Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a

Cell Metabolism

Volumn 13, Issue 5, 2011, Pages 540-549

  Im, Seung Soon ^a,b   Yousef, Leyla ^b   Blaschitz, Christoph ^c   Liu, Janet Z ^c   Edwards, Robert A ^c   Young, Stephen G ^d   Raffatellu, Manuela ^c   Osborne, Timothy F ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; LIPID; LIPOPOLYSACCHARIDE; NLRP1A PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; GENE TARGETING; INNATE IMMUNITY; LIPID METABOLISM; LIPOGENESIS; MACROPHAGE; MALE; MOUSE; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPTIC SHOCK; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; BONE MARROW; CASPASE 1; CYTOKINES; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNITY, INNATE; INFLAMMASOMES; INTERLEUKIN-1BETA; LIPID METABOLISM; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

BACTERIA (MICROORGANISMS); MUS;

EID: 79955632319     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.04.001     Document Type: Article

References (48)

1. Boyden, E.D., and Dietrich, W.F. (2006). Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38, 240-244.
2. Broz, P., Newton, K., Lamkanfi, M., Mariathasan, S., Dixit, V.M., and Monack, D.M. (2010). Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J. Exp. Med. 207, 1745-1755.
3. Castoreno, A.B., Wang, Y., Stockinger, W., Jarzylo, L.A., Du, H., Pagnon, J.C., Shieh, E.C., and Nohturfft, A. (2005). Transcriptional regulation of phagocytosis- induced membrane biogenesis by sterol regulatory element binding proteins. Proc. Natl. Acad. Sci. USA 102, 13129-13134.
4. Cordoba-Rodriguez, R., Fang, H., Lankford, C.S., and Frucht, D.M. (2004). Anthrax lethal toxin rapidly activates caspase-1/ICE and induces extracellular release of interleukin (IL)-1beta and IL-18. J. Biol. Chem. 279, 20563-20566.
5. Delano, M.J., Scumpia, P.O., Weinstein, J.S., Coco, D., Nagaraj, S., Kelly-Scumpia, K.M., O'Malley, K.A., Wynn, J.L., Antonenko, S., Al-Quran, S.Z., et al. (2007). MyD88-dependent expansion of an immature GR-1(+) CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 204, 1463-1474.
6. Fantuzzi, G., Zheng, H., Faggioni, R., Benigni, F., Ghezzi, P., Sipe, J.D., Shaw, A.R., and Dinarello, C.A. (1996). Effect of endotoxin in IL-1 beta-deficient mice. J. Immunol. 157, 291-296. (Pubitemid 26190560)
7. Franchi, L., Eigenbrod, T., Munoz-Planillo, R., and Nunez, G. (2009). The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10, 241-247.
8. Ghisletti, S., Huang, W., Ogawa, S., Pascual, G., Lin, M.E., Willson, T.M., Rosenfeld, M.G., and Glass, C.K. (2007). Parallel SUMOylation-dependent pathways mediate gene- and signal-specific transrepression by LXRs and PPARgamma. Mol. Cell 25, 57-70. (Pubitemid 46049061)
9. Gilchrist, M., Thorsson, V., Li, B., Rust, A.G., Korb, M., Roach, J.C., Kennedy, K., Hai, T., Bolouri, H., and Aderem, A. (2006). Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441, 173-178.
10. Gu, Y., Kuida, K., Tsutsui, H., Ku, G., Hsiao, K., Fleming, M.A., Hayashi, N., Higashino, K., Okamura, H., Nakanishi, K., et al. (1997). Activation of interferon- gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 275, 206-209. (Pubitemid 27034760)
11. Gurcel, L., Abrami, L., Girardin, S., Tschopp, J., and van der Goot, F.G. (2006). Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126, 1135-1145. (Pubitemid 44380297)
12. Horton, J.D., Bashmakov, Y., Shimomura, I., and Shimano, H. (1998). Regulation of sterol regulatory element binding proteins in livers of fasted and refed mice. Proc. Natl. Acad. Sci. USA 95, 5987-5992.
13. Horton, J.D., Goldstein, J.L., and Brown, M.S. (2002). SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131.
14. Hughes, A.L., Todd, B.L., and Espenshade, P.J. (2005). SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 120, 831-842. (Pubitemid 40568800)
15. Ianaro, A., Tersigni, M., and D'Acquisto, F. (2009). New insight in LPS antagonist. Mini Rev. Med. Chem. 9, 306-317.
16. Im, S.S., Hammond, L.E., Yousef, L., Nugas-Selby, C., Shin, D.J., Seo, Y.K., Fong, L.G., Young, S.G., and Osborne, T.F. (2009). Sterol regulatory element binding protein 1a regulates hepatic fatty acid partitioning by activating acetyl coenzyme A carboxylase 2. Mol. Cell. Biol. 29, 4864-4872.
17. Jeon, T.I., Zhu, B., Larson, J.L., and Osborne, T.F. (2008). SREBP-2 regulates gut peptide secretion through intestinal bitter taste receptor signaling in mice. J. Clin. Invest. 118, 3693-3700.
18. Joseph, S.B., Castrillo, A., Laffitte, B.A., Mangelsdorf, D.J., and Tontonoz, P. (2003). Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat. Med. 9, 213-219.
19. Joshi, A.D., Raymond, T., Coelho, A.L., Kunkel, S.L., and Hogaboam, C.M. (2008). A systemic granulomatous response to Schistosoma mansoni eggs alters responsiveness of bone-marrow-derived macrophages to Toll-like receptor agonists. J. Leukoc. Biol. 83, 314-324.
20. Kaisho, T., and Akira, S. (2000). Critical roles of Toll-like receptors in host defense. Crit. Rev. Immunol. 20, 393-405.
21. Kankkunen, P., Rintahaka, J., Aalto, A., Leino, M., Majuri, M.L., Alenius, H., Wolff, H., and Matikainen, S. (2009). Trichothecene mycotoxins activate inflammatory response in human macrophages. J. Immunol. 182, 6418-6425.
22. Kim, J.B., Sarraf, P., Wright, M., Yao, K.M., Mueller, E., Solanes, G., Lowell, B.B., and Speigelman, B.M. (1998). Nutritional and insulin regulation of fatty acid synthetase and leptin gene expression through ADD1/SREBP-1c. J. Clin. Invest. 101, 1-9.
23. Laffitte, B.A., Repa, J.J., Joseph, S.B., Wilpitz, D.C., Kast, H.R., Mangelsdorf, D.J., and Tontonoz, P. (2001). LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl. Acad. Sci. USA 98, 507-512.
24. Lara-Tejero, M., Sutterwala, F.S., Ogura, Y., Grant, E.P., Bertin, J., Coyle, A.J., Flavell, R.A., and Galan, J.E. (2006). Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203, 1407-1412.
25. Li, P., Allen, H., Banerjee, S., Franklin, S., Herzog, L., Johnston, C., McDowell, J., Paskind, M., Rodman, L., Salfeld, J., et al. (1995). Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80, 401-411.
26. Lusis, A.J. (2000). Atherosclerosis. Nature 407, 233-241.
27. Mariathasan, S., Newton, K., Monack, D.M., Vucic, D., French, D.M., Lee, W.P., Roose-Girma, M., Erickson, S., and Dixit, V.M. (2004). Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218. (Pubitemid 38902430)
28. Martinon, F., Gaide, O., Petrilli, V., Mayor, A., and Tschopp, J. (2007). NALP inflammasomes: a central role in innate immunity. Semin. Immunopathol. 29, 213-229.
29. Moreno, S.E., Alves-Filho, J.C., Alfaya, T.M., da Silva, J.S., Ferreira, S.H., and Liew, F.Y. (2006). IL-12, but not IL-18, is critical to neutrophil activation and resistance to polymicrobial sepsis induced by cecal ligation and puncture. J. Immunol. 177, 3218-3224. (Pubitemid 44277840)
30. Osborne, T.F., and Espenshade, P.J. (2009). Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it's been. Genes Dev. 23, 2578-2591.
31. Perkins, N.D., Edwards, N.L., Duckett, C.S., Agranoff, A.B., Schmid, R.M., and Nabel, G.J. (1993). A cooperative interaction between NF-κB and Sp1 is required for HIV-1 enhancer activation. EMBO J. 12, 3551-3558. (Pubitemid 23256442)
32. Posokhova, E.N., Khoshchenko, O.M., Chasovskikh, M.I., Pivovarova, E.N., and Dushkin, M.I. (2008). Lipid synthesis in macrophages during inflammation in vivo: effect of agonists of peroxisome proliferator activated receptors alpha and gamma and of retinoid X receptors. Biochemistry (Mosc.) 73, 296-304. (Pubitemid 351490978)
33. Raffatellu, M., George, M.D., Akiyama, Y., Hornsby, M.J., Nuccio, S.P., Paixao, T.A., Butler, B.P., Chu, H., Santos, R.L., Berger, T., et al. (2009). Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5, 476-486.
34. Remick, D.G., and Ward, P.A. (2005). Evaluation of endotoxin models for the study of sepsis. Shock 24 (Suppl 1 ), 7-11.
35. Repa, J.J., Liang, G., Ou, J., Bashmakov, Y., Lobaccaro, J.M., Shimomura, I., Shan, B., Brown, M.S., Goldstein, J.L., and Mangelsdorf, D.J. (2000). Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 14, 2819-2830.
36. Rittirsch, D., Huber-Lang, M.S., Flierl, M.A., and Ward, P.A. (2009). Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4, 31-36.
37. Ross, R. (1999). Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340, 115-126.
38. Schroder, K., and Tschopp, J. (2010). The inflammasomes. Cell 140, 821-832.
39. Sheng, Z., Otani, H., Brown, M.S., and Goldstein, J.L. (1995). Independent regulation of sterol regulatory element-binding proteins 1 and 2 in hamster liver. Proc. Natl. Acad. Sci. USA 92, 935-938.
40. Shimomura, I., Shimano, H., Horton, J.D., Goldstein, J.L., and Brown, M.S. (1997). Differential expression of exons 1a and 1c in mRNAs for sterol regulatory element binding protein-1 in human and mouse organs and cultured cells. J. Clin. Invest. 99, 838-845.
41. Shin, D.J., and Osborne, T.F. (2003). Thyroid hormone regulation and cholesterol metabolism are connected through Sterol Regulatory Element-Binding Protein-2 (SREBP-2). J. Biol. Chem. 278, 34114-34118.
42. Sutterwala, F.S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G.S., Grant, E.P., Bertin, J., Coyle, A.J., Galan, J.E., Askenase, P.W., and Flavell, R.A. (2006). Critical role for NALP3/CIAS1/ Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327.
43. Venkateswaran, A., Laffitte, B.A., Joseph, S.B., Mak, P.A., Wilpitz, D.C., Edwards, P.A., and Tontonoz, P. (2000). Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXR alpha. Proc. Natl. Acad. Sci. USA 97, 12097-12102.
44. Wagner, B.L., Valledor, A.F., Shao, G., Daige, C.L., Bischoff, E.D., Petrowski, M., Jepsen, K., Baek, S.H., Heyman, R.A., Rosenfeld, M.G., et al. (2003). Promoter-specific roles for liver X receptor/corepressor complexes in the regulation of ABCA1 and SREBP1 gene expression. Mol. Cell. Biol. 23, 5780-5789.
45. Welch, J.S., Ricote, M., Akiyama, T.E., Gonzalez, F.J., and Glass, C.K. (2003). PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc. Natl. Acad. Sci. USA 100, 6712-6717.
46. Witola, W.H., Mui, E., Hargrave, A., Liu, S., Hypolite, M., Montpetit, A., Cavailles, P., Bisanz, C., Cesbron-Delauw, M.F., Fournie, G.J., and McLeod, R. (2010). NALP1 influences susceptibility to human congenital toxoplasmosis, pro-inflammatory cytokine response and fate of T. gondii-infected monocytic cells. Infect. Immun. 79, 756-766.
47. Wu, J., Fernandes-Alnemri, T., and Alnemri, E.S. (2010). Involvement of the AIM2, NLRC4, and NLRP3 inflammasomes in caspase-1 activation by Listeria monocytogenes. J. Clin. Immunol. 30, 693-702.
48. Zhang, C.Z., Shin, D.-J., and Osborne, T.F. (2005). A simple promoter containing two Sp1 sites controls expression of sterol regulatory element binding protein-1a (SREBP-1a). Biochem. J. 386, 1-8.