Differential modulation of Toll-like receptors by fatty acids: Preferential inhibition by n-3 polyunsaturated fatty acids

Journal of Lipid Research

Volumn 44, Issue 3, 2003, Pages 479-486

  Lee, Joo Y ^a   Plakidas, Anthony ^a   Lee, Won H ^a   Heikkinen, Anne ^a   Chanmugam, Prithiva ^a   Bray, George ^a   Hwang, Daniel H ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Cyclooxygenase 2; n 3 polyunsaturated fatty acids; NF B; Toll like receptors; Unsaturated and saturated fatty acids

Indexed keywords

CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACID; FATTY ACID; FISH OIL; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; LUCIFERASE; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; CELL SURFACE RECEPTOR; ISOENZYME; LINOLEIC ACID; MEMBRANE PROTEIN; PROSTAGLANDIN SYNTHASE; PTGS2 PROTEIN, HUMAN; TLR2 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 2; TRIACYLGLYCEROL; UNSATURATED FATTY ACID;

ANIMAL CELL; ARTICLE; DIETARY INTAKE; ENZYME ASSAY; FAT INTAKE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOBLOTTING; MONOCYTE; NONHUMAN; NORMAL HUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REPORTER GENE; ANIMAL; CELL LINE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PROMOTER REGION; RANDOMIZED CONTROLLED TRIAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CYCLOOXYGENASE 2; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; FISH OILS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; LINOLEIC ACID; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MONOCYTES; NF-KAPPA B; PROMOTER REGIONS (GENETICS); PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; TRIGLYCERIDES;

EID: 0038143617     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M200361-JLR200     Document Type: Article

References (59)

1. Medzhitov, R., and C. Janeway, Jr. 2000. The Toll receptor family and microbial recognition. Trends Microbiol. 8: 452-456.
2. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature. 406: 782-787.
3. Heldwein, K. A., D. T. Golenbock, and M. J. Fenton. 2001. Recent advances in the biology of Toll-like receptors. Mod. Asp. Immunobiol. 1: 249-252.
4. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 388: 394-397.
5. Akira, S. 2001. Toll-like receptors and innate immunity. Adv. Immunol. 78: 1-56.
6. Zarember, K. A., and P. J. Godowski. 2002. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol. 168: 554-561.
7. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. V. Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. Freudenberg, P. Ricciardi-Castagnoli, B. Layton, and B. Beutler. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 282: 2085-2088.
8. Qureshi, S. T., L. Lariviere, G. Leveque, S. Clermont, K. J. Moore, P. Gros, and D. Malo. 1999. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J. Exp. Med. 189: 615-625.
9. Rhee, S. H., and D. Hwang. 2000. Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J. Biol. Chem. 275: 34035-34040.
10. Ohashi, K., V. Burkart, S. Flohe, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J. Immunol. 164: 558-561.
11. Okamura, Y., M. Watari, E. S. Jerud, D. W. Young, S. T. Ishizaka, J. Rose, J. C. Chow, and J. F. Strauss 3rd. 2001. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276: 10229-10233.
12. Yoshimura, A., E. Lien, R. R. Ingalls, E. Tuomanen, R. Dziarski, and D. Golenbock. 1999. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163: 1-5.
13. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1: 398-401.
14. Lee, J. Y., K. H. Sohn, S. H. Rhee, and D. Hwang. 2001. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276: 16683-16689.
15. Munford, R. S., and C. L. Hall. 1986. Detoxification of bacterial lipopolysaccharides (endotoxins) by a human neutrophil enzyme. Science. 234: 203-205.
16. Kitchens, R. L., R. J. Ulevitch, and R. S. Munford. 1992. Lipopolysaccharide (LPS) partial structures inhibit responses to LPS in a human macrophage cell line without inhibiting LPS uptake by a CD14- mediated pathway. J. Exp. Med. 176: 485-494.
17. Krauss, J. H., U. Seydel, J. Weckesser, and H. Mayer. 1989. Structural analysis of the nontoxic lipid A of Rhodobacter capsulatus 37b4. Eur. J. Biochem. 180: 519-526.
18. Qureshi, N., K. Takayama, and R. Kurtz. 1991. Diphosphoryl lipid A obtained from the nontoxic lipopolysaccharide of Rhodopseudomonas sphaeroides is an endotoxin antagonist in mice. Infect. Immun. 59: 441-444.
19. Brightbill, H. D., D. H. Libraty, S. R. Krutzik, R. B. Yang, J. T. Belisle, J. R. Bleharski, M. Maitland, M. V. Norgard, S. E. Plevy, S. T. Smale, P.J. Brennan, B. R. Bloom, P. J. Godowski, and R. L. Modlin. 1999. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science. 285: 732-736.
20. Wolf, B., S. Hauschildt, B. Uhl, J. Metzger, G. Jung, and W. G. Bessler. 1989. Localization of the cell activator lipopeptide in bone marrow-derived macrophages by electron energy loss spectroscopy (EELS). Immunol. Lett. 20: 121-126.
21. Uhl, B., V. Speth, B. Wolf, G. Jung, W. G. Bessler, and S. Hauschildt. 1992. Rapid alterations in the plasma membrane structure of macrophages stimulated with bacterial lipopeptides. Eur. J. Cell Biol. 58: 90-98.
22. Endres, S., R. Ghorbani, V. E. Kelley, K. Georgilis, G. Lonnemann, J. W. van der Meer, J. G. Cannon, T. S. Rogers, M. S. Klempner, and P. C. Weber. 1989. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N. Engl. J. Med. 320: 265-271.
23. Endres, S., S. N. Meydani, R. Ghorbani, R. Schindler, and C. A. Dinarello. 1993. Dietary supplementation with n-3 fatty acids suppresses interleukin-2 production and mononuclear cell proliferation. J. Leukoc. Biol. 54: 599-603.
24. Herschman, H. R. 1991. Primary response genes induced by growth factors and tumor promoters. Annu. Rev. Biochem. 60: 281-319.
25. Hwang, D., B. C. Jang, G. Yu, and M. Boudreau. 1997. Expression of mitogen-inducible cyclooxygenase induced by lipopolysaccharide: mediation through both mitogen-activated protein kinase and NF-kappaB signaling pathways in macrophages. Biochem. Pharmacol. 54: 87-96.
26. Paik, J. H., J. H. Ju, J. Y. Lee, M. D. Boudreau, and D. H. Hwang. 2000. Two opposing effects of non-steroidal anti-inflammatory drugs on the expression of the inducible cyclooxygenase. Mediation through different signaling pathways. J. Biol. Chem. 275: 28173-28179.
27. Lee, S. H., E. Soyoola, P. Chanmugam, S. Hart, W. Sun, H. Zhong, S. Liou, D. Simmons, and D. Hwang. 1992. Selective expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide. J. Biol. Chem. 267: 25934-25938.
28. Hwang, D., D. Scollard, J. Byrne, and E. Levine. 1998. Expression of cyclooxygenase-1 and cyclooxygenase-2 in human breast cancer. J. Natl. Cancer Inst. 90: 455-460.
29. Chanmugam, P., L. Feng, S. Liou, B.C. Jang, M. Boudreau, G. Yu, J.H. Lee, H.J. Kwon, T. Beppu, M. Yoshida, Y. Xia, Wilson, B. Curtis, and D. Hwang. 1995. Radicicol, a protein tyrosine kinase inhibitor, suppresses the expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide in an experimental glomerulonephritis. J. Bio. Chem. 270: 5418-5426.
30. Hwang, D., P. Chanmugam, D. H. Ryan, M. Boudreau, M. Windhauser, R. T. Tulley, E. R. Brooks, and G. A. Bray. 1997. Does vegetable oil attenuate the beneficial effects to fish oil reducing risk factors for cardiovascular disease? Am. J. Clin. Nutr. 66: 89-96.
31. McFaul, S. J. 1990. A method for isolating neutrophils from moderate volumes of human blood. J. Immunol. Methods. 130: 15-18.
32. Hajjar, A. M., D. S. O'Mahony, A. Ozinsky, D. M. Underhill, A. Aderem, S. J. Klebanoff, and C. B. Wilson. 2001. Cutting edge: functional interactions between toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol. 166:15-19.
33. Mohrhauer, H., and R. T. Holman. 1963. The effects of dose level of essential fatty acids upon the fatty acid composition of the rat liver. J. Lipid Res. 4: 151-159.
34. Lands, W. E., B. Libelt, A. Morris, N. C. Kramer, T. E. Prewitt, P. Bowen, D. Schmeisser, M. H. Davidson, and J. H. Burns. 1992. Maintenance of lower proportions of (n - 6) eicosanoid precursors in phospholipids of human plasma in response to added dietary (n - 3) fatty acids. Biochim. Biophys. Acta. 1180: 147-162.
35. Sprecher, H. 2000. Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim. Biophys. Acta. 1486: 219-231.
36. Samuelsson, B. 1970. Structures, biosynthesis, and metabolism of prostaglandins. In Lipids Metabolism. S. Wakil, editor. Academic Press, New York. 107.
37. Needleman, P., A. Raz, M. S. Minkes, J. A. Ferrendelli, and H. Sprecher. 1979. Triene prostaglandins: prostacyclin and thromboxane biosynthesis and unique biological properties. Proc. Natl. Acad. Sci. USA. 76:944-948.
38. Smith, W. L. 1992. Prostanoid biosynthesis and mechanisms of action. Am. J. Physiol. 263: F181-F191.
39. Hwang, D. 2000. Fatty acids and immune responses-a new perspective in searching for clues to mechanism. Annu. Rev. Nutr. 20: 431-456.
40. Liu, G., D. M. Bibus, A. M. Bode, W. Y. Ma, R. T. Holman, and Z. Dong. 2001. Omega 3 but not omega 6 fatty acids inhibit AP-1 activity and cell transformation in JB6 cells. Proc. Natl. Acad. Sci. USA 98: 7510-7515.
41. Jump, D. B. 2002. The biochemistry of n-3 polyunsaturated fatty acids. J. Biol. Chem. 277: 8755-8758.
42. Schmidt, E. B., and J. Dyerberg. 1994. Omega-3 fatty acids. Current status in cardiovascular medicine. Drugs. 47: 405-424.
43. Leaf, A., and P. C. Weber. 1988. Cardiovascular effects of n-3 fatty acids. N. Engl. J. Med. 318: 549-557.
44. Simopoulos, A. P. 1991. Omega-3 fatty acids in health and disease and in growth and development. Am. J. Clin. Nutr. 54: 438-463.
45. Willett, W. C., M. J. Stampfer, G. A. Colditz, B. A. Rosner, and F. E. Speizer. 1990. Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N. Engl. J Med. 323: 1664-1672.
46. Bostick, R. M., J. D. Potter, L. H. Kushi, T. A. Sellers, K. A. Steinmetz, D. R. McKenzie, S. M. Gapstur, and A. R. Folsom. 1994. Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control. 5: 38-52.
47. Hill, M. J., and C. P. Caygill. 1995. Fish, n-3 fatty acids and human colorectal and breast cancer mortality. Eur. J. Cancer Prev. 4: 329-332.
48. Anti, M., F. Armelao, G. Marra, A. Percesepe, G. M. Bartoli, P. Palozza, P. Parrella, C. Canetta, N. Gentiloni, I. De Vitis, and G. Gasbarrini. 1994. Effects of different doses of fish oil on rectal cell proliferation in patients with sporadic colonic adenomas. Gastroenterology. 107: 1709-1718.
49. Anti, M., G. Marra, F. Armelao, G. M. Bartoli, R. Ficarelli, A. Percesepe, I. De Vitis, G. Maria, L. Sofo, G. L. Rapaccini, N. Gentiloni, E. Piccioni, and G. Miggiano. 1992. Effect of omega-3 fatty acids on rectal mucosal cell proliferation in subjects at risk for colon cancer. Gastroenterology. 103: 883-891.
50. Kelley, D. S., P. C. Taylor, G. J. Nelson, P. C. Schmidt, A. Ferretti, K. L. Erickson, R. Yu, R. K. Chandra, and B. E. Mackey. 1999. Docosahexaenoic acid ingestion inhibits natural killer cell activity and production of inflammatory mediators in young healthy men. Lipids. 34: 317-324.
51. Jolly, C. A., Y. H. Jiang, R. S. Chapkin, and D. N. McMurray. 1997. Dietary (n-3) polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide. J. Nutr. 127: 37-43.
52. Virella, G., J. M. Kilpatrick, M. T. Rugeles, B. Hyman, and R. Russell. 1989. Depression of humoral responses and phagocytic functions in vivo and in vitro by fish oil and eicosapentanoic acid. Clin. Immunol. Immunopathol. 52: 257-270.
53. Kutchera, W., D. A. Jones, N. Matsunami, J. Groden, T. M. McIntyre, G. A. Zimmerman, R. L. White, and S. M. Prescott. 1996. Prostaglandin H synthase 2 is expressed abnormally in human colon cancer: evidence for a transcriptional effect. Proc. Natl. Acad. Sci. USA. 93: 4816-4820.
54. Eberhart, C. E., R. J. Coffey, A. Radhika, F. M. Giardiello, S. Ferrenbach, and R. N. DuBois. 1994. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology. 107: 1183-1188.
55. Sano, H., Y. Kawahito, R. L. Wilder, A. Hashiramoto, S. Mukai, K. Asai, S. Kimura, H. Kato, M. Kondo, and T. Hla. 1995. Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res. 55: 3785-3789.
56. Kargman, S. L., G. P. O'Neill, P. J. Vickers, J. F. Evans, J. A. Mancini, and S. Jothy. 1995. Expression of prostaglandin G/H synthase-1 and -2 protein in human colon cancer. Cancer Res. 55: 2556-2559.
57. Taubes, G. 2002. Cardiovascular disease: does inflammation cut to the heart of the matter? Science. 296: 242-245.
58. Dhurandhar, N. V. 2001. Chronic nutritional diseases of infectious origin: an assessment of a nascent field. J. Nutr. 131: 2787S-2788S.
59. Zimmer, C. 2001. Do chronic diseases have an infectious root? Science. 293: 1974-1977.