CCAAT/enhancer-binding protein β (C/EBPβ) expression regulates dietary-induced inflammation in macrophages and adipose tissue in mice

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34349-34360

  Rahman, Shaikh M ^a   Janssen, Rachel C ^a   Choudhury, Mahua ^a   Baquero, Karalee C ^a   Aikens, Rebecca M ^a   De La Houssaye, Becky A ^a   Friedman, Jacob E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3T3-L1 ADIPOCYTES; ADIPOCYTES; ADIPOSE TISSUE; ANTI-INFLAMMATORIES; BONE MARROW; CCAAT/ENHANCER-BINDING PROTEINS; DNA BINDING ACTIVITY; HIGH-FAT DIET; INFLAMMASOME; INFLAMMATORY RESPONSE; INSULIN RESISTANCE; INSULIN SENSITIVITY; JNK ACTIVATION; LOW LEVEL; MACROPHAGE ACTIVATION; MACROPHAGE CELLS; MITOCHONDRIAL GENES; OVER-EXPRESSION; PERITONEAL MACROPHAGE; PROTEIN EXPRESSIONS; SYSTEMIC INFLAMMATION; THERAPEUTIC TARGETS; TRANSCRIPTIONAL NETWORKS; WHITE ADIPOSE TISSUES;

BONE; CHEMICAL ACTIVATION; GENE EXPRESSION; INSULIN; MAMMALS; NUTRITION; PATHOLOGY; PROTEINS; SATURATED FATTY ACIDS; TISSUE;

MACROPHAGES;

ACYL COENZYME A DESATURASE 1; CCAAT ENHANCER BINDING PROTEIN BETA; CRYOPYRIN; CYTOKINE; DIACYLGLYCEROL ACYLTRANSFERASE 2; INFLAMMASOME; INTERLEUKIN 10; LIVER X RECEPTOR ALPHA; PALMITIC ACID; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; UNCOUPLING PROTEIN 1;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; BROWN ADIPOSE TISSUE; CELL ISOLATION; CHIMERA; CIDEA GENE; CONTROLLED STUDY; DISEASE RESISTANCE; ENZYME ACTIVATION; GENE; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; INFLAMMATION; INSULIN SENSITIVITY; KNOCKOUT MOUSE; LIPID DIET; LIVER; LXRALPHA GENE; MALE; MITOCHONDRION; MOUSE; NLRP3 GENE; NONHUMAN; OBESITY; PERITONEUM MACROPHAGE; PRDM16 GENE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; UCP1 GENE; UPREGULATION; WHITE ADIPOSE TISSUE;

3T3-L1 CELLS; ADIPOSE TISSUE, BROWN; ANIMALS; ANTIGENS, DIFFERENTIATION; CARRIER PROTEINS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; DIETARY FATS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-10; MACROPHAGE ACTIVATION; MACROPHAGES; MAP KINASE KINASE 4; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OBESITY; TRANSCRIPTION FACTOR RELA;

EID: 84867270004     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.410613     Document Type: Article

References (61)

1. Hummasti, S., and Hotamisligil, G. S. (2010) Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circ. Res. 107, 579-591
2. Lumeng, C. N., and Saltiel, A. R. (2011) Inflammatory links between obesity and metabolic disease. J. Clin. Invest. 121, 2111-2117
3. Fessler, M. B., Rudel, L. L., and Brown, J. M. (2009) Toll-like receptor signaling links dietary fatty acids to the metabolic syndrome. Curr. Opin. Lipidol. 20, 379-385
4. Shi, H., Kokoeva, M. V., Inouye, K., Tzameli, I., Yin, H., and Flier, J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025 (Pubitemid 44684486)
5. Holland, W. L., Bikman, B. T., Wang, L. P., Yuguang, G., Sargent, K. M., Bulchand, S., Knotts, T. A., Shui, G., Clegg, D. J., Wenk, M. R., Pagliassotti, M. J., Scherer, P. E., and Summers, S. A. (2011) Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest. 121, 1858-1870
6. Schaeffler, A., Gross, P., Buettner, R., Bollheimer, C., Buechler, C., Neumeier, M., Kopp, A., Schoelmerich, J., and Falk, W. (2009) Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-κB pathway in adipocytes links nutritional signaling with innate immunity. Immunology 126, 233-245
7. Suganami, T., Tanimoto-Koyama, K., Nishida, J., Itoh, M., Yuan, X., Mizuarai, S., Kotani, H., Yamaoka, S., Miyake, K., Aoe, S., Kamei, Y., and Ogawa, Y. (2007) Role of the Toll-like receptor 4/NF-κB pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler. Thromb. Vasc. Biol. 27, 84-91 (Pubitemid 46370478)
8. Lumeng, C. N., Bodzin, J. L., and Saltiel, A. R. (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117, 175-184 (Pubitemid 46048464)
9. Gordon, S., and Taylor, P. R. (2005) Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964 (Pubitemid 41746764)
10. Odegaard, J. I., Ricardo-Gonzalez, R. R., Goforth, M. H., Morel, C. R., Subramanian, V., Mukundan, L., Red Eagle, A., Vats, D., Brombacher, F., Ferrante, A. W., and Chawla, A. (2007) Macrophage-specific PPARγ controls alternative activation and improves insulin resistance. Nature 447, 1116-1120 (Pubitemid 47014427)
11. Odegaard, J. I., Ricardo-Gonzalez, R. R., Red Eagle, A., Vats, D., Morel, C. R., Goforth, M. H., Subramanian, V., Mukundan, L., Ferrante, A. W., and Chawla, A. (2008) Alternative M2 activation of Kupffer cells by PPARδ ameliorates obesity-induced insulin resistance. Cell Metab. 7, 496-507 (Pubitemid 351729205)
12. Saberi, M., Woods, N. B., de Luca, C., Schenk, S., Lu, J. C., Bandyopadhyay, G., Verma, I. M., and Olefsky, J. M. (2009) Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 10, 419-429
13. Arkan, M. C., Hevener, A. L., Greten, F. R., Maeda, S., Li, Z. W., Long, J. M., Wynshaw-Boris, A., Poli, G., Olefsky, J., and Karin, M. (2005) IKK-β links inflammation to obesity-induced insulin resistance. Nat. Med. 11, 191-198 (Pubitemid 40321355)
14. Solinas, G., Vilcu, C., Neels, J. G., Bandyopadhyay, G. K., Luo, J. L., Naugler, W., Grivennikov, S., Wynshaw-Boris, A., Scadeng, M., Olefsky, J. M., and Karin, M. (2007) JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metab. 6, 386-397 (Pubitemid 350012000)
15. Lesniewski, L. A., Hosch, S. E., Neels, J. G., de Luca, C., Pashmforoush, M., Lumeng, C. N., Chiang, S. H., Scadeng, M., Saltiel, A. R., and Olefsky, J. M. (2007) Bone marrow-specific Cap gene deletion protects against high-fat diet-induced insulin resistance. Nat. Med. 13, 455-462 (Pubitemid 46559827)
16. Furuhashi, M., Fucho, R., Görgün, C. Z., Tuncman, G., Cao, H., and Hotamisligil, G. S. (2008) Adipocyte/macrophage fatty acid-binding proteins contribute to metabolic deterioration through actions in both macrophages and adipocytes in mice. J. Clin. Invest. 118, 2640-2650 (Pubitemid 351949791)
17. Koliwad, S. K., Streeper, R. S., Monetti, M., Cornelissen, I., Chan, L., Terayama, K., Naylor, S., Rao, M., Hubbard, B., and Farese, R. V., Jr. (2010) DGAT1-dependent triacylglycerol storage by macrophages protects mice from diet-induced insulin resistance and inflammation. J. Clin. Invest. 120, 756-767
18. Wueest, S., Rapold, R. A., Schumann, D. M., Rytka, J. M., Schildknecht, A., Nov, O., Chervonsky, A. V., Rudich, A., Schoenle, E. J., Donath, M. Y., and Konrad, D. (2010) Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J. Clin. Invest. 120, 191-202
19. Lee, S. J., Kim, J. Y., Nogueiras, R., Linares, J. F., Perez-Tilve, D., Jung, D. Y., Ko, H. J., Hofmann, S. M., Drew, A., Leitges, M., Kim, J. K., Tschöp, M. H., Diaz-Meco, M. T., and Moscat, J. (2010) PKCζ-regulated inflammation in the nonhematopoietic compartment is critical for obesity-induced glucose intolerance. Cell Metab. 12, 65-77
20. Qi, L., Saberi, M., Zmuda, E., Wang, Y., Altarejos, J., Zhang, X., Dentin, R., Hedrick, S., Bandyopadhyay, G., Hai, T., Olefsky, J., and Montminy, M. (2009) Adipocyte CREB promotes insulin resistance in obesity. Cell Metab. 9, 277-286
21. Ron, D., and Habener, J. F. (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6, 439-453
22. Ramji, D. P., and Foka, P. (2002) CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365, 561-575 (Pubitemid 34864439)
23. Poli, V. (1998) The role of C/EBP isoforms in the control of inflammatory and native immunity functions. J. Biol. Chem. 273, 29279-29282
24. Descombes, P., and Schibler, U. (1991) A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67, 569-579 (Pubitemid 121001471)
25. Matsuda, T., Kido, Y., Asahara, S., Kaisho, T., Tanaka, T., Hashimoto, N., Shigeyama, Y., Takeda, A., Inoue, T., Shibutani, Y., Koyanagi, M., Hosooka, T., Matsumoto, M., Inoue, H., Uchida, T., Koike, M., Uchiyama, Y., Akira, S., and Kasuga, M. (2010) Ablation of C/EBPβ alleviates ER stress and pancreatic β cell failure through the GRP78 chaperone in mice. J. Clin. Invest. 120, 115-126
26. Rahman, S. M., Qadri, I., Janssen, R. C., and Friedman, J. E. (2009) Fenofibrate and PBA prevent fatty acid-induced loss of adiponectin receptor and pAMPK in human hepatoma cells and in hepatitis C virus-induced steatosis. J. Lipid Res. 50, 2193-2202
27. Schroeder-Gloeckler, J. M., Rahman, S. M., Janssen, R. C., Qiao, L., Shao, J., Roper, M., Fischer, S. J., Lowe, E., Orlicky, D. J., McManaman, J. L., Palmer, C., Gitomer, W. L., Huang, W., O'Doherty, R. M., Becker, T. C., Klemm, D. J., Jensen, D. R., Pulawa, L. K., Eckel, R. H., and Friedman, J. E. (2007) CCAAT/enhancer-binding protein β deletion reduces adiposity, hepatic steatosis, and diabetes in Lepr(db/db) mice. J. Biol. Chem. 282, 15717-15729 (Pubitemid 47093283)
28. Rahman, S. M., Schroeder-Gloeckler, J. M., Janssen, R. C., Jiang, H., Qadri, I., Maclean, K. N., and Friedman, J. E. (2007) CCAAT/enhancing binding protein β deletion in mice attenuates inflammation, endoplasmic reticulum stress, and lipid accumulation in diet-induced nonalcoholic steatohepatitis. Hepatology 45, 1108-1117 (Pubitemid 46775772)
29. Yan, C., Zhu, M., Staiger, J., Johnson, P. F., and Gao, H. (2012) C5a-regulated CCAAT/enhancer-binding proteins β and δ are essential in Fcγ receptor-mediated inflammatory cytokine and chemokine production in macrophages. J. Biol. Chem. 287, 3217-3230
30. Wang, L., Shao, J., Muhlenkamp, P., Liu, S., Klepcyk, P., Ren, J., and Friedman, J. E. (2000) Increased insulin receptor substrate-1 and enhanced skeletal muscle insulin sensitivity in mice lacking CCAAT/enhancer-binding protein β. J. Biol. Chem. 275, 14173-14181 (Pubitemid 30339694)
31. Student, A. K., Hsu, R. Y., and Lane, M. D. (1980) Induction of fatty acid synthetase synthesis in differentiating 3T3-L1 preadipocytes. J. Biol. Chem. 255, 4745-4750 (Pubitemid 10060752)
32. Ohashi, K., Parker, J. L., Ouchi, N., Higuchi, A., Vita, J. A., Gokce, N., Pedersen, A. A., Kalthoff, C., Tullin, S., Sams, A., Summer, R., and Walsh, K. (2010) Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J. Biol. Chem. 285, 6153-6160
33. Barbour, L. A., Mizanoor Rahman, S., Gurevich, I., Leitner, J. W., Fischer, S. J., Roper, M. D., Knotts, T. A., Vo, Y., McCurdy, C. E., Yakar, S., Leroith, D., Kahn, C. R., Cantley, L. C., Friedman, J. E., and Draznin, B. (2005) Increased P85α is a potent negative regulator of skeletal muscle insulin signaling and induces in vivo insulin resistance associated with growth hormone excess. J. Biol. Chem. 280, 37489-37494 (Pubitemid 41642357)
34. Ather, J. L., Ckless, K., Martin, R., Foley, K. L., Suratt, B. T., Boyson, J. E., Fitzgerald, K. A., Flavell, R. A., Eisenbarth, S. C., and Poynter, M. E. (2011) Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J. Immunol. 187, 64-73
35. Chiang, S. H., Bazuine, M., Lumeng, C. N., Geletka, L. M., Mowers, J., White, N. M., Ma, J. T., Zhou, J., Qi, N., Westcott, D., Delproposto, J. B., Blackwell, T. S., Yull, F. E., and Saltiel, A. R. (2009) The protein kinase IKKε regulates energy balance in obese mice. Cell 138, 961-975
36. Hansen, J. B., Jørgensen, C., Petersen, R. K., Hallenborg, P., De Matteis, R., Bøye, H. A., Petrovic, N., Enerbäck, S., Nedergaard, J., Cinti, S., te Riele, H., and Kristiansen, K. (2004) Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc. Natl. Acad. Sci. U.S.A. 101, 4112-4117 (Pubitemid 38405892)
37. Singh, R., Xiang, Y., Wang, Y., Baikati, K., Cuervo, A. M., Luu, Y. K., Tang, Y., Pessin, J. E., Schwartz, G. J., and Czaja, M. J. (2009) Autophagy regulates adipose mass and differentiation in mice. J. Clin. Invest. 119, 3329-3339
38. Toh, S. Y., Gong, J., Du, G., Li, J. Z., Yang, S., Ye, J., Yao, H., Zhang, Y., Xue, B., Li, Q., Yang, H., Wen, Z., and Li, P. (2008) Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of fsp27 deficient mice. PLoS One 3, e2890
39. Vegiopoulos, A., Müller-Decker, K., Strzoda, D., Schmitt, I., Chichelnitskiy, E., Ostertag, A., Berriel Diaz, M., Rozman, J., Hrabe de Angelis, M., Nüsing, R. M., Meyer, C. W., Wahli, W., Klingenspor, M., and Herzig, S. (2010) Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science 328, 1158-1161
40. Lu, Y. C., Kim, I., Lye, E., Shen, F., Suzuki, N., Suzuki, S., Gerondakis, S., Akira, S., Gaffen, S. L., Yeh, W. C., and Ohashi, P. S. (2009) Differential role for c-Rel and C/EBPβ/δ in TLR-mediated induction of proinflammatory cytokines. J. Immunol. 182, 7212-7221
41. Cloutier, A., Guindi, C., Larivée, P., Dubois, C. M., Amrani, A., and McDonald, P. P. (2009) Inflammatory cytokine production by human neutrophils involves C/EBP transcription factors. J. Immunol. 182, 563-571
42. Ricote, M., Li, A. C., Willson, T. M., Kelly, C. J., and Glass, C. K. (1998) The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391, 79-82 (Pubitemid 28079218)
43. Vandanmagsar, B., Youm, Y. H., Ravussin, A., Galgani, J. E., Stadler, K., Mynatt, R. L., Ravussin, E., Stephens, J. M., and Dixit, V. D. (2011) The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179-188
44. Tsai, V. W., Mohammad, M. G., Tolhurst, O., Breit, S. N., Sawchenko, P. E., and Brown, D. A. (2011) CCAAT/enhancer binding protein-δ expression by dendritic cells regulates CNS autoimmune inflammatory disease. J. Neurosci. 31, 17612-17621
45. Tanaka, T., Yoshida, N., Kishimoto, T., and Akira, S. (1997) Defective adipocyte differentiation in mice lacking the C/EBPβ and/or C/EBPδ gene. EMBO J. 16, 7432-7443 (Pubitemid 28010503)
46. Fan, W., Morinaga, H., Kim, J. J., Bae, E., Spann, N. J., Heinz, S., Glass, C. K., and Olefsky, J. M. (2010) FoxO1 regulates Tlr4 inflammatory pathway signaling in macrophages. EMBO J. 29, 4223-4236
47. Zelcer, N., and Tontonoz, P. (2006) Liver X receptors as integrators of metabolic and inflammatory signaling. J. Clin. Invest. 116, 607-614 (Pubitemid 43326865)
48. Laiosa, C. V., Stadtfeld, M., Xie, H., de Andres-Aguayo, L., and Graf, T. (2006) Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU.1 transcription factors. Immunity 25, 731-744 (Pubitemid 46107288)
49. Xie, H., Ye, M., Feng, R., and Graf, T. (2004) Stepwise reprogramming of B cells into macrophages. Cell 117, 663-676 (Pubitemid 38692531)
50. Bené, H., Lasky, D., and Ntambi, J. M. (2001) Cloning and characterization of the human stearoyl-CoA desaturase gene promoter: transcriptional activation by sterol regulatory element binding protein and repression by polyunsaturated fatty acids and cholesterol. Biochem. Biophys. Res. Commun. 284, 1194-1198 (Pubitemid 32917965)
51. Hui, T. Y., Frohnert, B. I., Smith, A. J., Schaffer, J. E., and Bernlohr, D. A. (1998) Characterization of the murine fatty acid transport protein gene and its insulin response sequence. J. Biol. Chem. 273, 27420-27429 (Pubitemid 28500460)
52. Tae, H. J., Luo, X., and Kim, K. H. (1994) Roles of CCAAT/enhancer- binding protein and its binding site on repression and derepression of acetyl-CoA carboxylase gene. J. Biol. Chem. 269, 10475-10484 (Pubitemid 24198245)
53. Erbay, E., Babaev, V. R., Mayers, J. R., Makowski, L., Charles, K. N., Snitow, M. E., Fazio, S., Wiest, M. M., Watkins, S. M., Linton, M. F., and Hotamisligil, G. S. (2009) Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat. Med. 15, 1383-1391
54. Boden, G., and Shulman, G. I. (2002) Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur. J. Clin. Invest. 32, 14-23 (Pubitemid 41704996)
55. Seimon, T. A., Nadolski, M. J., Liao, X., Magallon, J., Nguyen, M., Feric, N. T., Koschinsky, M. L., Harkewicz, R., Witztum, J. L., Tsimikas, S., Golenbock, D., Moore, K. J., and Tabas, I. (2010) Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab. 12, 467-482
56. Bensinger, S. J., Bradley, M. N., Joseph, S. B., Zelcer, N., Janssen, E. M., Hausner, M. A., Shih, R., Parks, J. S., Edwards, P. A., Jamieson, B. D., and Tontonoz, P. (2008) LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 134, 97-111 (Pubitemid 351905740)
57. Im, S. S., Yousef, L., Blaschitz, C., Liu, J. Z., Edwards, R. A., Young, S. G., Raffatellu, M., and Osborne, T. F. (2011) Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell Metab. 13, 540-549
58. Schenk, S., Saberi, M., and Olefsky, J. M. (2008) Insulin sensitivity: modulation by nutrients and inflammation. J. Clin. Invest. 118, 2992-3002
59. Gregor, M. F., and Hotamisligil, G. S. (2011) Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29, 415-445
60. Bennett, C. E., Nsengimana, J., Bostock, J. A., Cymbalista, C., Futers, T. S., Knight, B. L., McCormack, L. J., Prasad, U. K., Riches, K., Rolton, D., Scarrott, T., Barrett, J. H., and Carter, A. M. (2010) Diab. Vasc. Dis. Res. 7, 195-203
61. Wang, L. H., Yang, X. Y., Zhang, X., and Farrar, W. L. (2007) Inhibition of adhesive interaction between multiple myeloma and bone marrow stromal cells by PPARγ cross talk with NF-kappaB and C/EBP. Blood 110, 4373-4384 (Pubitemid 351377804)