Shi, Yunyan Ji, Yi Yan, Xiaomao Luo, and Xiuju Yu processed and analyzed the data, and contributed reagents/materials/analysis tools and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Xiaomao Luo or Haidong Wang.

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Xu, T., Wang, J., Shi, H. et al. CCE and EODF as two distinct non-shivering thermogenesis models inducing weight loss. Pflugers Arch - Eur J Physiol 475, 961–974 (2023). https://doi.org/10.1007/s00424-023-02827-7

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