5-Lipoxygenase-deficient mice infected with Borrelia burgdorferi develop persistent arthritis

Journal of Immunology

Volumn 186, Issue 5, 2011, Pages 3076-3084

  Blaho, Victoria A ^a,b   Zhang, Yan ^a   Hughes Hanks, Jennifer M ^a   Brown, Charles R ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE; IMMUNOGLOBULIN G ANTIBODY; LEUKOTRIENE B4; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BORRELIA BURGDORFERI; CONTROLLED STUDY; DISEASE DURATION; EFFEROCYTOSIS; ENZYME ACTIVITY; FEMALE; IMMUNOPATHOGENESIS; JOINT SWELLING; LYME DISEASE; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPIROCHETE;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; ARTHRITIS, EXPERIMENTAL; BORRELIA BURGDORFERI; CELLS, CULTURED; FEMALE; INFLAMMATION; INFLAMMATION MEDIATORS; LYME DISEASE; MICE; MICE, 129 STRAIN; MICE, INBRED C3H; MICE, KNOCKOUT; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 79952764903     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003473     Document Type: Article

References (69)

1. Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, and J. P. Davis. 1982. Lyme disease - a tick-borne spirochetosis? Science 216: 1317-1319.
2. CDC. 2010. Final 2009 reports of nationally notifiable infectious diseases. Morbid. Mortal. Weekly Rep. 59: 1025-1039.
3. Steere, A. C., R. T. Schoen, and E. Taylor. 1987. The clinical evolution of Lyme arthritis. Ann. Intern. Med. 107: 725-731.
4. Nocton, J. J., F. Dressler, B. J. Rutledge, P. N. Rys, D. H. Persing, and A. C. Steere. 1994. Detection of Borrelia burgdorferi DNA by polymerase chain reaction in synovial fluid from patients with Lyme arthritis. N. Engl. J. Med. 330: 229-234.
5. Wormser, G. P., R. J. Dattwyler, E. D. Shapiro, J. J. Halperin, A. C. Steere, M. S. Klempner, P. J. Krause, J. S. Bakken, F. Strle, G. Stanek, et al. 2006. The clinical assessment, treatment, and prevention of lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin. Infect. Dis. 43: 1089-1134.
6. 2008. The chronic debate over Lyme disease. Nat. Med. 14: 1135-1139.
7. Barthold, S. W., D. S. Beck, G. M. Hansen, G. A. Terwilliger, and K. D. Moody. 1990. Lyme borreliosis in selected strains and ages of laboratory mice. J. Infect. Dis. 162: 133-138.
8. Schaible, U. E., M. D. Kramer, C. Museteanu, G. Zimmer, H. Mossmann, and M. M. Simon. 1989. The severe combined immunodeficiency (scid) mouse. A laboratory model for the analysis of Lyme arthritis and carditis. J. Exp. Med. 170: 1427-1432.
9. Barthold, S. W., C. L. Sidman, and A. L. Smith. 1992. Lyme borreliosis in genetically resistant and susceptible mice with severe combined immunodeficiency. Am. J. Trop. Med. Hyg. 47: 605-613.
10. Brown, C. R., and S. L. Reiner. 1999. Genetic control of experimental lyme arthritis in the absence of specific immunity. Infect. Immun. 67: 1967-1973.
11. Ritzman, A. M., J. M. Hughes-Hanks, V. A. Blaho, L. E. Wax, W. J. Mitchell, and C. R. Brown. 2010. The chemokine receptor CXCR2 ligand KC (CXCL1) mediates neutrophil recruitment and is critical for development of experimental Lyme arthritis and carditis. Infect. Immun. 78: 4593-4600.
12. Brown, C. R., V. A. Blaho, and C. M. Loiacono. 2003. Susceptibility to experimental Lyme arthritis correlates with KC and monocyte chemoattractant protein-1 production in joints and requires neutrophil recruitment via CXCR2. J. Immunol. 171: 893-901.
13. Barthold, S. W., M. deSouza, and S. Feng. 1996. Serum-mediated resolution of Lyme arthritis in mice. Lab. Invest. 74: 57-67.
14. Wooten, R. M., Y. Ma, R. A. Yoder, J. P. Brown, J. H. Weis, J. F. Zachary, C. J. Kirschning, and J. J.Weis. 2002. Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J. Immunol. 168: 348-355. (Pubitemid 34014136)
15. Bolz, D. D., R. S. Sundsbak, Y. Ma, S. Akira, C. J. Kirschning, J. F. Zachary, J. H. Weis, and J. J. Weis. 2004. MyD88 plays a unique role in host defense but not arthritis development in Lyme disease. J. Immunol. 173: 2003-2010.
16. Liu, N., R. R. Montgomery, S. W. Barthold, and L. K. Bockenstedt. 2004. Myeloid differentiation antigen 88 deficiency impairs pathogen clearance but does not alter inflammation in Borrelia burgdorferi-infected mice. Infect. Immun. 72: 3195-3203.
17. Blaho, V. A., W. J. Mitchell, and C. R. Brown. 2008. Arthritis develops but fails to resolve during inhibition of cyclooxygenase 2 in a murine model of Lyme disease. Arthritis Rheum. 58: 1485-1495.
18. Harizi, H., J. B. Corcuff, and N. Gualde. 2008. Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol. Med. 14: 461-469.
19. Chen, X. S., J. R. Sheller, E. N. Johnson, and C. D. Funk. 1994. Role of leukotrienes revealed by targeted disruption of the 5-lipoxygenase gene. Nature 372: 179-182.
20. Serhan, C. N., S. D. Brain, C. D. Buckley, D. W. Gilroy, C. Haslett, L. A. O'Neill, M. Perretti, A. G. Rossi, and J. L. Wallace. 2007. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21: 325-332.
21. Griffiths, R. J., M. A. Smith, M. L. Roach, J. L. Stock, E. J. Stam, A. J. Milici, D. N. Scampoli, J. D. Eskra, R. S. Byrum, B. H. Koller, and J. D. McNeish. 1997. Collagen-induced arthritis is reduced in 5-lipoxygenase- activating protein-deficient mice. J. Exp. Med. 185: 1123-1129.
22. 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.
23. Kuwabara, K., K. Yasui, H. Jyoyama, T. Maruyama, J. H. Fleisch, and Y. Hori. 2000. Effects of the second-generation leukotriene B(4) receptor antagonist, LY293111Na, on leukocyte infiltration and collagen-induced arthritis in mice. Eur. J. Pharmacol. 402: 275-285.
24. Shao, W. H., A. Del Prete, C. B. Bock, and B. Haribabu. 2006. Targeted disruption of leukotriene B4 receptors BLT1 and BLT2: a critical role for BLT1 in collagen-induced arthritis in mice. J. Immunol. 176: 6254-6261.
25. 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.
26. Kim, N. D., R. C. Chou, E. Seung, A. M. Tager, and A. D. Luster. 2006. A unique requirement for the leukotriene B4 receptor BLT1 for neutrophil recruitment in inflammatory arthritis. J. Exp. Med. 203: 829-835.
27. Mathis, S. P., V. R. Jala, D. M. Lee, and B. Haribabu. 2010. Nonredundant roles for leukotriene B4 receptors BLT1 and BLT2 in inflammatory arthritis. J. Immunol. 185: 3049-3056.
28. Chou, R. C., N. D. Kim, C. D. Sadik, E. Seung, Y. Lan, M. H. Byrne, B. Haribabu, Y. Iwakura, and A. D. Luster. 2010. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 33: 266-278.
29. Bailie, M. B., T. J. Standiford, L. L. Laichalk, M. J. Coffey, R. Strieter, and M. Peters-Golden. 1996. Leukotriene-deficient mice manifest enhanced lethality from Klebsiella pneumonia in association with decreased alveolar macrophage phagocytic and bactericidal activities. J. Immunol. 157: 5221-5224. (Pubitemid 126448936)
30. Mancuso, P., P. Nana-Sinkam, and M. Peters-Golden. 2001. Leukotriene B4 augments neutrophil phagocytosis of Klebsiella pneumoniae. Infect. Immun. 69: 2011-2016.
31. Serezani, C. H., J. H. Perrela, M. Russo, M. Peters-Golden, and S. Jancar. 2006. Leukotrienes are essential for the control of Leishmania amazonensis infection and contribute to strain variation in susceptibility. J. Immunol. 177: 3201-3208. (Pubitemid 44277838)
32. Aliberti, J., C. Serhan, and A. Sher. 2002. Parasite-induced lipoxin A4 is an endogenous regulator of IL-12 production and immunopathology in Toxoplasma gondii infection. J. Exp. Med. 196: 1253-1262.
33. Wakeland, E., L. Morel, K. Achey, M. Yui, and J. Longmate. 1997. Speed congenics: a classic technique in the fast lane (relatively speaking). Immunol. Today 18: 472-477. (Pubitemid 27441589)
34. Brown, C. R., A. Y. C. Lai, S. T. Callen, V. A. Blaho, J. M. Hughes, and W. J. Mitchell. 2008. Adenoviral delivery of interleukin-10 fails to attenuate experimental Lyme disease. Infect. Immun. 76: 5500-5507.
35. Morrison, T. B., Y. Ma, J. H. Weis, and J. J. Weis. 1999. Rapid and sensitive quantification of Borrelia burgdorferi-infected mouse tissues by continuous fluorescent monitoring of PCR. J. Clin. Microbiol. 37: 987-992.
36. Blaho, V. A., M. W. Buczynski, E. A. Dennis, and C. R. Brown. 2009. Cyclooxygenase-1 orchestrates germinal center formation and antibody classs-witch via regulation of IL-17. J. Immunol. 183: 5644-5653.
37. Boxio, R., C. Bossenmeyer-Pourié, N. Steinckwich, C. Dournon, and O. Nüsse. 2004. Mouse bone marrow contains large numbers of functionally competent neutrophils. J. Leukoc. Biol. 75: 604-611.
38. Maderna, P., S. Yona, M. Perretti, and C. Godson. 2005. Modulation of phagocytosis of apoptotic neutrophils by supernatant from dexamethaso-netreated macrophages and annexin-derived peptide Ac(2-26). J. Immunol. 174: 3727-3733.
39. Takano, T., S. Fiore, J. F. Maddox, H. R. Brady, N. A. Petasis, and C. N. Serhan. 1997. Aspirin-triggered 15-epi-lipoxin A4 (LXA4) and LXA4 stable analogues are potent inhibitors of acute inflammation: evidence for anti-inflammatory receptors. J. Exp. Med. 185: 1693-1704.
40. Samuelsson, B., S. E. Dahlén, J. A. Lindgren, C. A. Rouzer, and C. N. Serhan. 1987. Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 237: 1171-1176.
41. Jakobsson, P. J., D. Steinhilber, B. Odlander, O. Rådmark, H. E. Claesson, and B. Samuelsson. 1992. On the expression and regulation of 5-lipoxygenase in human lymphocytes. Proc. Nat. Acad. Sci. USA 89: 3521-3525.
42. Kim, D. C., F. I. Hsu, N. A. Barrett, D. S. Friend, R. Grenningloh, I. C. Ho, A. Al-Garawi, J. M. Lora, B. K. Lam, K. F. Austen, and Y. Kanaoka. 2006. Cysteinyl leukotrienes regulate Th2 cell-dependent pulmonary inflammation. J. Immunol. 176: 4440-4448. (Pubitemid 44264424)
43. Chen, H., J. Qin, P. Wei, J. Zhang, Q. Li, L. Fu, S. Li, C. Ma, and B. Cong. 2009. Effects of leukotriene B4 and prostaglandin E2 on the differentiation of murine Foxp3+ T regulatory cells and Th17 cells. Prostaglandins Leukot. Essent. Fatty Acids 80: 195-200.
44. Firestein, G. S., M. Yeo, and N. J. Zvaifler. 1995. Apoptosis in rheumatoid arthritis synovium. J. Clin. Invest. 96: 1631-1638.
45. Schrijvers, D. M., G. R. Y. De Meyer, M. M. Kockx, A. G. Herman, and W. Martinet. 2005. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 25: 1256-1261.
46. Mancuso, P., T. J. Standiford, T. Marshall, and M. Peters-Golden. 1998. 5-Lipoxygenase reaction products modulate alveolar macrophage phagocytosis of Klebsiella pneumoniae. Infect. Immun. 66: 5140-5146.
47. Ravichandran, K. S. 2010. Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J. Exp. Med. 207: 1807-1817.
48. Montgomery, R. R., D. Lusitani, A. de Boisfleury Chevance, and S. E. Malawista. 2002. Human phagocytic cells in the early innate immune response to Borrelia burgdorferi. J. Infect. Dis. 185: 1773-1779.
49. Canetti, C., B. Hu, J. L. Curtis, and M. Peters-Golden. 2003. Syk activation is a leukotriene B4-regulated event involved in macrophage phagocytosis of IgG-coated targets but not apoptotic cells. Blood 102: 1877-1883. (Pubitemid 37022587)
50. Fourie, A. M. 2009. Modulation of inflammatory disease by inhibitors of leukotriene A4 hydrolase. Curr. Opin. Investig. Drugs 10: 1173-1182.
51. Sampson, A. P. 2009. FLAP inhibitors for the treatment of inflammatory diseases. Curr. Opin. Investig. Drugs 10: 1163-1172.
52. Buczynski, M. W., D. S. Dumlao, and E. A. Dennis. 2009. Thematic review series: proteomics. An integrated omics analysis of eicosanoid biology. J. Lipid Res. 50: 1015-1038.
53. Alencar, N. M., R. S. Oliveira, J. G. Figueiredo, I. J. Cavalcante, M. P. Matos, F. Q. Cunha, J. V. Nunes, L. R. Bomfim, and M. V. Ramos. 2010. An anti-inflammatory lectin from Luetzelburgia auriculata seeds inhibits adhesion and rolling of leukocytes and modulates histamine and PGE2 action in acute inflammation models. Inflamm. Res. 59: 245-254.
54. Mao, J. T., I. H. Tsu, S. M. Dubinett, B. Adams, T. Sarafian, F. Baratelli, M. D. Roth, and K. J. Serio. 2004. Modulation of pulmonary leukotriene B4 production by cyclooxygenase-2 inhibitors and lipopolysaccharide. Clin. Cancer Res. 10: 6872-6878.
55. Kapoor, M., F. Kojima, M. Qian, L. Yang, and L. J. Crofford. 2006. Shunting of prostanoid biosynthesis in microsomal prostaglandin E synthase-1 null embryo fibroblasts: regulatory effects on inducible nitric oxide synthase expression and nitrite synthesis. FASEB J. 20: 2387-2389.
56. Mahshid, Y., M. R. Lisy, X. Wang, R. Spanbroek, J. Flygare, B. Christensson, M. Bjorkholm, B. Sander, A. Habenicht, and H. E. Claesson. 2009. High expression of 5-lipoxygenase in normal and malignant mantle zone B lymphocytes. BMC Immunol. 10: 2.
57. Secor, W. E., M. R. Powell, J. Morgan, T. A. Wynn, and C. D. Funk. 1998. Mice deficient for 5-lipoxygenase, but not leukocyte-type 12-lipoxygenase, display altered immune responses during infection with Schistosoma mansoni. Prostaglandins Other Lipid Mediat. 56: 291-304.
58. Weis, J. J. 2002. Host-pathogen interactions and the pathogenesis of murine Lyme disease. Curr. Opin. Rheumatol. 14: 399-403.
59. Levy, B. D., C. B. Clish, B. Schmidt, K. Gronert, and C. N. Serhan. 2001. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2: 612-619.
60. Vandivier, R. W., P. M. Henson, and I. S. Douglas. 2006. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest 129: 1673-1682.
61. Voll, R. E., M. Herrmann, E. A. Roth, C. Stach, J. R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
62. Fadok, V. A., D. L. Bratton, A. Konowal, P. W. Freed, J. Y. Westcott, and P. M. Henson. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-b, PGE2, and PAF. J. Clin. Invest. 101: 890-898. (Pubitemid 28096086)
63. Huynh, M. L., K. C. Malcolm, C. Kotaru, J. A. Tilstra, J. Y. Westcott, V. A. Fadok, and S. E. Wenzel. 2005. Defective apoptotic cell phagocytosis attenuates prostaglandin E2 and 15-hydroxyeicosatetraenoic acid in severe asthma alveolar macrophages. Am. J. Respir. Crit. Care Med. 172: 972-979.
64. Munoz, L. E., U. S. Gaipl, S. Franz, A. Sheriff, R. E. Voll, J. R. Kalden, and M. Herrmann. 2005. SLE - a disease of clearance deficiency? Rheumatology (Oxford) 44: 1101-1107.
65. Serhan, C. N. 2010. Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am. J. Pathol. 177: 1576-1591.
66. Blaho, V. A., M. W. Buczynski, C. R. Brown, and E. A. Dennis. 2009. Lipidomic analysis of dynamic eicosanoid responses during the induction and resolution of Lyme arthritis. J. Biol. Chem. 284: 21599-21612.
67. Serhan, C. N., S. Yacoubian, and R. Yang. 2008. Anti-inflammatory and proresolving lipid mediators. Annu. Rev. Pathol. 3: 279-312.
68. Godson, C., S. Mitchell, K. Harvey, N. A. Petasis, N. Hogg, and H. R. Brady. 2000. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 164: 1663-1667.
69. Serhan, C. N. 2001. Lipoxins and aspirin-triggered 15-epi-lipoxins are endogenous components of antiinflammation: emergence of the counterregulatory side. Arch. Immunol. Ther. Exp. (Warsz.) 49: 177-188.