Adipocyte OGT governs diet-induced hyperphagia and obesity

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Li, Min Dian ^a,d   Vera, Nicholas B ^b   Yang, Yunfan ^a   Zhang, Bichen ^a   Ni, Weiming ^a   Ziso Qejvanaj, Enida ^b   Ding, Sheng ^a   Zhang, Kaisi ^a   Yin, Ruonan ^a   Wang, Simeng ^a   Zhou, Xu ^a   Fang, Ethan X ^c   Xu, Tian ^a   Erion, Derek M ^b   Yang, Xiaoyong ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PFIZER INC   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANANDAMIDE; BETA DEXTRO N ACETYLGLUCOSAMINE TRANSFERASE; CANNABINOID 1 RECEPTOR; CELL PROTEIN; DIACYLGLYCEROL; ENDOCANNABINOID; LIPID; TRANSFERASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CANNABINOID; N ACETYLGLUCOSAMINE;

CELL; DIET; DISEASE; FOOD INTAKE; INDUCED RESPONSE; METABOLISM; NUTRITIONAL STATUS; OBESITY;

ACYLATION; ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; DIET INDUCED OBESITY; ENERGY EXPENDITURE; FATTY ACID DESATURATION; FOOD INTAKE; GLUCOSE TOLERANCE; HYPERINSULINEMIA; HYPERLEPTINEMIA; HYPERPHAGIA; INSULIN RESISTANCE; INSULIN RESPONSE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; INTERSCAPULAR BROWN ADIPOSE TISSUE; LIPIDOMICS; MALE; MOUSE; NONHUMAN; NUTRIENT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; WHITE ADIPOSE TISSUE; ADIPOSE TISSUE; ANIMAL; BODY WEIGHT; C57BL MOUSE; CELL LINE; GENETICS; HUMAN; IN VITRO STUDY; METABOLISM; OBESITY; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ACETYLGLUCOSAMINE; ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; CANNABINOIDS; CELL LINE; HUMANS; HYPERPHAGIA; IN VITRO TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; OBESITY; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 85057786003     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-07461-x     Document Type: Article

References (58)

1. Ochner, C. N., Barrios, D. M., Lee, C. D. & Pi-Sunyer, F. X. Biological mechanisms that promote weight regain following weight loss in obese humans. Physiol. Behav. 120, 106–113 (2013).
2. Leibel, R. L. et al. Biologic responses to weight loss and weight regain: report from an American Diabetes Association Research Symposium. Diabetes 64, 2299–2309 (2015).
3. Dietrich, M. O. & Horvath, T. L. Limitations in anti-obesity drug development: the critical role of hunger-promoting neurons. Nat. Rev. Drug. Discov. 11, 675–691 (2012).
4. Dietrich, M. O. et al. Agrp neurons mediate Sirt1’s action on the melanocortin system and energy balance: roles for Sirt1 in neuronal firing and synaptic plasticity. J. Neurosci.: Off. J. Soc. Neurosci. 30, 11815–11825 (2010).
5. Cota, D. et al. Hypothalamic mTOR signaling regulates food intake. Science 312, 927–930 (2006).
6. Minokoshi, Y. et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428, 569–574 (2004).
7. Flier, J. S. & Maratos-Flier, E. Leptin’s physiologic role: does the emperor of energy balance have no clothes? Cell Metab. 26, 24–26 (2017).
8. Di Marzo, V. & Matias, I. Endocannabinoid control of food intake and energy balance. Nat. Neurosci. 8, 585–589 (2005).
9. Di Marzo, V. et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410, 822–825 (2001).
10. Cluny, N. L. et al. A novel peripherally restricted cannabinoid receptor antagonist, AM6545, reduces food intake and body weight, but does not cause malaise, in rodents. Br. J. Pharmacol. 161, 629–642 (2010).
11. Tam, J. et al. Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J. Clin. Invest. 120, 2953–2966 (2010).
12. Engeli, S. et al. Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54, 2838–2843 (2005).
13. Liu, J. et al. Monounsaturated fatty acids generated via stearoyl CoA desaturase-1 are endogenous inhibitors of fatty acid amide hydrolase. Proc. Natl Acad. Sci. USA 110, 18832–18837 (2013).
14. Hart, G. W., Housley, M. P. & Slawson, C. Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017–1022 (2007).
15. Yang, X. & Qian, K. Protein O-GlcNAcylation: emerging mechanisms and functions. Nat. Rev. Mol. Cell Biol. 18, 452–465 (2017).
16. Ruan, H. B., Singh, J. P., Li, M. D., Wu, J. & Yang, X. Cracking the O-GlcNAc code in metabolism. Trends Endocrinol. Metab. 24, 301–309 (2013).
17. Bond, M. R. & Hanover, J. A. O-GlcNAc cycling: a link between metabolism and chronic disease. Annu. Rev. Nutr. 33, 205–229 (2013).
18. Wang, J., Liu, R., Hawkins, M., Barzilai, N. & Rossetti, L. A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature 393, 684–688 (1998).
19. McClain, D. A. et al. Altered glycan-dependent signaling induces insulin resistance and hyperleptinemia. Proc. Natl Acad. Sci. USA 99, 10695–10699 (2002).
20. Rosen, E. D. & Spiegelman, B. M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847–853 (2006).
21. Myers, M. G. Jr., Leibel, R. L., Seeley, R. J. & Schwartz, M. W. Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol. Metab. 21, 643–651 (2010).
22. Erion, D. M. & Shulman, G. I. Diacylglycerol-mediated insulin resistance. Nat. Med. 16, 400–402 (2010).
23. Lee, J., Choi, J., Aja, S., Scafidi, S. & Wolfgang, M. J. Loss of adipose fatty acid oxidation does not potentiate obesity at thermoneutrality. Cell Rep. 14, 1308–1316 (2016).
24. Lee, J., Ellis, J. M. & Wolfgang, M. J. Adipose fatty acid oxidation is required for thermogenesis and potentiates oxidative stress-induced inflammation. Cell Rep. 10, 266–279 (2015).
25. Sugii, S. et al. PPARgamma activation in adipocytes is sufficient for systemic insulin sensitization. Proc. Natl Acad. Sci. USA 106, 22504–22509 (2009).
26. Riserus, U. et al. Rosiglitazone increases indexes of stearoyl-CoA desaturase activity in humans: link to insulin sensitization and the role of dominant-negative mutation in peroxisome proliferator-activated receptor-gamma. Diabetes 54, 1379–1384 (2005).
27. Shi, H. B. et al. Peroxisome proliferator-activated receptor-gamma stimulates the synthesis of monounsaturated fatty acids in dairy goat mammary epithelial cells via the control of stearoyl-coenzyme A desaturase. J. Dairy Sci. 96, 7844–7853 (2013).
28. Ahmadian, M. et al. PPARgamma signaling and metabolism: the good, the bad and the future. Nat. Med. 19, 557–566 (2013).
29. Ji, S., Park, S. Y., Roth, J., Kim, H. S. & Cho, J. W. O-GlcNAc modification of PPARgamma reduces its transcriptional activity. Biochem. Biophys. Res. Commun. 417, 1158–1163 (2012).
30. Mozaffarian, D. et al. Circulating palmitoleic acid and risk of metabolic abnormalities and new-onset diabetes. Am. J. Clin. Nutr. 92, 1350–1358 (2010).
31. Cao, H. et al. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134, 933–944 (2008).
32. von Holstein-Rathlou, S. et al. FGF21 Mediates endocrine control of simple sugar intake and sweet taste preference by the liver. Cell. Metab. 23, 335–343 (2016).
33. Talukdar, S. et al. FGF21 regulates sweet and alcohol preference. Cell. Metab. 23, 344–349 (2016).
34. Flowers, M. T., Ade, L., Strable, M. S. & Ntambi, J. M. Combined deletion of SCD1 from adipose tissue and liver does not protect mice from obesity. J. Lipid Res. 53, 1646–1653 (2012).
35. Sampath, H. et al. Skin-specific deletion of stearoyl-CoA desaturase-1 alters skin lipid composition and protects mice from high fat diet-induced obesity. J. Biol. Chem. 284, 19961–19973 (2009).
36. Ntambi, J. M. et al. Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl Acad. Sci. USA 99, 11482–11486 (2002).
37. Cohen, P. et al. Role for stearoyl-CoA desaturase-1 in leptin-mediated weight loss. Science 297, 240–243 (2002).
38. Martens, K., Bottelbergs, A. & Baes, M. Ectopic recombination in the central and peripheral nervous system by aP2/FABP4-Cre mice: implications for metabolism research. FEBS Lett. 584, 1054–1058 (2010).
39. Estruch, R. et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N. Engl. J. Med. 368, 1279–1290 (2013).
40. Estruch, R. et al. Effect of a high-fat Mediterranean diet on bodyweight and waist circumference: a prespecified secondary outcomes analysis of the PREDIMED randomised controlled trial. Lancet Diabetes Endocrinol. 4, 11 (2016).
41. Wilson, R. I. & Nicoll, R. A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588–592 (2001).
42. Buettner, C. et al. Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat. Med. 14, 667–675 (2008).
43. Cota, D. et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J. Clin. Invest. 112, 423–431 (2003).
44. Bensaid, M. et al. The cannabinoid CB1 receptor antagonist SR141716 increases Acrp30 mRNA expression in adipose tissue of obese fa/fa rats and in cultured adipocyte cells. Mol. Pharmacol. 63, 908–914 (2003).
45. Ruiz de Azua, I. et al. Adipocyte cannabinoid receptor CB1 regulates energy homeostasis and alternatively activated macrophages. J. Clin. Invest. 127, 4148–4162 (2017).
46. Yang, X. et al. Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 451, 964–969 (2008).
47. Ruan, H. B. et al. O-GlcNAc transferase/host cell factor C1 complex regulates gluconeogenesis by modulating PGC-1α stability. Cell. Metab. 16, 226–237 (2012).
48. Dentin, R., Hedrick, S., Xie, J., Yates, J. 3rd & Montminy, M. Hepatic glucose sensing via the CREB coactivator CRTC2. Science 319, 1402–1405 (2008).
49. Erickson, J. R. et al. Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 502, 372–376 (2013).
50. Ruan, H. B. et al. O-GlcNAc transferase enables AgRP neurons to suppress browning of white fat. Cell 159, 306–317 (2014).
51. Lagerlof, O. et al. The nutrient sensor OGT in PVN neurons regulates feeding. Science 351, 1293–1296 (2016).
52. Ortiz-Meoz, R. F. et al. A small molecule that inhibits OGT activity in cells. Acs. Chem. Biol. 10, 1392–1397 (2015).
53. Wang, Y., Zhu, J. & Zhang, L. Discovery of cell-permeable O-GlcNAc transferase inhibitors via tethering in situ click chemistry. J. Med. Chem. 60, 263–272 (2017).
54. Liu, Y. et al. Discovery of a low toxicity O-GlcNAc transferase (OGT) inhibitor by structure-based virtual screening of natural products. Sci. Rep. 7, 12334 (2017).
55. Lazarus, M. B., Nam, Y., Jiang, J., Sliz, P. & Walker, S. Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469, 564–567 (2011).
56. Li, M. D. et al. O-GlcNAc signaling entrains the circadian clock by inhibiting BMAL1/CLOCK ubiquitination. Cell. Metab. 17, 303–310 (2013).
57. Yuan, M. & Lin, Y. Model selection and estimation in the Gaussian graphical model. Biometrika 94, 19–35 (2007).
58. Parks, B. W. et al. Genetic architecture of insulin resistance in the mouse. Cell. Metab. 21, 334–346 (2015).