Deletion of C/EBP homologous protein (Chop) in C57Bl/6 mice dissociates obesity from insulin resistance

Diabetologia

Volumn 55, Issue 4, 2012, Pages 1167-1178

  Maris, M ^a   Overbergh, L ^a   Gysemans, C ^a   Waget, A ^a   Cardozo, A K ^c   Verdrengh, E ^a   Cunha, J P M ^a   Gotoh, T ^d   Cnop, M ^c,e   Eizirik, D L ^c   Burcelin, R ^b   Mathieu, C ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b CHU RANGUEIL   (France)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d KUMAMOTO UNIVERSITY   (Japan)

^e ERASME HOSPITAL   (Belgium)

Author keywords

CHOP. Endoplasmic reticulum Inflammation Obesity. Steatosis Type 2 diabetes

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; CARBOHYDRATE RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKINE; FATTY ACID SYNTHASE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEXOKINASE 2; INSULIN; LIOTHYRONINE; MESSENGER RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALLING 3; THAPSIGARGIN; THYROXINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1 SPLICED;

ABDOMINAL FAT; ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENERGY EXPENDITURE; FATTY LIVER; FEMALE; GLUCOSE TOLERANCE; HYPERINSULINEMIA; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID STORAGE; LIVER; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM;

ADIPOSE TISSUE; ANIMALS; FATTY LIVER; GLUCOSE INTOLERANCE; INFLAMMATION; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; LIVER; MICE; MICE, KNOCKOUT; OBESITY; TRANSCRIPTION FACTOR CHOP;

EID: 84862577245     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2427-7     Document Type: Article

References (50)

1. Ozcan L, Ergin AS, Lu A et al (2009) Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 9:35-51
2. Ozcan U, Cao Q, Yilmaz E et al (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461
3. Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D (2008) Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 135:61-73
4. Marciniak SJ, Yun CY, Oyadomari S et al (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18:3066-3077
5. Wang XZ, Kuroda M, Sok J et al (1998) Identification of novel stress-induced genes downstream of chop. EMBO J 17:3619-3630
6. Gotoh T, Terada K, Oyadomari S, Mori M (2004) hsp70-DnaJ chaperone pair prevents nitric oxide-and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ 11:390-402
7. Kayo T, Koizumi A (1998) Mapping of murine diabetogenic gene mody on chromosome 7 at D7Mit258 and its involvement in pancreatic islet and beta cell development during the perinatal period. J Clin Invest 101:2112-2118
8. Oyadomari S, Koizumi A, Takeda K et al (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109:525-532
9. Ariyama Y, Shimizu H, Satoh T et al (2007) Chop-deficient mice showed increased adiposity but no glucose intolerance. Obesity (Silver Spring) 15:1647-1656
10. Endo M, Oyadomari S, Suga M, Mori M, Gotoh T (2005) The ER stress pathway involving CHOP is activated in the lungs of LPS-treated mice. J Biochem 138:501-507
11. Endo M, Mori M, Akira S, Gotoh T (2006) C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J Immunol 176:6245-6253
12. Namba T, Tanaka K, Ito Y et al (2009) Positive role of CCAAT/enhancer-binding protein homologous protein, a transcription factor involved in the endoplasmic reticulum stress response in the development of colitis. Am J Pathol 174:1786-1798
13. Suyama K, Ohmuraya M, Hirota M et al (2008) C/EBP homologous protein is crucial for the acceleration of experimental pancreatitis. Biochem Biophys Res Commun 367:176-182
14. Woo CW, Cui D, Arellano J et al (2009) Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by tolllike receptor signalling. Nat Cell Biol 11:1473-1480
15. Mahadevan NR, Rodvold J, Sepulveda H, Rossi S, Drew AF, Zanetti M (2011) Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc Natl Acad Sci USA 108:6561-6566
16. Pereira RC, Stadmeyer LE, Smith DL, Rydziel S, Canalis E (2007) CCAAT/Enhancer-binding protein homologous protein (CHOP) decreases bone formation and causes osteopenia. Bone 40: 619-626
17. Oyadomari S, Takeda K, Takiguchi M et al (2001) Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA 98:10845-10850
18. Van Veldhoven PP, Swinnen JV, Esquenet M, Verhoeven G (1997) Lipase-based quantitation of triacylglycerols in cellular lipid extracts: requirement for presence of detergent and prior separation by thin-layer chromatography. Lipids 32:1297-1300
19. Mizuno K, Toyosato M, Yabumoto S, Tanimizu I, Hirakawa H (1980) A new enzymatic method for colorimetric determination of free fatty acids. Anal Biochem 108:6-10
20. Darras VM, Visser TJ, Berghman LR, Kuhn ER (1992) Ontogeny of type I and type III deiodinase activities in embryonic and posthatch chicks: relationship with changes in plasma triiodothy-ronine and growth hormone levels. Comp Biochem Physiol Comp Physiol 103:131-136
21. Burcelin R, Crivelli V, Dacosta A, Roy-Tirelli A, Thorens B (2002) Heterogeneous metabolic adaptation of C57BL/6 J mice to high-fat diet. Am J Physiol Endocrinol Metab 282:E834-E842
22. Bard-Chapeau EA, Hevener AL, Long S, Zhang EE, Olefsky JM, Feng GS (2005) Deletion of Gab1 in the liver leads to enhanced glucose tolerance and improved hepatic insulin action. Nat Med 11:567-571
23. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ (2008) Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 118:3378-3389
24. Cunha DA, Hekerman P, Ladriere L et al (2008) Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J Cell Sci 121:2308-2318
25. Hummasti S, Hotamisligil GS (2010) Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circ Res 107: 579-591
26. Maris M, Waelkens E, Cnop M et al (2011) Oleate-induced beta cell dysfunction and apoptosis: a proteomic approach to glucoli-potoxicity by an unsaturated fatty acid. J Proteome Res 10:3372-3385
27. Maris M, Ferreira GB, D'Hertog W et al (2010) High glucose induces dysfunction in insulin secretory cells by different pathways: a proteomic approach. J Proteome Res 9:6274-6287
28. Bastard JP, Maachi M, Lagathu C et al (2006) Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17:4-12
29. Boden G, Duan X, Homko C et al (2008) Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 57:2438-2444
30. Xu H, Barnes GT, Yang Q et al (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821-1830
31. Bouloumie A, Curat CA, Sengenes C, Lolmede K, Miranville A, Busse R (2005) Role of macrophage tissue infiltration in metabolic diseases. Curr Opin Clin Nutr Metab Care 8:347-354
32. Rotter V, Nagaev I, Smith U (2003) Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278:45777-45784
33. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM (1996) IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha-and obesity-induced insulin resistance. Science 271:665-668
34. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115:1111-1119
35. Szendroedi J, Roden M (2009) Ectopic lipids and organ function. Curr Opin Lipidol 20:50-56
36. Lettner A, Roden M (2008) Ectopic fat and insulin resistance. Curr Diab Rep 8:185-191
37. Minehira K, Young SG, Villanueva CJ et al (2008) Blocking VLDL secretion causes hepatic steatosis but does not affect peripheral lipid stores or insulin sensitivity in mice. J Lipid Res 49:2038-2044
38. Ogawa W, Kasuga M (2008) Cell signaling. Fat stress and liver resistance. Science 322:1483-1484
39. Kanda H, Tateya S, Tamori Y et al (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116:1494-1505
40. Weisberg SP, Hunter D, Huber R et al (2006) CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 116:115-124
41. Sartipy P, Loskutoff DJ (2003) Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc Natl Acad Sci USA 100:7265-7270
42. Tamura Y, Sugimoto M, Murayama T et al (2008) Inhibition of CCR2 ameliorates insulin resistance and hepatic steatosis in db/db mice. Arterioscler Thromb Vasc Biol 28:2195-2201
43. Jo D, Liu D, Yao S, Collins RD, Hawiger J (2005) Intracellular protein therapy with SOCS3 inhibits inflammation and apoptosis. Nat Med 11:892-898
44. Torisu T, Sato N, Yoshiga D et al (2007) The dual function of hepatic SOCS3 in insulin resistance in vivo. Genes Cells 12:143-154
45. Ueki K, Kondo T, Kahn CR (2004) Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 24:5434-5446
46. Fu S, Yang L, Li P et al (2011) Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473:528-531
47. Bruss MD, Arias EB, Lienhard GE, Cartee GD (2005) Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54:41-50
48. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endo-plasmic reticulum stress. Cell Death Differ 11:381-389
49. Bulua AC, Simon A, Maddipati R et al (2011) Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J Exp Med 208:519-533
50. Vij N, Amoako MO, Mazur S, Zeitlin PL (2008) CHOP transcription factor mediates IL-8 signaling in cystic fibrosis bronchial epithelial cells. Am J Respir Cell Mol Biol 38:176-184