Acyl-CoA synthetase 1 Is induced by gram-negative bacteria and lipopolysaccharide and is required for phospholipid turnover in stimulated macrophages

Journal of Biological Chemistry

Volumn 288, Issue 14, 2013, Pages 9957-9970

  Rubinow, Katya B ^a   Wall, Valerie Z ^a   Nelson, Joel ^a   Mar, Daniel ^a   Bomsztyk, Karol ^a   Askari, Bardia ^a   Lai, Marvin A ^a   Smith, Kelly D ^a   Han, Myoung Sook ^b   Vivekanandan Giri, Anuradha ^c   Pennathur, Subramaniam ^c   Albert, Carolyn J ^d   Ford, David A ^d   Davis, Roger J ^b   Bornfeldt, Karin E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; GRAM-NEGATIVE BACTERIA; INNATE IMMUNE RESPONSE; MYELOID DIFFERENTIATION; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; SIGNAL TRANSDUCTION PATHWAYS; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

BACTERIA; CYTOLOGY; ENZYMES; HISTOLOGY; INSULIN; PHOSPHOLIPIDS; SIGNAL TRANSDUCTION; TISSUE; TRANSCRIPTION;

MACROPHAGES;

GAMMA INTERFERON; LONG CHAIN FATTY ACID COENZYME A LIGASE; LONG CHAIN FATTY ACID COENZYME A LIGASE 1; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHOLIPID; ROSIGLITAZONE; STAT1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVATION; ESCHERICHIA COLI; FATTY ACID OXIDATION; FEMALE; GENE EXPRESSION PROFILING; GRAM NEGATIVE BACTERIUM; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE;

ANIMALS; BONE MARROW CELLS; COENZYME A LIGASES; FEMALE; GRAM-NEGATIVE BACTERIA; IMMUNITY, INNATE; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; MACROPHAGES; MACROPHAGES, PERITONEAL; MALE; MAP KINASE KINASE 4; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PHOSPHOLIPIDS; SIGNAL TRANSDUCTION;

NEGIBACTERIA;

EID: 84875967687     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.458372     Document Type: Article

References (50)

1. Mashek, D. G., Li, L. O., and Coleman, R. A. (2006) Rat long-chain acyl- CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet. J. Lipid Res. 47, 2004-2010
2. Suzuki, H., Kawarabayasi, Y., Kondo, J., Abe, T., Nishikawa, K., Kimura, S., Hashimoto, T., and Yamamoto, T. (1990) Structure and regulation of rat long-chain acyl-CoA synthetase. J. Biol. Chem. 265, 8681-8685
3. Lobo, S., Wiczer, B. M., and Bernlohr, D. A. (2009) Functional analysis of long-chain acyl-CoA synthetase 1 in 3T3-L1 adipocytes. J. Biol. Chem. 284, 18347-18356
4. de Jong, H., Neal, A. C., Coleman, R. A., and Lewin, T. M. (2007) Ontogeny of mRNA expression and activity of long-chain acyl-CoA synthetase (ACSL) isoforms in Mus musculus heart. Biochim. Biophys. Acta 1771, 75-82
5. Fujimoto, Y., Onoduka, J., Homma, K. J., Yamaguchi, S., Mori, M., Higashi, Y., Makita, M., Kinoshita, T., Noda, J., Itabe, H., and Takanoa, T. (2006) Long-chain fatty acids induce lipid droplet formation in a cultured human hepatocyte in a manner dependent of acyl-CoA synthetase. Biol. Pharm. Bull. 29, 2174-2180
6. Coleman, R. A., Lewin, T. M., Van Horn, C. G., and Gonzalez-Baró, M. R. (2002) Do long-chain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J. Nutr. 132, 2123-2126
7. Li, L. O., Ellis, J. M., Paich, H. A., Wang, S., Gong, N., Altshuller, G., Thresher, R. J., Koves, T. R., Watkins, S. M., Muoio, D. M., Cline, G. W., Shulman, G. I., and Coleman, R. A. (2009) Liver-specific loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and β-oxidation and alters phospholipid fatty acid composition. J. Biol. Chem. 284, 27816-27826
8. Ellis, J. M., Li, L. O., Wu, P. C., Koves, T. R., Ilkayeva, O., Stevens, R. D., Watkins, S. M., Muoio, D. M., and Coleman, R. A. (2010) Adipose acyl- CoA synthetase-1 directs fatty acids toward β-oxidation and is required for cold thermogenesis. Cell Metab. 12, 53-64
9. Ellis, J. M., Mentock, S. M., Depetrillo, M. A., Koves, T. R., Sen, S., Watkins, S. M., Muoio, D. M., Cline, G. W., Taegtmeyer, H., Shulman, G. I., Willis, M. S., and Coleman, R. A. (2011) Mouse cardiac acyl coenzyme a synthetase 1 deficiency impairs fatty acid oxidation and induces cardiac hypertrophy. Mol. Cell. Biol. 31, 1252-1262
10. Rakhshandehroo, M., Hooiveld, G., Müller, M., and Kersten, S. (2009) Comparative analysis of gene regulation by the transcription factor PPARα between mouse and human. PLoS One 4, e6796
11. Schoonjans, K., Watanabe, M., Suzuki, H., Mahfoudi, A., Krey, G., Wahli, W., Grimaldi, P., Staels, B., Yamamoto, T., and Auwerx, J. (1995) Induction of the acyl-coenzyme A synthetase gene by fibrates and fatty acids is mediated by a peroxisome proliferator response element in the C promoter. J. Biol. Chem. 270, 19269-19276
12. Schoonjans, K., Staels, B., Grimaldi, P., and Auwerx, J. (1993) Acyl-CoA synthetasemRNAexpression is controlled by fibric-acid derivatives, feeding and liver proliferation. Eur. J. Biochem. 216, 615-622
13. Martin, G., Schoonjans, K., Lefebvre, A. M., Staels, B., and Auwerx, J. (1997) Coordinate regulation of the expression of the fatty acid transport protein and acyl-CoA synthetase genes by PPARα and PPARγ activators. J. Biol. Chem. 272, 28210-28217
14. Kanter, J. E., Kramer, F., Barnhart, S., Averill, M. M., Vivekanandan-Giri, A., Vickery, T., Li, L. O., Becker, L., Yuan, W., Chait, A., Braun, K. R., Potter-Perigo, S., Sanda, S., Wight, T. N., Pennathur, S., Serhan, C. N., Heinecke, J. W., Coleman, R. A., and Bornfeldt, K. E. (2012) Diabetes promotes an inflammatory macrophage phenotype and atherosclerosis through acyl-CoA synthetase 1. Proc. Natl. Acad. Sci. U.S.A. 109, E715-E724
15. Das, M., Sabio, G., Jiang, F., Rincón, M., Flavell, R. A., and Davis, R. J. (2009) Induction of hepatitis by JNK-mediated expression of TNF-α. Cell 136, 249-260
16. Han, M. S., Jung, D. Y., Morel, C., Lakhani, S. A., Kim, J. K., Flavell, R. A., and Davis, R. J. (2013) JNK expression by macrophages promotes obesityinduced insulin resistance and inflammation. Science 339, 218-222
17. Hoshino, K., Takeuchi, O., Kawai, T., Sanjo, H., Ogawa, T., Takeda, Y., Takeda, K., and Akira, S. (1999) Cutting edge. Toll-like receptor 4 (TLR4)- deficient mice are hyporesponsive to lipopolysaccharide. Evidence for TLR4 as the Lps gene product. J. Immunol. 162, 3749-3752
18. Hawn, T. R., Smith, K. D., Aderem, A., and Skerrett, S. J. (2006) Myeloid differentiation primary response gene (88)- and Toll-like receptor 2-deficient mice are susceptible to infection with aerosolized Legionella pneumophila. J. Infect. Dis. 193, 1693-1702
19. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K., and Akira, S. (2003) Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301, 640-643
20. Hoiseth, S. K., and Stocker, B. A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238-239
21. Flanagin, S., Nelson, J. D., Castner, D. G., Denisenko, O., and Bomsztyk, K. (2008) Microplate-based chromatin immunoprecipitation method, matrix ChIP. A platform to study signaling of complex genomic events. Nucleic Acids Res. 36, e17
22. Das, M., Jiang, F., Sluss, H. K., Zhang, C., Shokat, K. M., Flavell, R. A., and Davis R. J. (2007) Suppression of p53-dependent senescence by the JNK signal transduction pathway. Proc. Natl. Acad. Sci. U.S.A. 104, 15759-15764
23. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
24. Ford, D. A., Monda, J. K., Brush, R. S., Anderson, R. E., Richards, M. J., and Fliesler, S. J. (2008) Lipidomic analysis of the retina in a rat model of Smith-Lemli-Opitz syndrome. Alterations in docosahexaenoic acid content of phospholipid molecular species. J. Neurochem. 105, 1032-1047
25. Han, X., and Gross, R. W. (2005) Shotgun lipidomics. Electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24, 367-412
26. Han, X. (2002) Characterization and direct quantitation of ceramide molecular species from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry. Anal. Biochem. 302, 199-212
27. Wagner, J. D., Shadoan, M. K., Zhang, L., Ward, G. M., Royer, L. J., Kavanagh, K., Francone, O. L., Auerbach, B. J., and Harwood, H. J., Jr. (2010) A selective peroxisome proliferator-activated receptor α agonist, CP- 900691, improves plasma lipids, lipoproteins, and glycemic control in diabetic monkeys. J. Pharmacol. Exp. Ther. 333, 844-853
28. Beutler, B., Hoebe, K., Du, X., and Ulevitch, R. J. (2003) How we detect microbes and respond to them. The Toll-like receptors and their transducers. J. Leukoc. Biol. 74, 479-485
29. Suram, S., Gangelhoff, T. A., Taylor, P. R., Rosas, M., Brown, G. D., Bonventre, J. V., Akira, S., Uematsu, S., Williams, D. L., Murphy, R. C., and Leslie, C. C. (2010) Pathways regulating cytosolic phospholipase A2 activation and eicosanoid production in macrophages by Candida albicans. J. Biol. Chem. 285, 30676-30685
30. Pålsson-McDermott, E. M., and O'Neill, L. A. (2004) Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 113, 153-162
31. Davis, R. J. (2000) Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252
32. Kang, Y. J., Chen, J., Otsuka, M., Mols, J., Ren, S., Wang, Y., and Han, J. (2008) Macrophage deletion of p38α partially impairs lipopolysaccharideinduced cellular activation. J. Immunol. 180, 5075-5082
33. Schieven, G. L. (2005) The biology of p38 kinase. A central role in inflammation. Curr. Top. Med. Chem. 5, 921-928
34. Bogoyevitch, M. A., Boehm, I., Oakley, A., Ketterman, A. J., and Barr, R. K. (2004) Targeting the JNK MAPK cascade for inhibition. Basic science and therapeutic potential. Biochim. Biophys. Acta 1697, 89-101
35. Ma, W., Gee, K., Lim, W., Chambers, K., Angel, J. B., Kozlowski, M., and Kumar, A. (2004) Dexamethasone inhibits IL-12p40 production in lipopolysaccharide- stimulated human monocytic cells by down-regulating the activity of c-Jun N-terminal kinase, the activation protein-1, and NF-κB transcription factors. J. Immunol. 172, 318-330
36. Hale, K. K., Trollinger, D., Rihanek, M., and Manthey, C. L. (1999) Differential expression and activation of p38 mitogen-activated protein kinase α, β, γ, and δ in inflammatory cell lineages. J. Immunol. 162, 4246-4252
37. Comalada, M., Lloberas, J., and Celada, A. (2012) MKP-1. A critical phosphatase in the biology of macrophages controlling the switch between proliferation and activation. Eur. J. Immunol. 42, 1938-1948
38. Maloney, N. S., Thackray, L. B., Goel, G., Hwang, S., Duan, E., Vachharajani, P., Xavier, R., and Virgin, H. W. (2012) Essential cell-autonomous role for interferon (IFN) regulatory factor 1 in IFN-γ-mediated inhibition of norovirus replication in macrophages. J. Virol. 86, 12655-12664
39. Sato, S., Sugiyama, M., Yamamoto, M., Watanabe, Y., Kawai, T., Takeda, K., and Akira, S. (2003) Toll/IL-1 receptor domain-containing adaptor inducing IFN-β (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1 and activates two distinct transcription factors, NF-κB and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171, 4304-4310
40. Lefterova, M. I., Steger, D. J., Zhuo, D., Qatanani, M., Mullican, S. E., Tuteja, G., Manduchi, E., Grant, G. R., and Lazar, M. A. (2010) Cellspecific determinants of peroxisome proliferator-activated receptor γ function in adipocytes and macrophages. Mol. Cell. Biol. 30, 2078-2089
41. Mullican, S. E., Gaddis, C. A., Alenghat, T., Nair, M. G., Giacomin, P. R., Everett, L. J., Feng, D., Steger, D. J., Schug, J., Artis, D., and Lazar, M. A. (2011) Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev. 25, 2480-2488
42. Ho, H. H., Antoniv, T. T., Ji, J. D., and Ivashkiv, L. B. (2008) Lipopolysaccharide- induced expression of matrix metalloproteinases in human monocytes is suppressed by IFN-γ via superinduction of ATF-3 and suppression of AP-1. J. Immunol. 181, 5089-5097
43. Cuenda, A., and Rousseau, S. (2007) p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 1773, 1358-1375
44. Han, J., Jiang, Y., Li, Z., Kravchenko, V. V., and Ulevitch, R. J. (1997) Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386, 296-299
45. Utsugi, M., Dobashi, K., Ono, A., Ishizuka, T., Hisada, T., Koga, Y., Shimizu, Y., Kawata, T., Matsuzaki, S., Aoki, H., Kamide, Y., and Mori, M. (2010) JNK1 and JNK2 differently regulate IL-12 production in THP-1 macrophage cells. Cytokine 51, 127-131
46. Sánchez-Tilló, E., Comalada, M., Xaus, J., Farrera, C., Valledor, A. F., Caelles, C., Lloberas, J., and Celada, A. (2007) JNK1 Is required for the induction ofMkp1expression in macrophages during proliferationandlipopolysaccharide- dependent activation. J. Biol. Chem. 282, 12566-12573
47. Zhu, J., Krishnegowda, G., and Gowda, D. C. (2005) Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum. The requirement of extracellular signalregulated kinase, p38, c-Jun N-terminal kinase and NF-κB pathways for the expression of proinflammatory cytokines and nitric oxide. J. Biol. Chem. 280, 8617-8627
48. Lazear, H. M., Lancaster, A., Wilkins, C., Suthar, M. S., Huang, A., Vick, S. C., Clepper, L., Thackray, L., Brassil, M. M., Virgin, H. W., Nikolich- Zugich, J., Moses, A. V., Gale, M. Jr., Früh, K., and Diamond, M. S. (2013) IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog. 9, e1003118
49. Ruiz-García, A., Monsalve, E., Novellasdemunt, L., Navarro-Sabaté, A., Manzano, A., Rivero, S., Castrillo, A., Casado, M., Laborda, J., Bartrons, R., and Díaz-Guerra, M. J. (2011) Cooperation of adenosine with macrophage Toll-4 receptor agonists leads to increased glycolytic flux through the enhanced expression of PFKFB3 gene. J. Biol. Chem. 286, 19247-19258
50. Schwartz, E. A., Zhang, W. Y., Karnik, S. K., Borwege, S., Anand, V. R., Laine, P. S., Su, Y., and Reaven, P. D. (2010) Nutrient modification of the innate immune response. A novel mechanism by which saturated fatty acids greatly amplify monocyte inflammation. Arterioscler. Thromb. Vasc. Biol. 30, 802-808