Antiasthmatic drugs targeting the cysteinyl leukotriene receptor 1 alleviate central nervous system inflammatory cell infiltration and pathogenesis of experimental autoimmune encephalomyelitis

Journal of Immunology

Volumn 187, Issue 5, 2011, Pages 2336-2345

  Wang, Liefeng ^a   Du, Changsheng ^a   Lv, Jie ^a   Wei, Wei ^a   Cui, Ye ^a   Xie, Xin ^a,b  

^a TONGJI UNIVERSITY   (China)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINYL LEUKOTRIENE RECEPTOR 1; GLYCOPROTEIN; INTERLEUKIN 17; LEUKOTRIENE RECEPTOR; MONTELUKAST; MYELIN; PEPTIDOLEUKOTRIENE; UNCLASSIFIED DRUG; ZAFIRLUKAST;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL INFILTRATION; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; DRUG TARGETING; FEMALE; HELPER CELL; INFLAMMATORY CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MEMBRANE PERMEABILITY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPINAL CORD; T LYMPHOCYTE; TISSUE DISTRIBUTION;

ACETATES; ANIMALS; ANTI-ASTHMATIC AGENTS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; CELL SEPARATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; MICE; MICE, INBRED C57BL; QUINOLINES; RECEPTORS, LEUKOTRIENE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPINAL CORD; TOSYL COMPOUNDS;

EID: 80052672267     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100333     Document Type: Article

References (53)

1. Krishnamoorthy, G., A. Saxena, L. T. Mars, H. S. Domingues, R. Mentele, A. Ben-Nun, H. Lassmann, K. Dornmair, F. C. Kurschus, R. S. Liblau, and H. Wekerle. 2009. Myelin-specific T cells also recognize neuronal autoantigen in a transgenic mouse model of multiple sclerosis. Nat. Med. 15: 626-632.
2. Harkiolaki, M., S. L. Holmes, P. Svendsen, J. W. Gregersen, L. T. Jensen, R. McMahon, M. A. Friese, G. Van Boxel, R. Etzensperger, J. S. Tzartos, et al. 2009. T cell-mediated autoimmune disease due to low-affinity crossreactivity to common microbial peptides. Immunity 30: 348-357.
3. Bennett, J., J. Basivireddy, A. Kollar, K. E. Biron, P. Reickmann, W. A. Jefferies, and S. McQuaid. 2010. Blood-brain barrier disruption and enhanced vascular permeability in the multiple sclerosis model EAE. J. Neuroimmunol. 229: 180-191.
4. Hay, D. W., T. J. Torphy, and B. J. Undem. 1995. Cysteinyl leukotrienes in asthma: old mediators up to new tricks. Trends Pharmacol. Sci. 16: 304-309.
5. Machida, I., H. Matsuse, Y. Kondo, T. Kawano, S. Saeki, S. Tomari, Y. Obase, C. Fukushima, and S. Kohno. 2004. Cysteinyl leukotrienes regulate dendritic cell functions in a murine model of asthma. J. Immunol. 172: 1833-1838. (Pubitemid 38116832)
6. Shirasaki, H. 2008. Cysteinyl leukotriene receptor CysLT1 as a novel therapeutic target for allergic rhinitis treatment. Expert Opin. Ther. Targets 12: 415-423. (Pubitemid 351546368)
7. Fabis, M. J., T. W. Phares, R. B. Kean, H. Koprowski, and D. C. Hooper. 2008. Blood-brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity. Proc. Natl. Acad. Sci. USA 105: 15511-15516.
8. Engelhardt, B. 2006. Molecular mechanisms involved in T cell migration across the blood-brain barrier. J. Neural Transm. 113: 477-485.
9. Allayee, H., J. Hartiala, W. Lee, M. Mehrabian, C. G. Irvin, D. V. Conti, and J. J. Lima. 2007. The effect of montelukast and low-dose theophylline on cardiovascular disease risk factors in asthmatics. Chest 132: 868-874.
10. 4 excretion: a biomarker of inflammatory bowel disease activity. Inflamm. Bowel Dis. 14: 769-774.
11. Tantisira, K. G., and J. M. Drazen. 2009. Genetics and pharmacogenetics of the leukotriene pathway. J. Allergy Clin. Immunol. 124: 422-427.
12. 4 receptor, BLT1, is required for the induction of experimental autoimmune encephalomyelitis. Biochem. Biophys. Res. Commun. 394: 673-678.
13. Jiang, Y., L. A. Borrelli, Y. Kanaoka, B. J. Bacskai, and J. A. Boyce. 2007. CysLT2 receptors interact with CysLT1 receptors and down-modulate cysteinyl leukotriene dependent mitogenic responses of mast cells. Blood 110: 3263-3270. (Pubitemid 350106319)
14. Rao, N. L., P. J. Dunford, X. Xue, X. Jiang, K. A. Lundeen, F. Coles, J. P. Riley, K. N. Williams, C. A. Grice, J. P. Edwards, et al. 2007. Anti-inflammatory activity of a potent, selective leukotriene A4 hydrolase inhibitor in comparison with the 5-lipoxygenase inhibitor zileuton. J. Pharmacol. Exp. Ther. 321: 1154-1160. (Pubitemid 46762702)
15. Yu, G. L., E. Q. Wei, S. H. Zhang, H. M. Xu, L. S. Chu, W. P. Zhang, Q. Zhang, Z. Chen, R. H. Mei, and M. H. Zhao. 2005. Montelukast, a cysteinyl leukotriene receptor-1 antagonist, dose- and time-dependently protects against focal cerebral ischemia in mice. Pharmacology 73: 31-40. (Pubitemid 39664219)
16. Schelfhout, V., V. Van De Velde, R. Pauwels, and G. Joos. 2008. The effect of the leukotriene receptor antagonist zafirlukast on neurokinin A-induced bronchoconstriction in patients with asthma: a comparison with leukotriene D4 induced broncoconstriction. Pulm. Pharmacol. Ther. 21: 276-284. (Pubitemid 351312670)
17. Nishio, H., Y. Hayashi, S. Terashima, and K. Takeuchi. 2007. Protective effect of pranlukast, a cysteinyl-leukotriene receptor 1 antagonist, on indomethacininduced small intestinal damage in rats. Inflammopharmacology 15: 266-272. (Pubitemid 351196135)
18. Whitney, L. W., S. K. Ludwin, H. F. McFarland, and W. E. Biddison. 2001. Microarray analysis of gene expression in multiple sclerosis and EAE identifies 5-lipoxygenase as a component of inflammatory lesions. J. Neuroimmunol. 121: 40-48. (Pubitemid 34008449)
19. Marusic, S., P. Thakker, J. W. Pelker, N. L. Stedman, K. L. Lee, J. C. McKew, L. Han, X. Xu, S. F. Wolf, A. J. Borey, et al. 2008. Blockade of cytosolic phospholipase A2a prevents experimental autoimmune encephalomyelitis and diminishes development of Th1 and Th17 responses. J. Neuroimmunol. 204: 29-37.
20. Gladue, R. P., L. A. Carroll, A. J. Milici, D. N. Scampoli, H. A. Stukenbrok, E. R. Pettipher, E. D. Salter, L. Contillo, and H. J. Showell. 1996. Inhibition of leukotriene B4-receptor interaction suppresses eosinophil infiltration and disease pathology in a murine model of experimental allergic encephalomyelitis. J. Exp. Med. 183: 1893-1898. (Pubitemid 26134329)
21. Hooper, D. C., G. S. Scott, A. Zborek, T. Mikheeva, R. B. Kean, H. Koprowski, and S. V. Spitsin. 2000. Uric acid, a peroxynitrite scavenger, inhibits CNS inflammation, blood-CNS barrier permeability changes, and tissue damage in a mouse model of multiple sclerosis. FASEB J. 14: 691-698. (Pubitemid 30198568)
22. Mabondzo, A., M. Bottlaender, A. C. Guyot, K. Tsaouin, J. R. Deverre, and P. V. Balimane. 2010. Validation of in vitro cell-based human blood-brain barrier model using clinical positron emission tomography radioligands to predict in vivo human brain penetration. Mol. Pharm. 7: 1805-1815.
23. Culot, M., C. Mysiorek, M. Renftel, B. D. Roussel, Y. Hommet, D. Vivien, R. Cecchelli, L. Fenart, V. Berezowski, M. P. Dehouck, and S. Lundquist. 2009. Cerebrovascular protection as a possible mechanism for the protective effects of NXY-059 in preclinical models: an in vitro study. Brain Res. 1294: 144-152.
24. Aranami, T., and T. Yamamura. 2008. Th17 cells and autoimmune encephalomyelitis (EAE/MS). Allergol. Int. 57: 115-120. (Pubitemid 351897665)
25. Oyamada, A., H. Ikebe, M. Itsumi, H. Saiwai, S. Okada, K. Shimoda, Y. Iwakura, K. I. Nakayama, Y. Iwamoto, Y. Yoshikai, and H. Yamada. 2009. Tyrosine kinase 2 plays critical roles in the pathogenic CD4 T cell responses for the development of experimental autoimmune encephalomyelitis. J. Immunol. 183: 7539-7546.
26. Yu, J. Z., J. Ding, C. G. Ma, C. H. Sun, Y. F. Sun, C. Z. Lu, and B. G. Xiao. 2010. Therapeutic potential of experimental autoimmune encephalomyelitis by Fasudil, a Rho kinase inhibitor. J. Neurosci. Res. 88: 1664-1672.
27. Nozaki, M., M. Yoshikawa, K. Ishitani, H. Kobayashi, K. Houkin, K. Imai, Y. Ito, and T. Muraki. 2010. Cysteinyl leukotriene receptor antagonists inhibit tumor metastasis by inhibiting capillary permeability. Keio J. Med. 59: 10-18.
28. Kolaczkowska, E. 2002. Shedding light on vascular permeability during peritonitis: role of mast cell histamine versus macrophage cysteinyl leukotrienes. Inflamm. Res. 51: 519-521. (Pubitemid 36009177)
29. Li, G., M. J. Simon, L. M. Cancel, Z. D. Shi, X. Ji, J. M. Tarbell, B. Morrison, III, and B. M. Fu. 2010. Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery studies. Ann. Biomed. Eng. 38: 2499-2511.
30. Huang, W., S. Y. Eum, I. E. András, B. Hennig, and M. Toborek. 2009. PPARa and PPARγ attenuate HIV-induced dysregulation of tight junction proteins by modulations of matrix metalloproteinase and proteasome activities. FASEB J. 23: 1596-1606.
31. Schulze-Topphoff, U., A. Prat, T. Prozorovski, V. Siffrin, M. Paterka, J. Herz, I. Bendix, I. Ifergan, I. Schadock, M. A. Mori, et al. 2009. Activation of kinin receptor B1 limits encephalitogenic T lymphocyte recruitment to the central nervous system. Nat. Med. 15: 788-793.
32. Rolls, A., L. Cahalon, S. Bakalash, H. Avidan, O. Lider, and M. Schwartz. 2006. A sulfated disaccharide derived from chondroitin sulfate proteoglycan protects against inflammation-associated neurodegeneration. FASEB J. 20: 547-549. (Pubitemid 46671245)
33. Fregonese, L., M. Silvestri, F. Sabatini, and G. A. Rossi. 2002. Cysteinyl leukotrienes induce human eosinophil locomotion and adhesion molecule expression via a CysLT1 receptor-mediated mechanism. Clin. Exp. Allergy 32: 745-750. (Pubitemid 34534022)
34. 4 induces gene expression in human monocytes through cysteinyl leukotriene type I receptor. J. Allergy Clin. Immunol. 121: 215-221.e1.
35. John, G. R., S. L. Shankar, B. Shafit-Zagardo, A. Massimi, S. C. Lee, C. S. Raine, and C. F. Brosnan. 2002. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 8: 1115-1121. (Pubitemid 35175966)
36. Hohlfeld, R., and H. Wekerle. 2004. Autoimmune concepts of multiple sclerosis as a basis for selective immunotherapy: from pipe dreams to (therapeutic) pipelines. Proc. Natl. Acad. Sci. USA 101(Suppl. 2): 14599-14606. (Pubitemid 39346730)
37. Jalink, K., and W. H. Moolenaar. 2010. G protein-coupled receptors: the inside story. Bioessays 32: 13-16.
38. Li, Y. Y., T. J. Hou, and W. A. Goddard III, 2010. Computational modeling of structure-function of G protein-coupled receptors with applications for drug design. Curr. Med. Chem. 17: 1167-1180.
39. Brinkmann, V., A. Billich, T. Baumruker, P. Heining, R. Schmouder, G. Francis, S. Aradhye, and P. Burtin. 2010. Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis. Nat. Rev. Drug Discov. 9: 883-897.
40. 2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling. J. Exp. Med. 206: 535-548.
41. Stegbauer, J., D. H. Lee, S. Seubert, G. Ellrichmann, A. Manzel, H. Kvakan, D. N. Muller, S. Gaupp, L. C. Rump, R. Gold, and R. A. Linker. 2009. Role of the renin-angiotensin system in autoimmune inflammation of the central nervous system. Proc. Natl. Acad. Sci. USA 106: 14942-14947.
42. Sporici, R., and T. B. Issekutz. 2010. CXCR3 blockade inhibits T-cell migration into the CNS during EAE and prevents development of adoptively transferred, but not actively induced, disease. Eur. J. Immunol. 40: 2751-2761.
43. Kuwabara, T., F. Ishikawa, T. Yasuda, K. Aritomi, H. Nakano, Y. Tanaka, Y. Okada, M. Lipp, and T. Kakiuchi. 2009. CCR7 ligands are required for development of experimental autoimmune encephalomyelitis through generating IL-23-dependent Th17 cells. J. Immunol. 183: 2513-2521.
44. 4 are mediated by the 7-transmembrane receptor CysLT1. Blood 97: 3433-3440.
45. Ni, J., Y. N. Zhu, X. G. Zhong, Y. Ding, L. F. Hou, X. K. Tong, W. Tang, S. Ono, Y. F. Yang, and J. P. Zuo. 2009. The chemokine receptor antagonist, TAK-779, decreased experimental autoimmune encephalomyelitis by reducing inflammatory cell migration into the central nervous system, without affecting T cell function. Br. J. Pharmacol. 158: 2046-2056.
46. H-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10: 514-523.
47. Kolaczkowska, E., S. Shahzidi, R. Seljelid, N. Van Rooijen, and B. Plytycz. 2002. Early vascular permeability in murine experimental peritonitis is comediated by resident peritoneal macrophages and mast cells: crucial involvement of macrophage-derived cysteinyl-leukotrienes. Inflammation 26: 61-71. (Pubitemid 34274484)
48. Sonobe, Y., H. Takeuchi, K. Kataoka, H. Li, S. Jin, M. Mimuro, Y. Hashizume, Y. Sano, T. Kanda, T. Mizuno, and A. Suzumura. 2009. Interleukin-25 expressed by brain capillary endothelial cells maintains blood-brain barrier function in a protein kinase Cε-dependent manner. J. Biol. Chem. 284: 31834-31842.
49. Furuse, M. 2010. Molecular basis of the core structure of tight junctions. Cold Spring Harb. Perspect. Biol. 2: a002907.
50. Umeda, K., J. Ikenouchi, S. Katahira-Tayama, K. Furuse, H. Sasaki, M. Nakayama, T. Matsui, S. Tsukita, M. Furuse, and S. Tsukita. 2006. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126: 741-754. (Pubitemid 44233624)
51. Willis, C. L., D. S. Meske, and T. P. Davis. 2010. Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygenation. J. Cereb. Blood Flow Metab. 30: 1847-1859.
52. Leal, E. C., J. Martins, P. Voabil, J. Liberal, C. Chiavaroli, J. Bauer, J. Cunha-Vaz, and A. F. Ambrósio. 2010. Calcium dobesilate inhibits the alterations in tight junction proteins and leukocyte adhesion to retinal endothelial cells induced by diabetes. Diabetes 59: 2637-2645.
53. 4. Mol. Immunol. 46: 1204-1211.