Toll-like receptor agonists promote prolonged triglyceride storage in macrophages

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 3001-3012

  Huang, Ying Ling ^a   Morales Rosado, Joel ^a   Ray, Jessica ^a   Myers, Timothy G ^b   Kho, Terry ^a   Lu, Mingfang ^a,c   Munford, Robert S ^a  

^a Laboratory of Clinical Infectious Diseases   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACSL; ACYL-COA SYNTHETASE; ADIPOSE TRIGLYCERIDE LIPASE; DGAT2; LIPID DROPLET; LIPOLYSIS; LIPOPOLYSACCHARIDE (LPS); MACROPHAGES; TOLL-LIKE RECEPTORS (TLR); TRIGLYCERIDE;

ANIMALS; CELLS, CULTURED; COENZYME A LIGASES; DIACYLGLYCEROL O-ACYLTRANSFERASE; FATTY ACIDS; FOAM CELLS; HUMANS; LIPOLYSIS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TRIGLYCERIDES;

EID: 84893444919     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.524587     Document Type: Article

References (34)

1. Bozza, P. T., Magalhães, K. G., and Weller, P. F. (2009) Leukocyte lipid bodies-Biogenesis and functions in inflammation. Biochim. Biophys. Acta 1791, 540-551
2. Kim, M. J., Wainwright, H. C., Locketz, M., Bekker, L. G., Walther, G. B., Dittrich, C., Visser, A., Wang, W., Hsu, F. F., Wiehart, U., Tsenova, L., Kaplan, G., and Russell, D. G. (2010) Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol. Med. 2, 258-274
3. Newsholme, P., Curi, R., Gordon, S., and Newsholme, E. A. (1986) Metabolism of glucose, glutamine, long chain fatty acids and ketone bodies by murine macrophages. Biochem. J. 239, 121-125
4. Newsholme, E. A., and Crabtree, B. (1976) Substrate cycles in metabolic regulation and in heat generation. Biochem. Soc. Symp. 41, 61-109
5. Funk, J. L., Feingold, K. R., Moser, A. H., and Grunfeld, C. (1993) Lipopolysaccharide stimulation of RAW 264. 7 macrophages induces lipid accumulation and foam cell formation. Atherosclerosis 98, 67-82
6. Feingold, K. R., Shigenaga, J. K., Kazemi, M. R., McDonald, C. M., Patzek, S. M., Cross, A. S., Moser, A., and Grunfeld, C. (2012) Mechanisms of triglyceride accumulation in activated macrophages. J. Leukocyte Biol. 92, 829-839
7. Munford, R. S., De Veaux, L. C., Cronan, J. E., Jr., and Rick, P. D. (1992) Biosynthetic radiolabeling of bacterial lipopolysaccharide to high specific activity. J. Immunol. Methods 148, 115-120
8. Lu, M., Zhang, M., Kitchens, R. L., Fosmire, S., Takashima, A., and Munford, R. S. (2003) Stimulus-dependent deacylation ofbacterial lipopolysaccharide by dendritic cells. J. Exp. Med. 197, 1745-1754
9. Tansey, J. T., Huml, A. M., Vogt, R., Davis, K. E., Jones, J. M., Fraser, K. A., Brasaemle, D. L., Kimmel, A. R., and Londos, C. (2003) Functional studies on native and mutated forms of perilipins. A role in protein kinase A-mediated lipolysis of triacylglycerols. J. Biol. Chem. 278, 8401-8406
10. Saraswathi, V., and Hasty, A. H. (2009) Inhibition of long chain acyl coenzyme a synthetases during fatty acid loading induces lipotoxicityinmacrophages. Arterioscler. Thromb. Vasc. Biol. 29, 1937-1943
11. Igal, R. A., Wang, P., and Coleman, R. A. (1997) Triacsin C blocks de novo synthesis of glycerolipids and cholesterol esters but not recycling of fatty acid into phospholipid: evidence for functionally separate pools of acyl-CoA. Biochem. J. 324, 529-534
12. Deberardinis, R. J., Lum, J. J., and Thompson, C. B. (2006) Phosphatidylinositol 3-kinase-dependent modulation of carnitine palmitoyltransferase 1A expression regulates lipid metabolism during hematopoietic cell growth. J. Biol. Chem. 281, 37372-37380
13. Krawczyk, C. M., Holowka, T., Sun, J., Blagih, J., Amiel, E., De Berardinis, R. J., Cross, J. R., Jung, E., Thompson, C. B., Jones, R. G., and Pearce, E. J. (2010) Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115, 4742-4749
14. Rubinow, K. B., Wall, V. Z., Nelson, J., Mar, D., Bomsztyk, K., Askari, B., Lai, M. A., Smith, K. D., Han, M. S., Vivekanandan-Giri, A., Pennathur, S., Albert, C. J., Ford, D. A., Davis, R. J., and Bornfeldt, K. E. (2013) Acyl-CoA synthetase 1 is induced by Gram-negative bacteria and lipopolysaccharide and is required for phospholipid turnover in stimulated macrophages. J. Biol. Chem. 288, 9957-9970
15. Newsholme, P., and Newsholme, E. A. (1989) Rates of utilization of glucose, glutamine and oleate and formation of end-products by mouse peritoneal macrophages in culture. Biochem. J. 261, 211-218
16. Soupene, E., and Kuypers, F. A. (2008) Mammalian long chain acyl-CoA synthetases. Exp. Biol. Med. 233, 507-521
17. Arias-Barrau, E., Dirusso, C. C., and Black, P. N. (2009) Methods to monitor fatty acid transport proceeding through vectorial acylation. Methods Mol. Biol. 580, 233-249
18. Nye, C., Kim, J., Kalhan, S. C., and Hanson, R. W. (2008) Reassessing triglyceride synthesis in adipose tissue. Trends Endocrinol. Metab. 19, 356-361
19. Prentki, M., and Madiraju, S. R. (2008) Glycerolipid metabolism and signaling in health and disease. Endocr. Rev. 29, 647-676
20. Adler-Wailes, D. C., Guiney, E. L., Wolins, N. E., and Yanovski, J. A. (2010) Long term ritonavir exposure increases fatty acid and glycerol recycling in 3T3-L1 adipocytes as compensatory mechanisms for increased triacylglycerol hydrolysis. Endocrinology 151, 2097-2105
21. Ghosn, E. E., Cassado, A. A., Govoni, G. R., Fukuhara, T., Yang, Y., Monack, D. M., Bortoluci, K. R., Almeida, S. R., Herzenberg, L. A., and Herzenberg, L. A. (2010) Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. U. S. A. 107, 2568-2573
22. Newsholme, P., Gordon, S., and Newsholme, E. A. (1987) Rates of utilization and fates of glucose, glutamine, pyruvate, fatty acids and ketone bodies by mouse macrophages. Biochem. J. 242, 631-636
23. Loike, J. D., Kaback, E., Silverstein, S. C., and Steinberg, T. H. (1993) Lactate transport in macrophages. J. Immunol. 150, 1951-1958
24. Maurya, M. R., Gupta, S., Li, X., Fahy, E., Dinasarapu, A. R., Sud, M., Brown, H. A., Glass, C. K., Murphy, R. C., Russell, D. W., Dennis, E. A., and Subramaniam, S. (2013) Analysis of inflammatory and lipid metabolic networks across RAW264. 7 and thioglycolate-elicited macrophages. J. Lipid Res. 54, 2525-2542
25. Feingold, K. R., Kazemi, M. R., Magra, A. L., McDonald, C. M., Chui, L. G., Shigenaga, J. K., Patzek, S. M., Chan, Z. W., Londos, C., and Grunfeld, C. (2010) ADRP/ADFP and Mal1 expression are increased in macrophages treated with TLR agonists. Atherosclerosis 209, 81-88
26. Kazemi, M. R., McDonald, C. M., Shigenaga, J. K., Grunfeld, C., and Feingold, K. R. (2005) Adipocyte fatty acid-binding protein expression and lipid accumulation are increased during activation of murine macrophages by toll-like receptor agonists. Arterioscler. Thromb. Vasc. Biol. 25, 1220-1224
27. Li, L. O., Klett, E. L., and Coleman, R. A. (2010) Acyl-CoA synthesis, lipid metabolism and lipotoxicity. Biochim. Biophys. Acta 1801, 246-251
28. 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
29. Namatame, I., Tomoda, H., Arai, H., Inoue, K., and Omura, S. (1999) Complete inhibition of mouse macrophage-derived foam cell formation by triacsin C. J. Biochem. 125, 319-327
30. D'Avila, H., Melo, R. C., Parreira, G. G., Werneck-Barroso, E., Castro-Faria-Neto, H. C., and Bozza, P. T. (2006) Mycobacterium bovis bacillus Calmette-Guerin induces TLR2-mediated formation of lipid bodies: intracellular domains for eicosanoid synthesis in vivo. J. Immunol. 176, 3087-3097
31. 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
32. Nilsson, R., Bajic, V. B., Suzuki, H., Di Bernardo, D., Björkegren, J., Katayama, S., Reid, J. F., Sweet, M. J., Gariboldi, M., Carninci, P., Hayashizaki, Y., Hume, D. A., Tegner, J., and Ravasi, T. (2006) Transcriptional network dynamics in macrophage activation. Genomics 88, 133-142
33. Nicolaou, G., Goodall, A. H., and Erridge, C. (2012) Diverse bacteria promote macrophage foam cell formation via toll-like receptor-dependent lipid body biosynthesis. J. Atheroscler. Thromb. 19, 137-148
34. Spann, N. J., Garmire, L. X., McDonald, J. G., Myers, D. S., Milne, S. B., Shibata, N., Reichart, D., Fox, J. N., Shaked, I., Heudobler, D., Raetz, C. R., Wang, E. W., Kelly, S. L., Sullards, M. C., Murphy, R. C., Merrill, A. H., Jr., Brown, H. A., Dennis, E. A., Li, A. C., Ley, K., Tsimikas, S., Fahy, E., Subramaniam, S., Quehenberger, O., Russell, D. W., and Glass, C. K. (2012) Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 151, 138-152