Joint tissues amplify inflammation and alter their invasive behavior via leukotriene B4 in experimental inflammatory arthritis

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 5503-5511

  Chen, Mei ^a,b   Lam, Bing K ^a,b   Luster, Andrew D ^a   Zarini, Simona ^c   Murphy, Robert C ^c   Bair, Angela M ^a   Soberman, Roy J ^a   Lee, David M ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; LEUKOTRIENE A4 HYDROLASE; LEUKOTRIENE B4; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; BONE MARROW; BONE TISSUE; CELL LINEAGE; CELL METABOLISM; CELL POPULATION; CELL STIMULATION; CHIMERA; CONTROLLED STUDY; EX VIVO STUDY; FATTY ACID SYNTHESIS; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNOVIOCYTE; SYNOVITIS; SYNTHESIS; ANIMAL; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE MUTANT; NEUTROPHIL; PATHOLOGY; SYNOVIUM; WESTERN BLOTTING;

ANIMALS; ARTHRITIS, EXPERIMENTAL; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; LEUKOTRIENE B4; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; SYNOVIAL MEMBRANE;

EID: 78149489303     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001258     Document Type: Article

References (64)

1. Henderson, W. R., Jr. 1994. The role of leukotrienes in inflammation. Ann. Intern. Med. 121:684-697.
2. Murphy, R. C., and M. A. Gijón. 2007. Biosynthesis and metabolism of leukotrienes. Biochem. J. 405:379-395.
3. Carlos, T. M., and J. M. Harlan. 1994. Leukocyte-endothelial adhesion molecules. Blood 84:2068-2101.
4. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7:678-689.
5. Werz, O. 2002. 5-Lipoxygenase: cellular biology and molecular pharmacology. Curr. Drug Targets Inflamm. Allergy 1:23-44.
6. Funk, C. D. 2001. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871-1875.
7. Reid, G. K., S. Kargman, P. J. Vickers, J. A. Mancini, C. Léveillé, D. Ethier, D. K. Miller, J. W. Gillard, R. A. Dixon, and J. F. Evans. 1990. Correlation between expression of 5-lipoxygenase-activating protein, 5-lipoxygenase, and cellular leukotriene synthesis. J. Biol. Chem. 265:19818-19823.
8. Miller, D. K., J. W. Gillard, P. J. Vickers, S. Sadowski, C. Léveillé, J. A. Mancini, P. Charleson, R. A. Dixon, A. W. Ford-Hutchinson, R. Fortin, et al. 1990. Identification and isolation of a membrane protein necessary for leukotriene production. Nature 343:278-281.
9. Dixon, R. A., R. E. Diehl, E. Opas, E. Rands, P. J. Vickers, J. F. Evans, J. W. Gillard, and D. K. Miller. 1990. Requirement of a 5- lipoxygenaseactivating protein for leukotriene synthesis. Nature 343:282-284.
10. Samuelsson, B., and C. D. Funk. 1989. Enzymes involved in the biosynthesis of leukotriene B4. J. Biol. Chem. 264:19469-19472.
11. Mandal, A. K., P. B. Jones, A. M. Bair, P. Christmas, D. Miller, T. T. Yamin, D. Wisniewski, J. Menke, J. F. Evans, B. T. Hyman, et al. 2008. The nuclear membrane organization of leukotriene synthesis. Proc. Natl. Acad. Sci. USA 105:20434-20439.
12. Folco, G., and R. C. Murphy. 2006. Eicosanoid transcellular biosynthesis: from cellcell interactions to in vivo tissue responses. Pharmacol. Rev. 58:375-388.
13. Dahinden, C. A., R. M. Clancy, M. Gross, J. M. Chiller, and T. E. Hugli. 1985. Leukotriene C4 production by murine mast cells: evidence of a role for extracellular leukotriene A4. Proc. Natl. Acad. Sci. USA 82:6632-6636.
14. Grimminger, F., U. Sibelius, and W. Seeger. 1991. Amplification of LTB4 generation in AM-PMN cocultures: transcellular 5-lipoxygenase metabolism. Am. J. Physiol. 261: L195-L203.
15. McGee, J. E., and F. A. Fitzpatrick. 1986. Erythrocyte-neutrophil interactions: formation of leukotriene B4 by transcellular biosynthesis. Proc. Natl. Acad. Sci. USA 83:1349-1353.
16. Bigby, T. D., and N. Meslier. 1989. Transcellular lipoxygenase metabolism between monocytes and platelets. J. Immunol. 143:1948-1954.
17. Edenius, C., K. Heidvall, and J. A. Lindgren. 1988. Novel transcellular interaction: conversion of granulocyte-derived leukotriene A4 to cysteinyl-containing leukotrienes by human platelets. Eur. J. Biochem. 178:81-86.
18. Maclouf, J., R. C. Murphy, and P. M. Henson. 1989. Transcellular sulfidopeptide leukotriene biosynthetic capacity of vascular cells. Blood 74:703-707.
19. Fabre, J. E., J. L. Goulet, E. Riche, M. Nguyen, K. Coggins, S. Offenbacher, and B. H. Koller. 2002. Transcellular biosynthesis contributes to the production of leukotrienes during inflammatory responsesinvivo. J. Clin. Invest. 109:1373-1380.
20. Zarini, S., M. A. Gijón, A. E. Ransome, R. C. Murphy, and A. Sala. 2009. Transcellular biosynthesis of cysteinyl leukotrienes in vivo during mouse peritoneal inflammation. Proc. Natl. Acad. Sci. USA 106:8296-8301.
21. Lee, D. M., H. P. Kiener, S. K. Agarwal, E. H. Noss, G. F. Watts, O. Chisaka, M. Takeichi, and M. B. Brenner. 2007. Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315:1006-1010.
22. Lee, D. M., H. P. Kiener, and M. B. Brenner. 2005. Synoviocytes. In Kelley's Textbook of Rheumatology, 7th Ed., E. D. Harris, R. C. Eudd, M. C. Genovese, G. S. Firestein, J. S. Sargent, and C. B. Sludge, eds. Elsevier Saunders, Philadelphia. p. 175-188.
23. Goulet, J. L., J. N. Snouwaert, A. M. Latour, T. M. Coffman, and B. H. Koller. 1994. Altered inflammatory responses in leukotriene-deficient mice. Proc. Natl. Acad. Sci. USA 91:12852-12856.
24. Byrum, R. S., J. L. Goulet, J. N. Snouwaert, R. J. Griffiths, and B. H. Koller. 1999. Determination of the contribution of cysteinyl leukotrienes and leukotriene B4 in acute inflammatory responses using 5-lipoxygenase-and leukotriene A4 hydrolase-deficient mice. J. Immunol. 163:6810-6819.
25. Tager, A. M., J. H. Dufour, K. Goodarzi, S. D. Bercury, U. H. von Andrian, and A. D. Luster. 2000. BLTR mediates leukotriene B (4)-induced chemotaxis and adhesion and plays a dominant role in eosinophil accumulation in a murine model of peritonitis. J. Exp. Med. 192:439-446.
26. Korganow, A. S., H. Ji, S. Mangialaio, V. Duchatelle, R. Pelanda, T. Martin, C. Degott, H. Kikutani, K. Rajewsky, J. L. Pasquali, et al. 1999. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity 10:451-461.
27. Chen, M., B. K. Lam, Y. Kanaoka, P. A. Nigrovic, L. P. Audoly, K. F. Austen, and D. M. Lee. 2006. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis. J. Exp. Med. 203:837-842.
28. Chen, M., E. Boilard, P. A. Nigrovic, P. Clark, D. Xu, G. A. Fitzgerald, L. P. Audoly, and D. M. Lee. 2008. Predominance of cyclooxygenase 1 over cyclooxygenase 2 in the generation of proinflammatory prostaglandins in autoantibody-driven K/BxN serum-transfer arthritis. Arthritis Rheum. 58:1354-1365.
29. Lee, D. M., D. S. Friend, M. F. Gurish, C. Benoist, D. Mathis, and M. B. Brenner. 2002. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 297:1689-1692.
30. Kanaoka, Y., A. Maekawa, J. F. Penrose, K. F. Austen, and B. K. Lam. 2001. Attenuated zymosan-induced peritoneal vascular permeability and IgE-dependent passive cutaneous anaphylaxis in mice lacking leukotriene C4 synthase. J. Biol. Chem. 276:22608-22613.
31. Lam, B. K., W. F. Owen, Jr., K. F. Austen, and R. J. Soberman. 1989. The identification of a distinct export step following the biosynthesis of leukotriene C4 by human eosinophils. J. Biol. Chem. 264:12885-12889.
32. Humason, G. L. 1967. Animal Tissue Techniques. W. H. Freeman, New York.
33. Shin, K., G. F. Watts, H. C. Oettgen, D. S. Friend, A. D. Pemberton, M. F. Gurish, and D. M. Lee. 2008. Mouse mast cell tryptase mMCP-6 is a critical link between adaptive and innate immunity in the chronic phase of Trichinella spiralis infection. J. Immunol. 180:4885-4891.
34. Gijón, M. A., S. Zarini, and R. C. Murphy. 2007. Biosynthesis of eicosanoids and transcellular metabolism of leukotrienes in murine bone marrow cells. J. Lipid Res. 48:716-725.
35. Farias, S. E., S. Zarini, T. Precht, R. C. Murphy, and K. A. Heidenreich. 2007. Transcellular biosynthesis of cysteinyl leukotrienes in rat neuronal and glial cells. J. Neurochem. 103:1310-1318.
36. Nanki, T., K. Nagasaka, K. Hayashida, Y. Saita, and N. Miyasaka. 2001. Chemokines regulate IL-6 and IL-8 production by fibroblast-like synoviocytes from patients with rheumatoid arthritis. J. Immunol. 167:5381-5385.
37. Griffiths, R. J., E. R. Pettipher, K. Koch, C. A. Farrell, R. Breslow, M. J. Conklyn, M. A. Smith, B. C. Hackman, D. J. Wimberly, A. J. Milici, et al. 1995. Leukotriene B4 plays a critical role in the progression of collagen-induced arthritis. Proc. Natl. Acad. Sci. USA 92:517-521.
38. 4. Purification and characterization of a novel epoxide hydrolase from human erythrocytes. J. Biol. Chem. 260:12832-12837.
39. Yokomizo, T., N. Uozumi, T. Takahashi, K. Kume, T. Izumi, and T. Shimizu. 1995. Leukotriene A4 hydrolase and leukotriene B4 metabolism. J. Lipid Mediat. Cell Signal. 12:321-332.
40. Medina, J. F., C. Barrios, C. D. Funk, O. Larsson, J. Haeggström, and O. Rådmark. 1990. Human fibroblasts show expression of the leukotriene-A4-hydrolase gene, whichisincreased after simian-virus- 40transformation. Eur. J. Biochem. 191:27-31.
41. Aloe, L., L. Probert, G. Kollias, L. Bracci-Laudiero, A. Micera, C. Mollinari, and R. Levi-Montalcini. 1993. Level of nerve growth factor and distribution of mast cells in the synovium of tumour necrosis factor transgenic arthritic mice. Int. J. Tissue React. 15:139-143.
42. Simmonds, R. E., and B. M. Foxwell. 2008. Signalling, inflammation and arthritis: NF-kappaB and its relevance to arthritis and inflammation. Rheumatology (Oxford) 47:584-590.
43. Houssiau, F. A., J. P. Devogelaer, J. Van Damme, C. N. de Deuxchaisnes, and J. Van Snick. 1988. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum. 31:784-788.
44. Guerne, P. A., B. L. Zuraw, J. H. Vaughan, D. A. Carson, and M. Lotz. 1989. Synovium as a source of interleukin 6 in vitro. Contribution to local and systemic manifestations of arthritis. J. Clin. Invest. 83:585-592.
45. Chomarat, P., M. C. Rissoan, J. J. Pin, J. Banchereau, and P. Miossec. 1995. Contribution of IL-1, CD14, and CD13 in the increased IL-6 production induced by in vitro monocyte-synoviocyte interactions. J. Immunol. 155:3645-3652.
46. Rathanaswami, P., M. Hachicha, W. L. Wong, T. J. Schall, and S. R. McColl. 1993. Synergistic effect of interleukin-1 beta and tumor necrosis factor alpha on interleukin-8 gene expression in synovial fibroblasts. Evidence that interleukin-8 is the major neutrophil-activating chemokine released in response to monokine activation. Arthritis Rheum. 36:1295-1304.
47. Koch, A. E., S. L. Kunkel, L. A. Harlow, B. Johnson, H. L. Evanoff, G. K. Haines, M. D. Burdick, R. M. Pope, and R. M. Strieter. 1992. Enhanced production of monocyte chemoattractant protein-1 in rheumatoid arthritis. J. Clin. Invest. 90:772-779.
48. Inoue, H., M. Takamori, Y. Shimoyama, H. Ishibashi, S. Yamamoto, and Y. Koshihara. 2002. Regulation by PGE2 of the production of interleukin-6, macrophage colony stimulating factor, and vascular endothelial growth factor in human synovial fibroblasts. Br. J. Pharmacol. 136:287-295.
49. Trebino, C. E., J. L. Stock, C. P. Gibbons, B. M. Naiman, T. S. Wachtmann, J. P. Umland, K. Pandher, J. M. Lapointe, S. Saha, M. L. Roach, et al. 2003. Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc. Natl. Acad. Sci. USA 100:9044-9049.
50. Camacho, M., and L. Vila. 2000. Transcellular formation of thromboxane A (2) in mixed incubations of endothelial cells and aspirin-treated platelets strongly depends on the prostaglandin I-synthase activity. Thromb. Res. 99:155-164.
51. Schumacher, H. R., and R. C. Kitridou. 1972. Synovitis of recent onset. A clinicopathologic study during the first month of disease. Arthritis Rheum. 15:465-485.
52. Kulka, J. P., D. Bocking, M. W. Ropes, and W. Bauer. 1955. Early joint lesions of rheumatoid arthritis; report of eight cases, with knee biopsies of lesions of less than one year's duration. AMA Arch. Pathol. 59:129-150.
53. Henderson, B., and E. R. Pettipher. 1985. The synovial lining cell: biology and pathobiology. Semin. Arthritis Rheum. 15:1-32.
54. Athanasou, N. A., and J. Quinn. 1991. Immunocytochemical analysis of human synovial lining cells: phenotypic relation to other marrow derived cells. Ann. Rheum. Dis. 50:311-315.
55. Xu, S., H. Lu, J. Lin, Z. Chen, and D. Jiang. 2010. Regulation of TNFalpha and IL1beta in rheumatoid arthritis synovial fibroblasts by leukotriene B4. Rheumatol. Int. 30:1183-1189.
56. Fitzpatrick, F. A., D. R. Morton, and M. A. Wynalda. 1982. Albumin stabilizes leukotriene A4. J. Biol. Chem. 257:4680-4683.
57. 4. J. Biol. Chem. 259:11403-11407.
58. Claesson, H. E., and J. Haeggström. 1988. Human endothelial cells stimulate leukotriene synthesis and convert granulocyte released leukotriene A4 into leukotrienes B4, C4, D4 and E4. Eur. J. Biochem. 173:93-100.
59. Feinmark, S. J., and P. J. Cannon. 1986. Endothelial cell leukotriene C4 synthesis results from intercellular transfer of leukotriene A4 synthesized by polymorphonuclear leukocytes. J. Biol. Chem. 261:16466-16472.
60. Ibe, B. O., and W. B. Campbell. 1988. Synthesis and metabolism of leukotrienes by human endothelial cells: influence on prostacyclin release. Biochim. Biophys. Acta 960:309-321.
61. Feinmark, S. J., and P. J. Cannon. 1987. Vascular smooth muscle cell leukotriene C4 synthesis: requirement for transcellular leukotriene A4 metabolism. Biochim. Biophys. Acta 922:125-135.
62. Hollingsworth, J. W., E. R. Siegel, and W. A. Creasey. 1967. Granulocyte survival in synovial exudate of patients with rheumatoid arthritis and other inflammatory joint diseases. Yale J. Biol. Med. 39:289-296.
63. Klickstein, L. B., C. Shapleigh, and E. J. Goetzl. 1980. Lipoxygenation of arachidonic acid as a source of polymorphonuclear leukocyte chemotactic factors in synovial fluid and tissue in rheumatoid arthritis and spondyloarthritis. J. Clin. Invest. 66:1166-1170.
64. Edwards, S. W., and M. B. Hallett. 1997. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol. Today 18:320-324.