A macrophage NBR1-MEKK3 complex triggers JNK-mediated adipose tissue inflammation in obesity

Cell Metabolism

Volumn 20, Issue 3, 2014, Pages 499-511

  Hernandez, Eloy D ^a   Lee, Sang Jun ^a   Kim, Ji Young ^a   Duran, Angeles ^a   Linares, Juan F ^a   Yajima, Tomoko ^a   Müller, Timo D ^b   Tschöp, Matthias H ^b   Smith, Steven R ^c   Diaz Meco, Maria T ^a   Moscat, Jorge ^a  

^a BURNHAM INSTITUTE   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c FLORIDA HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CHEMOATTRACTANT; CHLORDANE; GAMMA INTERFERON; GLUCOSE; GLUCOSE 6 PHOSPHATASE; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; NBR1 PROTEIN; PB1 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PKC ZETA PROTEIN; PROTEIN; PROTEIN P62; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NBR1 PROTEIN, HUMAN; NBR1 PROTEIN, MOUSE;

ADIPOGENESIS; ADIPOSE TISSUE; ADIPOSE TISSUE INFLAMMATION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME REGULATION; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIPID METABOLISM; MACROPHAGE; MACROPHAGE FUNCTION; MALE; METABOLIC PARAMETERS; METABOLIC SYNDROME X; MIDDLE AGED; MOUSE; NONHUMAN; OBESITY; PHENOTYPE; POLARIZATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CELL LINE; CHEMISTRY; COMPLICATION; GENE DELETION; GENETICS; IMMUNOLOGY; INSULIN RESISTANCE; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; SEQUENCE ALIGNMENT;

ADIPOSE TISSUE; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELLS, CULTURED; FEMALE; GENE DELETION; HUMANS; INFLAMMATION; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MACROPHAGES; MALE; MAP KINASE KINASE KINASE 3; MICE; MOLECULAR SEQUENCE DATA; OBESITY; PROTEINS; SEQUENCE ALIGNMENT;

EID: 84913602512     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.06.008     Document Type: Article

References (43)

1. C.K. Glass, and J.M. Olefsky Inflammation and lipid signaling in the etiology of insulin resistance Cell Metab. 15 2012 635 645
2. S. Gordon Alternative activation of macrophages Nat. Rev. Immunol. 3 2003 23 35
3. S. Gordon, and P.R. Taylor Monocyte and macrophage heterogeneity Nat. Rev. Immunol. 5 2005 953 964
4. M.F. Gregor, and G.S. Hotamisligil Inflammatory mechanisms in obesity Annu. Rev. Immunol. 29 2011 415 445
5. S.M. Grundy, H.B. Brewer Jr., J.I. Cleeman, S.C. Smith Jr., and C. Lenfant Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition Circulation 109 2004 433 438
6. M.S. Han, D.Y. Jung, C. Morel, S.A. Lakhani, J.K. Kim, R.A. Flavell, and R.J. Davis JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation Science 339 2013 218 222
7. J. Hirosumi, G. Tuncman, L. Chang, C.Z. Görgün, K.T. Uysal, K. Maeda, M. Karin, and G.S. Hotamisligil A central role for JNK in obesity and insulin resistance Nature 420 2002 333 336
8. R.G. Holzer, E.J. Park, N. Li, H. Tran, M. Chen, C. Choi, G. Solinas, and M. Karin Saturated fatty acids induce c-Src clustering within membrane subdomains, leading to JNK activation Cell 147 2011 173 184
9. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 2006 860 867
10. A. Jaeschke, and R.J. Davis Metabolic stress signaling mediated by mixed-lineage kinases Mol. Cell 27 2007 498 508
11. K. Kang, S.M. Reilly, V. Karabacak, M.R. Gangl, K. Fitzgerald, B. Hatano, and C.H. Lee Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity Cell Metab. 7 2008 485 495
12. V. Kirkin, T. Lamark, Y.S. Sou, G. Bjørkøy, J.L. Nunn, J.A. Bruun, E. Shvets, D.G. McEwan, T.H. Clausen, and P. Wild A role for NBR1 in autophagosomal degradation of ubiquitinated substrates Mol. Cell 33 2009 505 516
13. S. Lange, F. Xiang, A. Yakovenko, A. Vihola, P. Hackman, E. Rostkova, J. Kristensen, B. Brandmeier, G. Franzen, and B. Hedberg The kinase domain of titin controls muscle gene expression and protein turnover Science 308 2005 1599 1603
14. J. Lanuza-Masdeu, M.I. Arévalo, C. Vila, A. Barberà, R. Gomis, and C. Caelles In vivo JNK activation in pancreatic β-cells leads to glucose intolerance caused by insulin resistance in pancreas Diabetes 62 2013 2308 2317
15. S.J. Lee, J.Y. Kim, R. Nogueiras, J.F. Linares, D. Perez-Tilve, D.Y. Jung, H.J. Ko, S.M. Hofmann, A. Drew, and M. Leitges PKCzeta-regulated inflammation in the nonhematopoietic compartment is critical for obesity-induced glucose intolerance Cell Metab. 12 2010 65 77
16. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J. Clin. Invest. 117 2007 175 184
17. C.N. Lumeng, S.M. Deyoung, J.L. Bodzin, and A.R. Saltiel Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity Diabetes 56 2007 16 23
18. C.N. Lumeng, S.M. Deyoung, and A.R. Saltiel Macrophages block insulin action in adipocytes by altering expression of signaling and glucose transport proteins Am. J. Physiol. Endocrinol. Metab. 292 2007 E166 E174
19. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol. 25 2004 677 686
20. F.K. Mardakheh, M. Yekezare, L.M. Machesky, and J.K. Heath Spred2 interaction with the late endosomal protein NBR1 down-regulates fibroblast growth factor receptor signaling J. Cell Biol. 187 2009 265 277
21. J. Moscat, and M.T. Diaz-Meco Feedback on fat: p62-mTORC1-autophagy connections Cell 147 2011 724 727
22. J. Moscat, M.T. Diaz-Meco, A. Albert, and S. Campuzano Cell signaling and function organized by PB1 domain interactions Mol. Cell 23 2006 631 640
23. J. Moscat, M.T. Diaz-Meco, and M.W. Wooten Signal integration and diversification through the p62 scaffold protein Trends Biochem. Sci. 32 2007 95 100
24. J. Moscat, M.T. Diaz-Meco, and M.W. Wooten Of the atypical PKCs, Par-4 and p62: recent understandings of the biology and pathology of a PB1-dominated complex Cell Death Differ. 16 2009 1426 1437
25. T.D. Müller, S.J. Lee, M. Jastroch, D. Kabra, K. Stemmer, M. Aichler, B. Abplanalp, G. Ananthakrishnan, N. Bhardwaj, and S. Collins p62 links β-adrenergic input to mitochondrial function and thermogenesis J. Clin. Invest. 123 2013 469 478
26. K. Nakamura, A.J. Kimple, D.P. Siderovski, and G.L. Johnson PB1 domain interaction of p62/sequestosome 1 and MEKK3 regulates NF-kappaB activation J. Biol. Chem. 285 2010 2077 2089
27. J.I. Odegaard, R.R. Ricardo-Gonzalez, A. Red Eagle, D. Vats, C.R. Morel, M.H. Goforth, V. Subramanian, L. Mukundan, A.W. Ferrante, and A. Chawla Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance Cell Metab. 7 2008 496 507
28. D. Patsouris, P.P. Li, D. Thapar, J. Chapman, J.M. Olefsky, and J.G. Neels Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals Cell Metab. 8 2008 301 309
29. M. Qatanani, and M.A. Lazar Mechanisms of obesity-associated insulin resistance: many choices on the menu Genes Dev. 21 2007 1443 1455
30. A. Rodriguez, A. Durán, M. Selloum, M.F. Champy, F.J. Diez-Guerra, J.M. Flores, M. Serrano, J. Auwerx, M.T. Diaz-Meco, and J. Moscat Mature-onset obesity and insulin resistance in mice deficient in the signaling adapter p62 Cell Metab. 3 2006 211 222
31. G. Sabio, M. Das, A. Mora, Z. Zhang, J.Y. Jun, H.J. Ko, T. Barrett, J.K. Kim, and R.J. Davis A stress signaling pathway in adipose tissue regulates hepatic insulin resistance Science 322 2008 1539 1543
32. S. Schenk, M. Saberi, and J.M. Olefsky Insulin sensitivity: modulation by nutrients and inflammation J. Clin. Invest. 118 2008 2992 3002
33. S.E. Shoelson, J. Lee, and A.B. Goldfine Inflammation and insulin resistance J. Clin. Invest. 116 2006 1793 1801
34. G. Solinas, C. Vilcu, J.G. Neels, G.K. Bandyopadhyay, J.L. Luo, W. Naugler, S. Grivennikov, A. Wynshaw-Boris, M. Scadeng, J.M. Olefsky, and M. Karin JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity Cell Metab. 6 2007 386 397
35. A.M. Spiegel, and E.G. Nabel NIH research on obesity and type 2 diabetes: providing the scientific evidence base for actions to improve health Nat. Med. 12 2006 67 69
36. K. Takahashi, S. Mizuarai, H. Araki, S. Mashiko, A. Ishihara, A. Kanatani, H. Itadani, and H. Kotani Adiposity elevates plasma MCP-1 levels leading to the increased CD11b-positive monocytes in mice J. Biol. Chem. 278 2003 46654 46660
37. G. Tuncman, J. Hirosumi, G. Solinas, L. Chang, M. Karin, and G.S. Hotamisligil Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance Proc. Natl. Acad. Sci. USA 103 2006 10741 10746
38. B. Ukropcova, O. Sereda, L. de Jonge, I. Bogacka, T. Nguyen, H. Xie, G.A. Bray, and S.R. Smith Family history of diabetes links impaired substrate switching and reduced mitochondrial content in skeletal muscle Diabetes 56 2007 720 727
39. S.N. Vallerie, M. Furuhashi, R. Fucho, and G.S. Hotamisligil A predominant role for parenchymal c-Jun amino terminal kinase (JNK) in the regulation of systemic insulin sensitivity PLoS ONE 3 2008 e3151
40. D. Vats, L. Mukundan, J.I. Odegaard, L. Zhang, K.L. Smith, C.R. Morel, R.A. Wagner, D.R. Greaves, P.J. Murray, and A. Chawla Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation Cell Metab. 4 2006 13 24
41. D. Yach, D. Stuckler, and K.D. Brownell Epidemiologic and economic consequences of the global epidemics of obesity and diabetes Nat. Med. 12 2006 62 66
42. J.Q. Yang, H.Z. Liu, M.T. Diaz-Meco, and J. Moscat NBR1 is a new PB1 signalling adapter in Th2 differentiation and allergic airway inflammation in vivo EMBO J. 29 2010 3421 3433
43. X. Zhang, A. Xu, S.K. Chung, J.H. Cresser, G. Sweeney, R.L. Wong, A. Lin, and K.S. Lam Selective inactivation of c-Jun NH2-terminal kinase in adipose tissue protects against diet-induced obesity and improves insulin sensitivity in both liver and skeletal muscle in mice Diabetes 60 2011 486 495