Oxidatively modified low density lipoprotein (LDL) inhibits TLR2 and TLR4 cytokine responses in human monocytes but not in macrophages

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23479-23488

  Kannan, Yashaswini ^a,b   Sundaram, Kruthika ^a,b   Narasimhulu, Chandrakala Aluganti ^a   Parthasarathy, Sampath ^a   Wewers, Mark D ^a,b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATHEROSCLEROTIC PLAQUE; CHEMOKINES; CYTOKINE RESPONSE; CYTOKINES; HUMAN MACROPHAGES; HUMAN MONOCYTES; INFLAMMATORY RESPONSE; LOW DENSITY LIPOPROTEINS; MICROENVIRONMENTS; PROINFLAMMATORY; SCAVENGER RECEPTOR; TOLL-LIKE RECEPTORS;

DISEASES; LIGANDS; LIPIDS; MACROPHAGES;

BODY FLUIDS;

ENDOTOXIN; I KAPPA B KINASE EPSILON; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIGAND; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOBLOTTING; MACROPHAGE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION;

ANTIGENS, CD36; CELLS, CULTURED; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; IMMUNOBLOTTING; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIPOPEPTIDES; LIPOPOLYSACCHARIDES; LIPOPROTEINS, LDL; MACROPHAGES; MONOCYTES; NUCLEAR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84863611013     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.320960     Document Type: Article

References (55)

1. Carter, A. M. (2005) Inflammation, thrombosis, and acute coronary syndromes. Diab. Vasc. Dis. Res. 2, 113-121
2. Libby, P., and Theroux, P. (2005) Pathophysiology of coronary artery disease. Circulation 111, 3481-3488 (Pubitemid 40923403)
3. Parthasarathy, S., Raghavamenon, A., Garelnabi, M. O., and Santanam, N. (2010) Oxidized low density lipoprotein. Methods Mol. Biol. 610, 403-417
4. Greaves, D. R., and Gordon, S. (2009) The macrophage scavenger receptor at 30 years of age: current knowledge and future challenges. J. Lipid Res. 50, (suppl.) S282-S286
5. Silverstein, R. L., and Febbraio, M. (2009) CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci. Signal 2, re3
6. Hoebe, K., Georgel, P., Rutschmann, S., Du, X., Mudd, S., Crozat, K., Sovath, S., Shamel, L., Hartung, T., Zähringer, U., and Beutler, B. (2005) CD36 is a sensor of diacylglycerides. Nature 433, 523-527 (Pubitemid 40204309)
7. Jimenez-Dalmaroni, M. J., Xiao, N., Corper, A. L., Verdino, P., Ainge, G. D., Larsen, D. S., Painter, G. F., Rudd, P. M., Dwek, R. A., Hoebe, K., Beutler, B., and Wilson, I. A. (2009) Soluble CD36 ectodomain binds negatively charged diacylglycerol ligands and acts as a co-receptor for TLR2. PLoS. One 4, e7411
8. Triantafilou, M., Gamper, F. G., Haston, R. M., Mouratis, M. A., Morath, S., Hartung, T., and Triantafilou, K. (2006) Membrane sorting of Toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002-31011 (Pubitemid 44582155)
9. Hansson, G. K., and Hermansson, A. (2011) The immune system in atherosclerosis. Nat. Immunol. 12, 204-212
10. Yamamoto, M., Yamazaki, S., Uematsu, S., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Kuwata, H., Takeuchi, O., Takeshige, K., Saitoh, T., Yamaoka, S., Yamamoto, N., Yamamoto, S., Muta, T., Takeda, K., and Akira, S. (2004) Regulation of Toll/IL-1-receptor-mediated gene expression by the inducible nuclear protein IκBζ. Nature 430, 218-222 (Pubitemid 38902431)
11. Seshadri, S., Kannan, Y., Mitra, S., Parker-Barnes, J., and Wewers, M. D. (2009) MAIL regulates human monocyte IL-6 production. J. Immunol. 183, 5358-5368
12. Santanam, N., and Parthasarathy, S. (1995) Paradoxical actions of antioxidants in the oxidation of low density lipoprotein by peroxidases. J. Clin. Invest. 95, 2594-2600
13. Raices, R. M., Kannan, Y., Bellamkonda-Athmaram, V., Seshadri, S., Wang, H., Guttridge, D. C., and Wewers, M. D. (2009) A novel role for IκBζ in the regulation of IFNγ production. PLoS. One 4, e6776
14. Kannan, Y., Yu, J., Raices, R. M., Seshadri, S., Wei, M., Caligiuri, M. A., and Wewers, M. D. (2011) IκBζ augments IL-12- and IL-18-mediated IFNγ production in human NK cells. Blood 117, 2855-2863
15. Herzyk, D. J., Allen, J. N., Marsh, C. B., and Wewers, M. D. (1992) Macrophage and monocyte IL-1β regulation differs at multiple sites: messenger RNA expression, translation, and post-translational processing. J. Immunol. 149, 3052-3058
16. Marsh, C. B., Gadek, J. E., Kindt, G. C., Moore, S. A., and Wewers, M. D. (1995) Monocyte Fcγ receptor cross-linking induces IL-8 production. J. Immunol. 155, 3161-3167
17. Marsh, C. B., Lowe, M. P., Rovin, B. H., Parker, J. M., Liao, Z., Knoell, D. L., and Wewers, M. D. (1998) Lymphocytes produce IL-1β in response to Fcγ receptor cross-linking: effects on parenchymal cell IL-8 release. J. Immunol. 160, 3942-3948 (Pubitemid 28176101)
18. Huh, H. Y., Pearce, S. F., Yesner, L. M., Schindler, J. L., and Silverstein, R. L. (1996) Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. Blood 87, 2020-2028 (Pubitemid 26068918)
19. Podrez, E. A., Febbraio, M., Sheibani, N., Schmitt, D., Silverstein, R. L., Hajjar, D. P., Cohen, P. A., Frazier, W. A., Hoff, H. F., and Hazen, S. L. (2000) Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J. Clin. Invest. 105, 1095-1108 (Pubitemid 30217694)
20. Rahaman, S. O., Lennon, D. J., Febbraio, M., Podrez, E. A., Hazen, S. L., and Silverstein, R. L. (2006) A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab. 4, 211-221 (Pubitemid 44283954)
21. Silverstein, R. L. (2009) Inflammation, atherosclerosis, and arterial thrombosis: role of the scavenger receptor CD36. Cleve. Clin. J. Med. 76, Suppl. 2, S27-S30
22. Björkbacka, H. (2006) Multiple roles of Toll-like receptor signaling in atherosclerosis. Curr. Opin. Lipidol. 17, 527-533
23. Beutler, B. A. (2009) TLRs and innate immunity. Blood 113, 1399-1407
24. Aqel, N. M., Ball, R. Y., Waldmann, H., and Mitchinson, M. J. (1984) Monocytic origin of foam cells in human atherosclerotic plaques. Atherosclerosis 53, 265-271 (Pubitemid 15194149)
25. Schwartz, C. J., Valente, A. J., Sprague, E. A., Kelley, J. L., Suenram, C. A., and Rozek, M. M. (1985) Atherosclerosis as an inflammatory process: the roles of the monocyte-macrophage. Ann. N.Y. Acad. Sci. 454, 115-120 (Pubitemid 16198842)
26. Ross, R. (1986) The pathogenesis of atherosclerosis: an update. N. Engl. J. Med. 314, 488-500
27. Sato, T., Takebayashi, S., and Kohchi, K. (1987) Increased subendothelial infiltration of the coronary arteries with monocytes/macrophages in patients with unstable angina: histological data on 14 autopsied patients. Atherosclerosis 68, 191-197 (Pubitemid 17159771)
28. Ylä-Herttuala, S., Palinski, W., Rosenfeld, M. E., Parthasarathy, S., Carew, T. E., Butler, S., Witztum, J. L., and Steinberg, D. (1989) Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84, 1086-1095 (Pubitemid 19247577)
29. Szmitko, P. E., Wang, C. H., Weisel, R. D., de Almeida, J. R., Anderson, T. J., and Verma, S. (2003) New markers of inflammation and endothelial cell activation: Part I. Circulation 108, 1917-1923 (Pubitemid 37296533)
30. Biwa, T., Sakai, M., Shichiri, M., and Horiuchi, S. (2000) Granulocyte/macrophage colony-stimulating factor plays an essential role in oxidized low density lipoprotein-induced macrophage proliferation. J. Atheroscler. Thromb. 7, 14-20
31. Collins, R. F., Touret, N., Kuwata, H., Tandon, N. N., Grinstein, S., and Trimble, W. S. (2009) Uptake of oxidized low density lipoprotein by CD36 occurs by an actin-dependent pathway distinct from macropinocytosis. J. Biol. Chem. 284, 30288-30297
32. 2 expression in THP-1 monocytes via PI3K and p38MAPKpathways. Cardiovasc. Res. 85, 845-852
33. Lopes-Virella, M. F., and Virella, G. (2010) Clinical significance of the humoral immune response to modified LDL. Clin. Immunol. 134, 55-65
34. Seshiah, P. N., Kereiakes, D. J., Vasudevan, S. S., Lopes, N., Su, B. Y., Flavahan, N. A., and Goldschmidt-Clermont, P. J. (2002) Activated monocytes induce smooth muscle cell death: role of macrophage colony-stimulating factor and cell contact. Circulation 105, 174-180 (Pubitemid 34084315)
35. Krieger, M. (1997) The other side of scavenger receptors: pattern recognition for host defense. Curr. Opin. Lipidol. 8, 275-280
36. Miller, Y. I., Viriyakosol, S., Binder, C. J., Feramisco, J. R., Kirkland, T. N., and Witztum, J. L. (2003) Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J. Biol. Chem. 278, 1561-1568 (Pubitemid 36801384)
37. Miller, Y. I., Viriyakosol, S., Worrall, D. S., Boullier, A., Butler, S., and Witztum, J. L. (2005) Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low density lipoprotein in macrophages. Arterioscler. Thromb. Vasc. Biol. 25, 1213-1219 (Pubitemid 40776611)
38. Schroder, K., and Tschopp, J. (2010) The inflammasomes. Cell 140, 821-832
39. Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., Abela, G. S., Franchi, L., Nuñez, G., Schnurr, M., Espevik, T., Lien, E., Fitzgerald, K. A., Rock, K. L., Moore, K. J., Wright, S. D., Hornung, V., and Latz, E. (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361
40. Kawai, T., and Akira, S. (2009) The roles of TLRs, RLRs, and NLRs in pathogen recognition. International immunology 21, 317-337
41. Byrne, G. I., and Kalayoglu, M. V. (1999) Chlamydia pneumoniae and atherosclerosis: links to the disease process. Am. Heart J. 138, S488-S490 (Pubitemid 29523240)
42. Yumoto, H., Chou, H. H., Takahashi, Y., Davey, M., Gibson, F. C., 3rd, and Genco, C. A. (2005) Sensitization of human aortic endothelial cells to lipopolysaccharide via regulation of Toll-like receptor 4 by bacterial fimbria-dependent invasion. Infect. Immun. 73, 8050-8059 (Pubitemid 41740292)
43. Triantafilou, M., Gamper, F. G., Lepper, P. M., Mouratis, M. A., Schumann, C., Harokopakis, E., Schifferle, R. E., Hajishengallis, G., and Triantafilou, K. (2007) Lipopolysaccharides from atherosclerosis-associated bacteria antagonize TLR4, induce formation of TLR2/1/CD36 complexes in lipid rafts, and trigger TLR2-induced inflammatory responses in human vascular endothelial cells. Cell Microbiol. 9, 2030-2039 (Pubitemid 47087093)
44. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801 (Pubitemid 43261452)
45. Hamilton, T. A., Ma, G. P., and Chisolm, G. M. (1990) Oxidized low density lipoprotein suppresses the expression of tumor necrosis factor-α mRNA in stimulated murine peritoneal macrophages. J. Immunol. 144, 2343-2350 (Pubitemid 20106578)
46. Hamilton, T. A., Major, J. A., and Chisolm, G. M. (1995) The effects of oxidized low density lipoproteins on inducible mouse macrophage gene expression are gene- and stimulus-dependent. J. Clin. Invest. 95, 2020-2027
47. Leitinger, N. (2005) Oxidized phospholipids as triggers of inflammation in atherosclerosis. Mol. Nutr. Food Res. 49, 1063-1071
48. Ohlsson, B. G., Englund, M. C., Karlsson, A. L., Knutsen, E., Erixon, C., Skribeck, H., Liu, Y., Bondjers, G., and Wiklund, O. (1996) Oxidized low density lipoprotein inhibits lipopolysaccharide-induced binding of nuclear factor-βB to DNA and the subsequent expression of tumor necrosis factor-α and interleukin-1β in macrophages. J. Clin. Invest. 98, 78-89 (Pubitemid 26243823)
49. Hirose, K., Iwabuchi, K., Shimada, K., Kiyanagi, T., Iwahara, C., Nakayama, H., and Daida, H. (2011) Different responses to oxidized low density lipoproteins in human polarized macrophages. Lipids Health Dis. 10, 1
50. Mattaliano, M. D., Huard, C., Cao, W., Hill, A. A., Zhong, W., Martinez, R. V., Harnish, D. C., Paulsen, J. E., and Shih, H. H. (2009) LOX-1-dependent transcriptional regulation in response to oxidized LDL treatment of human aortic endothelial cells. Am. J. Physiol. Cell Physiol. 296, C1329-1337
51. Hamilton, T. A., and Major, J. A. (1996) Oxidized LDL potentiates LPS-induced transcription of the chemokine KC gene. J. Leukoc Biol. 59, 940-947 (Pubitemid 26238492)
52. Henning, L. N., Azad, A. K., Parsa, K. V., Crowther, J. E., Tridandapani, S., and Schlesinger, L. S. (2008) Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J. Immunol. 180, 7847-7858
53. van Tits, L. J., Stienstra, R., van Lent, P. L., Netea, M. G., Joosten, L. A., and Stalenhoef, A. F. (2011) Oxidized LDL enhances proinflammatory responses of alternatively activated M2 macrophages: a crucial role for Krüppel-like factor 2. Atherosclerosis 214, 345-349
54. Tontonoz, P., Nagy, L., Alvarez, J. G., Thomazy, V. A., and Evans, R. M. (1998) PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93, 241-252 (Pubitemid 28180857)
55. Bouhlel, M. A., Derudas, B., Rigamonti, E., Dièvart, R., Brozek, J., Haulon, S., Zawadzki, C., Jude, B., Torpier, G., Marx, N., Staels, B., and Chinetti-Gbaguidi, G. (2007) PPARγ activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab. 6, 137-143 (Pubitemid 47189091)