Xbp1s in pomc neurons connects ER stress with energy balance and glucose homeostasis

Cell Metabolism

Volumn 20, Issue 3, 2014, Pages 471-482

  Williams, Kevin W ^a   Liu, Tiemin ^a   Kong, Xingxing ^c   Fukuda, Makoto ^a,d   Deng, Yingfeng ^a   Berglund, Eric D ^a,b   Deng, Zhuo ^a,e   Gao, Yong ^a,f   Liu, Tianya ^a,g   Sohn, Jong Woo ^a   Jia, Lin ^a   Fujikawa, Teppei ^a   Kohno, Daisuke ^a,h   Scott, Michael M ⁱ   Lee, Syann ^a   Lee, Charlotte E ^a   Sun, Kai ^a   Chang, Yongsheng ^f   Scherer, Philipp E ^a,b   Elmquist, Joel K ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c HARVARD UNIVERSITY   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^f INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^g SOOCHOW UNIVERSITY   (China)

^h GUNMA UNIVERSITY   (Japan)

ⁱ UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; LEPTIN; PROOPIOMELANOCORTIN; X BOX BINDING PROTEIN 1; GLUCOSE REGULATED PROTEIN 78; INITIATION FACTOR 2; MESSENGER RNA; PROTEIN TYROSINE PHOSPHATASE 1B; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; DNA BINDING PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; DIABETES MELLITUS; DIET; ENDOPLASMIC RETICULUM STRESS; ENERGY BALANCE; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MOUSE; NERVE CELL; NONHUMAN; OBESITY; PRIORITY JOURNAL; SENSOR; WHITE ADIPOSE TISSUE; ARCUATE NUCLEUS; BASAL METABOLIC RATE; ENERGY EXPENDITURE; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; INSULIN BLOOD LEVEL; LIPID DIET; LIVER METABOLISM; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ADVERSE EFFECTS; ANIMAL; ENERGY METABOLISM; GENETICS; HOMEOSTASIS; LIVER; METABOLISM;

ANIMALS; DIET, HIGH-FAT; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; ENERGY METABOLISM; GLUCOSE; HOMEOSTASIS; INSULIN; LEPTIN; LIVER; MALE; MICE; NEURONS; OBESITY; PRO-OPIOMELANOCORTIN; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 84913530022     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.06.002     Document Type: Article

References (71)

1. A. Agouni, N. Mody, C. Owen, A. Czopek, D. Zimmer, M. Bentires-Alj, K.K. Bence, and M. Delibegović Liver-specific deletion of protein tyrosine phosphatase (PTP) 1B improves obesity- and pharmacologically induced endoplasmic reticulum stress Biochem. J. 438 2011 369 378
2. H. Al-Qassab, M.A. Smith, E.E. Irvine, J. Guillermet-Guibert, M. Claret, A.I. Choudhury, C. Selman, K. Piipari, M. Clements, and S. Lingard et al. Dominant role of the p110beta isoform of PI3K over p110alpha in energy homeostasis regulation by POMC and AgRP neurons Cell Metab. 10 2009 343 354
3. N. Balthasar, R. Coppari, J. McMinn, S.M. Liu, C.E. Lee, V. Tang, C.D. Kenny, R.A. McGovern, S.C. Chua Jr., J.K. Elmquist, and B.B. Lowell Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis Neuron 42 2004 983 991
4. R. Banno, D. Zimmer, B.C. De Jonghe, M. Atienza, K. Rak, W. Yang, and K.K. Bence PTP1B and SHP2 in POMC neurons reciprocally regulate energy balance in mice J. Clin. Invest. 120 2010 720 734
5. B.F. Belgardt, and J.C. Brüning CNS leptin and insulin action in the control of energy homeostasis Ann. N Y Acad. Sci. 1212 2010 97 113
6. G. Belteki, J. Haigh, N. Kabacs, K. Haigh, K. Sison, F. Costantini, J. Whitsett, S.E. Quaggin, and A. Nagy Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction Nucleic Acids Res. 33 2005 e51
7. K.K. Bence, M. Delibegovic, B. Xue, C.Z. Gorgun, G.S. Hotamisligil, B.G. Neel, and B.B. Kahn Neuronal PTP1B regulates body weight, adiposity and leptin action Nat. Med. 12 2006 917 924
8. E.D. Berglund, C.R. Vianna, J. Donato Jr., M.H. Kim, J.C. Chuang, C.E. Lee, D.A. Lauzon, P. Lin, L.J. Brule, and M.M. Scott et al. Direct leptin action on POMC neurons regulates glucose homeostasis and hepatic insulin sensitivity in mice J. Clin. Invest. 122 2012 1000 1009
9. A. Bettaieb, S. Liu, Y. Xi, N. Nagata, K. Matsuo, I. Matsuo, S. Chahed, J. Bakke, H. Keilhack, T. Tiganis, and F.G. Haj Differential regulation of endoplasmic reticulum stress by protein tyrosine phosphatase 1B and T cell protein tyrosine phosphatase J. Biol. Chem. 286 2011 9225 9235
10. C. Bjørbaek, J.K. Elmquist, J.D. Frantz, S.E. Shoelson, and J.S. Flier Identification of SOCS-3 as a potential mediator of central leptin resistance Mol. Cell 1 1998 619 625
11. A.A. Butler, and L.P. Kozak A recurring problem with the analysis of energy expenditure in genetic models expressing lean and obese phenotypes Diabetes 59 2010 323 329
12. R.V. Considine, M.K. Sinha, M.L. Heiman, A. Kriauciunas, T.W. Stephens, M.R. Nyce, J.P. Ohannesian, C.C. Marco, L.J. McKee, and T.L. Bauer et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans N. Engl. J. Med. 334 1996 292 295
13. W.S. Cook, and R.H. Unger Protein tyrosine phosphatase 1B: a potential leptin resistance factor of obesity Dev. Cell 2 2002 385 387
14. A.M. Cypess, S. Lehman, G. Williams, I. Tal, D. Rodman, A.B. Goldfine, F.C. Kuo, E.L. Palmer, Y.H. Tseng, and A. Doria et al. Identification and importance of brown adipose tissue in adult humans N. Engl. J. Med. 360 2009 1509 1517
15. M. Delibegovic, D. Zimmer, C. Kauffman, K. Rak, E.G. Hong, Y.R. Cho, J.K. Kim, B.B. Kahn, B.G. Neel, and K.K. Bence Liver-specific deletion of protein-tyrosine phosphatase 1B (PTP1B) improves metabolic syndrome and attenuates diet-induced endoplasmic reticulum stress Diabetes 58 2009 590 599
16. Y. Deng, Z.V. Wang, C. Tao, N. Gao, W.L. Holland, A. Ferdous, J.J. Repa, G. Liang, J. Ye, and M.A. Lehrman et al. The Xbp1s/GalE axis links ER stress to postprandial hepatic metabolism J. Clin. Invest. 123 2013 455 468
17. P.J. Enriori, A.E. Evans, P. Sinnayah, E.E. Jobst, L. Tonelli-Lemos, S.K. Billes, M.M. Glavas, B.E. Grayson, M. Perello, and E.A. Nillni et al. Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons Cell Metab. 5 2007 181 194
18. R.C. Frederich, A. Hamann, S. Anderson, B. Löllmann, B.B. Lowell, and J.S. Flier Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action Nat. Med. 1 1995 1311 1314
19. J.M. Friedman Obesity in the new millennium Nature 404 2000 632 634
20. M. Fukuda, K.W. Williams, L. Gautron, and J.K. Elmquist Induction of leptin resistance by activation of cAMP-Epac signaling Cell Metab. 13 2011 331 339
21. B.H. Gähwiler, and I. Llano Sodium and potassium conductances in somatic membranes of rat Purkinje cells from organotypic cerebellar cultures J. Physiol. 417 1989 105 122
22. F. Gu, D.T. Nguyên, M. Stuible, N. Dubé, M.L. Tremblay, and E. Chevet Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress J. Biol. Chem. 279 2004 49689 49693
23. A. Guilherme, J.V. Virbasius, V. Puri, and M.P. Czech Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes Nat. Rev. Mol. Cell Biol. 9 2008 367 377
24. J.W. Hill, K.W. Williams, C. Ye, J. Luo, N. Balthasar, R. Coppari, M.A. Cowley, L.C. Cantley, B.B. Lowell, and J.K. Elmquist Acute effects of leptin require PI3K signaling in hypothalamic proopiomelanocortin neurons in mice J. Clin. Invest. 118 2008 1796 1805
25. T. Hosoi, M. Sasaki, T. Miyahara, C. Hashimoto, S. Matsuo, M. Yoshii, and K. Ozawa Endoplasmic reticulum stress induces leptin resistance Mol. Pharmacol. 74 2008 1610 1619
26. J.K. Howard, and J.S. Flier Attenuation of leptin and insulin signaling by SOCS proteins Trends Endocrinol. Metab. 17 2006 365 371
27. J.K. Howard, B.J. Cave, L.J. Oksanen, I. Tzameli, C. Bjørbaek, and J.S. Flier Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3 Nat. Med. 10 2004 734 738
28. S.E. Kahn, R.L. Hull, and K.M. Utzschneider Mechanisms linking obesity to insulin resistance and type 2 diabetes Nature 444 2006 840 846
29. H. Kaneto, Y. Nakatani, D. Kawamori, T. Miyatsuka, T.A. Matsuoka, M. Matsuhisa, and Y. Yamasaki Role of oxidative stress, endoplasmic reticulum stress, and c-Jun N-terminal kinase in pancreatic beta-cell dysfunction and insulin resistance Int. J. Biochem. Cell Biol. 37 2005 1595 1608
30. A.C. Könner, and J.C. Brüning Selective insulin and leptin resistance in metabolic disorders Cell Metab. 16 2012 144 152
31. N. Krishnan, C. Fu, D.J. Pappin, and N.K. Tonks H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response Sci. Signal. 4 2011 ra86
32. H. Mori, R. Hanada, T. Hanada, D. Aki, R. Mashima, H. Nishinakamura, T. Torisu, K.R. Chien, H. Yasukawa, and A. Yoshimura Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity Nat. Med. 10 2004 739 743
33. G.J. Morton, D.E. Cummings, D.G. Baskin, G.S. Barsh, and M.W. Schwartz Central nervous system control of food intake and body weight Nature 443 2006 289 295
34. H. Münzberg, J.S. Flier, and C. Bjørbaek Region-specific leptin resistance within the hypothalamus of diet-induced obese mice Endocrinology 145 2004 4880 4889
35. M.G. Myers Jr., and D.P. Olson Central nervous system control of metabolism Nature 491 2012 357 363
36. M.G. Myers, M.A. Cowley, and H. Münzberg Mechanisms of leptin action and leptin resistance Annu. Rev. Physiol. 70 2008 537 556
37. M.G. Myers Jr., S.B. Heymsfield, C. Haft, B.B. Kahn, M. Laughlin, R.L. Leibel, M.H. Tschöp, and J.A. Yanovski Challenges and opportunities of defining clinical leptin resistance Cell Metab. 15 2012 150 156
38. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Görgün, L.H. Glimcher, and G.S. Hotamisligil Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461
39. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Görgün, and G.S. Hotamisligil Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140
40. L. Ozcan, A.S. Ergin, A. Lu, J. Chung, S. Sarkar, D. Nie, M.G. Myers Jr., and U. Ozcan Endoplasmic reticulum stress plays a central role in development of leptin resistance Cell Metab. 9 2009 35 51
41. E. Panzhinskiy, Y. Hua, B. Culver, J. Ren, and S. Nair Endoplasmic reticulum stress upregulates protein tyrosine phosphatase 1B and impairs glucose uptake in cultured myotubes Diabetologia 56 2013 598 607
42. L.E. Parton, C.P. Ye, R. Coppari, P.J. Enriori, B. Choi, C.Y. Zhang, C. Xu, C.R. Vianna, N. Balthasar, and C.E. Lee et al. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity Nature 449 2007 228 232
43. G. Ramadori, T. Fujikawa, M. Fukuda, J. Anderson, D.A. Morgan, R. Mostoslavsky, R.C. Stuart, M. Perello, C.R. Vianna, and E.A. Nillni et al. SIRT1 deacetylase in POMC neurons is required for homeostatic defenses against diet-induced obesity Cell Metab. 12 2010 78 87
44. J. Rossi, N. Balthasar, D. Olson, M. Scott, E. Berglund, C.E. Lee, M.J. Choi, D. Lauzon, B.B. Lowell, and J.K. Elmquist Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis Cell Metab. 13 2011 195 204
45. M. Schneeberger, M.O. Dietrich, D. Sebastián, M. Imbernón, C. Castaño, A. Garcia, Y. Esteban, A. Gonzalez-Franquesa, I.C. Rodríguez, and A. Bortolozzi et al. Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance Cell 155 2013 172 187
46. M.W. Schwartz, and D. Porte Jr. Diabetes, obesity, and the brain Science 307 2005 375 379
47. M.M. Scott, J.L. Lachey, S.M. Sternson, C.E. Lee, C.F. Elias, J.M. Friedman, and J.K. Elmquist Leptin targets in the mouse brain J. Comp. Neurol. 514 2009 518 532
48. S.E. Shoelson, J. Lee, and A.B. Goldfine Inflammation and insulin resistance J. Clin. Invest. 116 2006 1793 1801
49. J.W. Sohn, Y. Xu, J.E. Jones, K. Wickman, K.W. Williams, and J.K. Elmquist Serotonin 2C receptor activates a distinct population of arcuate pro-opiomelanocortin neurons via TRPC channels Neuron 71 2011 488 497
50. J.W. Sohn, L.E. Harris, E.D. Berglund, T. Liu, L. Vong, B.B. Lowell, N. Balthasar, K.W. Williams, and J.K. Elmquist Melanocortin 4 receptors reciprocally regulate sympathetic and parasympathetic preganglionic neurons Cell 152 2013 612 619
51. B.M. Spiegelman, and J.S. Flier Obesity and the regulation of energy balance Cell 104 2001 531 543
52. R.C. Taylor, and A. Dillin XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity Cell 153 2013 1435 1447
53. J.P. Thaler, and M.W. Schwartz Minireview: Inflammation and obesity pathogenesis: the hypothalamus heats up Endocrinology 151 2010 4109 4115
54. J.P. Thaler, C.X. Yi, E.A. Schur, S.J. Guyenet, B.H. Hwang, M.O. Dietrich, X. Zhao, D.A. Sarruf, V. Izgur, and K.R. Maravilla et al. Obesity is associated with hypothalamic injury in rodents and humans J. Clin. Invest. 122 2012 153 162
55. M.H. Tschöp, J.R. Speakman, J.R. Arch, J. Auwerx, J.C. Brüning, L. Chan, R.H. Eckel, R.V. Farese Jr., J.E. Galgani, and C. Hambly et al. A guide to analysis of mouse energy metabolism Nat. Methods 9 2012 57 63
56. P.C. Tsiotra, and C. Tsigos Stress, the endoplasmic reticulum, and insulin resistance Ann. N Y Acad. Sci. 1083 2006 63 76
57. W.D. van Marken Lichtenbelt, J.W. Vanhommerig, N.M. Smulders, J.M. Drossaerts, G.J. Kemerink, N.D. Bouvy, P. Schrauwen, and G.J. Teule Cold-activated brown adipose tissue in healthy men N. Engl. J. Med. 360 2009 1500 1508
58. K.A. Virtanen, M.E. Lidell, J. Orava, M. Heglind, R. Westergren, T. Niemi, M. Taittonen, J. Laine, N.J. Savisto, S. Enerbäck, and P. Nuutila Functional brown adipose tissue in healthy adults N. Engl. J. Med. 360 2009 1518 1525
59. K.E. Wellen, and G.S. Hotamisligil Inflammation, stress, and diabetes J. Clin. Invest. 115 2005 1111 1119
60. C. Weyer, C. Bogardus, D.M. Mott, and R.E. Pratley The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus J. Clin. Invest. 104 1999 787 794
61. C.L. White, A. Whittington, M.J. Barnes, Z. Wang, G.A. Bray, and C.D. Morrison HF diets increase hypothalamic PTP1B and induce leptin resistance through both leptin-dependent and -independent mechanisms Am. J. Physiol. Endocrinol. Metab. 296 2009 E291 E299
62. K.W. Williams, and J.K. Elmquist From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior Nat. Neurosci. 15 2012 1350 1355
63. K.W. Williams, L.O. Margatho, C.E. Lee, M. Choi, S. Lee, M.M. Scott, C.F. Elias, and J.K. Elmquist Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons J. Neurosci. 30 2010 2472 2479
64. K.W. Williams, M.M. Scott, and J.K. Elmquist Modulation of the central melanocortin system by leptin, insulin, and serotonin: co-ordinated actions in a dispersed neuronal network Eur. J. Pharmacol. 660 2011 2 12
65. J. Wu, P. Boström, L.M. Sparks, L. Ye, J.H. Choi, A.H. Giang, M. Khandekar, K.A. Virtanen, P. Nuutila, and G. Schaart et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human Cell 150 2012 366 376
66. C. Xu, B. Bailly-Maitre, and J.C. Reed Endoplasmic reticulum stress: cell life and death decisions J. Clin. Invest. 115 2005 2656 2664
67. G.S. Yeo, and L.K. Heisler Unraveling the brain regulation of appetite: lessons from genetics Nat. Neurosci. 15 2012 1343 1349
68. A. Yoshimura, T. Naka, and M. Kubo SOCS proteins, cytokine signalling and immune regulation Nat. Rev. Immunol. 7 2007 454 465
69. J.M. Zabolotny, K.K. Bence-Hanulec, A. Stricker-Krongrad, F. Haj, Y. Wang, Y. Minokoshi, Y.B. Kim, J.K. Elmquist, L.A. Tartaglia, B.B. Kahn, and B.G. Neel PTP1B regulates leptin signal transduction in vivo Dev. Cell 2 2002 489 495
70. J.M. Zabolotny, Y.B. Kim, L.A. Welsh, E.E. Kershaw, B.G. Neel, and B.B. Kahn Protein-tyrosine phosphatase 1B expression is induced by inflammation in vivo J. Biol. Chem. 283 2008 14230 14241
71. X. Zhang, G. Zhang, H. Zhang, M. Karin, H. Bai, and D. Cai Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity Cell 135 2008 61 73