Synergism between platelet-activating factor-like phospholipids and peroxisome proliferator-activated receptor γ agonists generated during low density lipoprotein oxidation that induces lipid body formation in leukocytes

Journal of Immunology

Volumn 171, Issue 4, 2003, Pages 2090-2098

  De Assis, Edson F ^a   Silva, Adriana R ^a   Caiado, Lara F C ^a   Marathe, Gopal K ^b   Zimmerman, Guy A ^b,c   Prescott, Stephen M ^b,d   McIntyre, Thomas M ^b,c   Bozza, Patricia T ^a   De Castro Faria Neto, Hugo C ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 LIPOXYGENASE ANTAGONIST; ARACHIDONATE 5 LIPOXYGENASE; AZELAOYLPHOSPHATIDYLCHOLINE; BUTENOYL PLATELET ACTIVATING FACTOR; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; OXIDIZED LOW DENSITY LIPOPROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PLATELET ACTIVATING FACTOR LIKE PHOSPHOLIPID; RECOMBINANT PLATELET ACTIVATING FACTOR ACETYLHYDROLASE; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR ANTAGONIST; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME LOCALIZATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INFLAMMATION; LEUKOCYTE; LIPID BODY; LIPOPROTEIN METABOLISM; LIPOPROTEIN OXIDATION; MACROPHAGE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PLEURA CAVITY; PRIORITY JOURNAL;

EID: 0041633798     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.4.2090     Document Type: Article

References (57)

1. Ross, R., and J. A. Glomset. 1973. Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 180:1332.
2. Ross, R. 1999. Atherosclerosis: an inflammatory disease. N. Engl. J. Med. 340:115.
3. Steinbrecher, U. P. 1999. Receptors for oxidized low density lipoprotein. Biochim. Biophys. Acta 1436:279.
4. Brown, M. S., P. T. Kovanen, and J. L. Goldstein. 1979. Receptor-mediated uptake of lipoprotein-cholesterol and its utilization for steroid synthesis in the adrenal cortex. Recent Prog. Horm. Res. 35:215.
5. Steinberg, D. 1997, Lewis A. Conner Memorial Lecture: oxidative modification of LDL and atherogenesis. Circulation 95:1062.
6. Witztum, J. L., and D. Steinberg. 2001. The oxidative modification hypothesis of atherosclerosis: does it hold for humans? Trends Cardiovasc. Med 11:93.
7. Berliner, J. A., M. C. Territo, A. Sevanian, S. Ramin, J. A. Kim, B. Bamshad, M. Esterson, and A. M. Fogelman. 1990. Minimally modified low density lipoprotein stimulates monocyte endothelial interactions. J. Clin. Invest. 85:1260.
8. Berliner, J. A., D. S. Schwartz, M. C. Territo, A. Andalibi, L. Almada, A. J. Lusis, D. Quismorio, Z. P. Fang, and A. M. Fogelman. 1993. Induction of chemotactic cytokines by minimally oxidized LDL. Adv. Exp. Med. Biol. 351:13.
9. Boullier, A., K. L. Gillotte, S. Horkko, S. R. Green, P. Friedman, E. A. Dennis, J. L. Witztum, D. Steinberg, and O. Quehenberger. 2000. The binding of oxidized low density lipoprotein to mouse CD36 is mediated in part by oxidized phospholipids that are associated with both the lipid and protein moieties of the lipoprotein. J. Biol. Chem. 275:9163.
10. Podrez, E. A., E. Poliakov, Z. Shen, R. Zhang, Y. Deng, M. Sun, P. J. Finton, L. Shan, M, Febbraio, D. P. Hajjar, et al. 2002. A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277:38517.
11. Podrez, E. A., E. Poliakov, Z. Shen, R. Zhang, Y. Deng, M. Sun, P. J. Finton, L. Shan, B. Gugiu, P. L. Fox, et al. 2002. Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36. J. Biol. Chem. 277:38503.
12. Heery, J. M., M. Kozak, D. M. Stafforini, D. A. Jones, G. A. Zimmerman, T. M. McIntyre, and S. M. Prescott. 1995. Oxidatively modified LDL contains phospholipids with platelet-activating factor-like activity and stimulates the growth of smooth muscle cells. J. Clin. Invest. 96:2322.
13. Marathe, G. K. S. S. Davies, K. A. Harrison, A. R. Silva, R. C. Murphy, H. Castro-Faria-Neto, S. M. Prescott, G. A. Zimmerman, and T. M. McIntyre. 1999. Inflammatory platelet-activating factor-like phospholipids in oxidized low density lipoproteins are fragmented alkyl phosphatidylcholines. J. Biol. Chem. 274:28395.
14. 2+ induced LDL oxidation. Free Radical Biol. Med. 33:S147.
15. Bussolino, F., M. G. Porcellini, L. Varese, and A. Bosia. 1987. Intravascular release of platelet activating factor in children with sepsis. Thromb. Res. 48:619.
16. Lloberas, N., J. Torras, I. Herrero-Fresneda, J. M. Cruzado, M. Riera, I. Hurtado, and J. M. Grinyo. 2002. Postischemic renal oxidative stress induces inflammatory response through PAF and oxidized phospholipids: prevention by antioxidant treatment. FASEB J. 16:908.
17. Tetta, C., F. Bussolino, V. Modena, G. Montrucchio, G. Segoloni, G. Pescarmona, and G. Camussi. 1990. Release of platelet-activating factor in systemic lupus erythematosus. Int. Arch. Allergy Appl. Immunol. 91:244.
18. Imaizumi, T., K. Satoh, H. Yoshida, Y. Kawamura, M. Hiramoto, and S. Takamatsu. 1991. Effect of cigarette smoking on the levels of platelet-activating factor-like lipid(s) in plasma lipoproteins. Atherosclerosis 87:47.
19. Subbanagounder, G., N. Leitinger, P. T. Shih, K. F. Faull, and J. A. Berliner. 1999. Evidence that phospholipid oxidation products and/or platelet-activating factor play an important role in early atherogenesis: in vitro and in vivo inhibition by WEB 2086. Circ. Res. 85:311.
20. Bozza, P. T., J. L. Payne, J. L. Goulet, and P. F. Weller. 1996. Mechanisms of platelet-activating factor-induced lipid body formation: requisite roles for 5-lipoxygenase and de novo protein synthesis in the compartmentalization of neutrophil lipids. J. Exp. Med. 183:1515.
21. Bozza, P. T., W. Yu, J. F. Penrose, E. S. Morgan, A. M. Dvorak, and P. F. Weller. 1997. Eosinophil lipid bodies: specific, inducible intracellular sites for enhanced eicosanoid formation. J. Exp. Med. 186:909.
22. Bozza, P. T., W. Yu, J. Cassara, and P. F. Weller. 1998. Pathways for eosinophil lipid body induction: differing signal transduction in cells from normal and hypereosinophilic subjects. J. Leukocyte Biol. 64:563.
23. Weller, P. F., P. T. Bozza, W. Yu, and A. M. Dvorak. 1999. Cytoplasmic lipid bodies in eosinophils: central roles in eicosanoid generation. Int. Arch. Allergy Immunol. 118:450.
24. Murphy, D. J. 2001. The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40:325.
25. Dvorak, A. M., E. Morgan, R. P. Schleimer, S. W. Ryeom, L. M. Lichtenstein, and P. F. Weller. 1992. Ultrastructural immunogold localization of prostaglandin endoperoxide synthase (cyclooxygenase) to non-membrane-bound cytoplasmic lipid bodies in human lung mast cells, alveolar macrophages, type II pneumocytes, and neutrophils. J. Histochem. Cytochem. 40:759.
26. 2 at cytoplasmic arachidonate-rich lipid bodies. Am. J. Pathol. 152:759.
27. Davies, S. S., A. V. Pontsler, G. K. Marathe, K. A. Harrison, R. C. Murphy, J. C. Hinshaw, G. D. Prestwich, A. S. Hilaire, S. M. Prescott, G. A. Zimmerman, and T. M. McIntyre. 2001. Oxidized alkyl phospholipids are specific, high affinity peroxisome proliferator-activated receptor γ ligands and agonists. J. Biol. Chem. 276:16015.
28. Nagy, L., P. Tontonoz, J. G. Alvarez, H. Chen, and R. M. Evans. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARγ. Cell 93:229.
29. Tontonoz, P., L. Nagy, J. G. Alvarez, V. A. Thomazy, and R. M. Evans. 1998. PPARγ promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93:241.
30. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911.
31. Kaluzny, M. A., L. A. Duncan, M. V. Merritt, and D. E. Epps. 1985. Rapid separation of lipid classes in high yield and purity using bonded phase columns. J. Lipid Res. 26:135.
32. Bozza, P. T., W. Yu, and P. F. Weller. 1997. Mechanisms of formation and function of eosinophil lipid bodies: inducible intracellular sites involved in arachidonic acid metabolism. Mem. Inst. Oswaldo Cruz 92(Suppl. 2):135.
33. Silva, A. R., E. F. de Assis, L. F. Caiado, G. K. Marathe, M. T. Bozza, T. M. McIntyre, G. A. Zimmerman, S. M. Prescott, P. T. Bozza, and H. C, Castro-Faria-Neto. 2002. Monocyte chemoattractant protein-1 and 5-lipoxygenase products recruit leukocytes in response to platelet-activating factor-like lipids in oxidized low-density lipoprotein. J. Immunol. 168:4112.
34. Weller, P. F., R. A. Monahan-Earley, H. F. Dvorak, and A. M. Dvorak. 1991. Cytoplasmic lipid bodies of human eosinophils: subcellular isolation and analysis of arachidonate incorporation. Am. J. Pathol. 138:141.
35. Navab, M., J. A. Berliner, A. D. Watson, S. Y. Hama, M. C. Territo, A. J. Lusis, D. M. Shih, B. J. Van Lenten, J. S. Frank, L. L. Demer, et al. 1996. The Yin and Yang of oxidation in the development of the fatty streak: a review based on the 1994 George Lyman Duff Memorial Lecture. Arterioscler. Thromb. Vasc. Biol. 16:831.
36. Tsimikas, S., and J. L. Witztum. 2000. The oxidative modification hypothesis of atherogenesis. In Oxidative Stress and Vascular Disease, Vol. 1. John F. Keaney, Jr., ed. Kluwer Academic, Dordrecht, The Netherlands, p. 49.
37. Coimbra, A., and A. Lopes-Vaz. 1971. The presence of lipid droplets and the absence of stable sudanophilia in osmium-fixed human leukocytes. J. Histochem. Cytochem. 19:551.
38. Pacheco, P., F. A. Bozza, R. N. Gomes, M. Bozza, P. F. Weller, H. C. Castro-Faria-Neto, and P. T. Bozza. 2002. Lipopolysaccharide-induced leukocyte lipid body formation in vivo: innate immunity elicited intracellular loci involved in eicosanoid metabolism. J. Immunol. 169:6498.
39. Melo, R. C., H. D'Avila, D. L. Fabrino, P. E. Almeida, and P. T. Bozza. 2003. Macrophage lipid body induction by Chagas disease in vivo: putative intracellular domains for eicosanoid formation during infection. Tissue Cell 35:59.
40. Beil, W. J., P. F. Weller, M. A. Peppercorn, S. J. Galli, and A, M. Dvorak. 1995. Ultrastructural immunogold localization of subcellular sites of TNF-α in colonic Crohn's disease. J. Leukocyte Biol. 58:284.
41. Scarfo, L. M., P. F. Weller, and H. W. Farber. 2001. Induction of endothelial cell cytoplasmic lipid bodies during hypoxia. Am. J. Physiol. Heart Circ. Physiol. 280:H294.
42. Triggiani, M., A. Oriente, M. C. Seeds, D. A. Bass, G. Marone, and F. H. Chilton. 1995. Migration of human inflammatory cells into the lung results in the remodeling of arachidonic acid into a triglyceride pool. J. Exp. Med. 182:1181.
43. 4 production in eosinophils and basophils. J. Biol. Chem. 276:22779.
44. Bozza, P. T., J. L. Payne, S. G. Morham, R. Langenbach, O. Smithies, and P. F. Weller. 1996. Leukocyte lipid body formation and eicosanoid generation: cyclooxygenase-independent inhibition by aspirin. Proc. Natl. Acad. Sci. USA 93:11091.
45. Prescott, S. M., G. A. Zimmerman, D. M. Stafforini, and T. M. McIntyre. 2000. Platelet-activating factor and related lipid mediators. Annu. Rev. Biochem. 69:419.
46. Pontsler, A. V., A. St. Hilaire, G. K. Marathe, G. A. Zimmerman, and T. M. McIntyre. 2002. Cyclooxygenase-2 is induced in monocytes by peroxisome proliferator activated receptor γ and oxidized alkyl phospholipids from oxidized low density lipoprotein. J. Biol. Chem. 277:13029.
47. Baker, C. S., R. J. Hall, T. J. Evans, A. Pomerance, J. Maclouf, C. Creminon. M. H. Yacoub, and J. M. Polak. 1999. Cyclooxygenase-2 is widely expressed in atherosclerotic lesions affecting native and transplanted human coronary arteries and colocalizes with inducible nitric oxide synthase and nitrotyrosine particularly in macrophages. Arterioscler. Thromb. Vasc. Biol. 19:646.
48. Schonbeck, U., G. K. Sukhova, P. Graber, S. Coulter, and P. Libby. 1999. Augmented expression of cyclooxygenase-2 in human atherosclerotic lesions. Am. J. Pathol. 155:1281.
49. Pritchard, K. A., Jr., M. K. O'Banion, J. M. Miano, N. Vlasic, U. G. Bhatia, D. A. Young, and M. B. Stemerman. 1994. Induction of cyclooxygenase-2 in rat vascular smooth muscle cells in vitro and in vivo. J. Biol. Chem. 269:8504.
50. 4 receptor antagonism reduces monocytic foam cells in mice. Arterioscler. Thromb. Vasc. Biol. 22:443.
51. 4. Proc. Natl. Acad. Sci. USA 79:7866.
52. Bozza, P. T., P. Pacheco, W, Yu, and P. F. Weller. 2002. NS-398: cyclooxygenase-2 independent inhibition of leukocyte priming for lipid body formation and enhanced leukotriene generation. Prostaglandins Leukotrienes Essent. Fatty Acids 67:237.
53. Bandeira-Melo, C., P. T. Bozza, and P. F. Weller. 2002. The cellular biology of eosinophil eicosanoid formation and function. J. Allergy Clin. Immunol. 109:393.
54. Ricote, M., J. Huang, L. Fajas, A. Li, J. Welch, J. Najib, J. L. Witztum, J. Auwerx, W. Palinski, and C. K. Glass. 1998. Expression of the peroxisome proliferator-activated receptor γ (PPARγ) in human atherosclerosis and regulation in macrophages by colony stimulating factors and oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 95:7614.
55. Chawla, A., Y. Barak, L. Nagy, D. Liao, P. Tontonoz, and R. M. Evans. 2001. PPAR-γ dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 7:48.
56. Bozza, P. T., and P. F. Weller. 2001. Arachidonyl trifluoromethyl ketone induces lipid body formation in leukocytes. Prostaglandins Leukotrienes Essent. Fatty Acids 64:227.
57. Hourton, D., P. Delerive, J. Stankova, B. Staels, M. J. Chapman, and E. Ninio. 2001. Oxidized low-density lipoprotein and peroxisome-proliferator-activated receptor α down-regulate platelet-activating-factor receptor expression in human macrophages. Biochem. J. 354:225.