Therapeutic targeting of CCR1 attenuates established chronic fungal asthma in mice

British Journal of Pharmacology

Volumn 145, Issue 8, 2005, Pages 1160-1172

  Carpenter, Kristin J ^a   Ewing, Jillian L ^a   Schuh, Jane M ^a   Ness, Traci L ^a   Kunkel, Steven L ^a   Aparici, Monica ^b   Miralpeix, Montserrat ^b   Hogaboam, Cory M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Almirall Prodesfarma S A   (Spain)

Author keywords

Aspergillus fumigatus; BX 471; CCR1; Chemokine; Chemokine receptor; Fungal asthma; Therapy

Indexed keywords

1 [5 CHLORO 2 [2 [4 (4 FLUOROBENZYL) 2 METHYL 1 PIPERAZINYL] 2 OXOETHOXY]PHENYL]UREA; BETA CHEMOKINE; CHEMOKINE RECEPTOR CCR1; INTERLEUKIN 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

AIRWAY; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; ATTENUATION; CELL ISOLATION; CONIDIUM; CYTOKINE RELEASE; DOSE RESPONSE; DRUG EFFECT; DRUG EFFICACY; FEMALE; INFLAMMATION; INNATE IMMUNITY; LUNG; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; ASTHMA; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; IMMUNITY, NATURAL; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; PHENYLUREA COMPOUNDS; PIPERIDINES; RECEPTORS, CHEMOKINE;

EID: 30544433445     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706243     Document Type: Article

References (45)

1. ANDERS, H.J., BANAS, B., LINDE, Y., WELLER, L., COHEN, C.D., KRETZLER, M., MARTIN, S., VIELHAUER, V., SCHLONDORFF, D. & GRONE, H.J. (2003). Bacterial CpG-DNA aggravates immune complex glomerulonephritis: role of TLR9-mediated expression of chemokines and chemokine receptors. J. Am. Soc. Nephrol., 14, 317-326.
2. ANDERS, H.J., BELEMEZOVA, E., EIS, V., SEGERER, S., VIELHAUER, V., PEREZ DE LEMA, G., KRETZLER, M., COHEN, C.D., FRINK, M., HORUK, R., HUDKINS, K.L., ALPERS, C.E., MAMPASO, F. & SCHLONDORFF, D. (2004). Late onset of treatment with a chemokine receptor CCR1 antagonist prevents progression of lupus nephritis in MRL-Fas (1pr) mice. J. Am. Soc. Nephrol., 15, 1504-1513.
3. ANDERS, HJ., VIELHAUER, V., FRINK, M., LINDE, Y., COHEN, C.D., BLATTNER, S.M., KRETZLER, M., STRUTZ, F., MACK, M., GRONE, H.J., ONUFFER, J., HORUK, R., NELSON, P.J. & SCHLONDORFF, D. (2002). A chemokine receptor CCR-1 antagonist reduces renal fibrosis after unilateral ureter ligation. J. Clin. Invest., 109, 251-259.
4. BACHAR, O., ADNER, M., UDDMAN, R. & CARDELL, L.O. (2004). Toll-like receptor stimulation induces airway hyper-responsiveness to bradykinin, an effect mediated by JNK and NF-kappa B signaling pathways. Eur. J. Immunol., 34, 1196-1207.
5. BARNES, P.J. (2001). Cytokine-directed therapies for asthma. J. Allergy Clin. Immunol., 108, S72-S76.
6. BELLOCCHIO, S., MONTAGNOLI, C., BOZZA, S., GAZIANO, R., ROSSI, G., MAMBULA, S.S., VECCHI, A., MANTOVANI, A., LEVITZ, S.M. & ROMANI, L. (2004). The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol., 172, 3059-3069.
7. BLEASE, K., KUNKEL, S.L. & HOGABOAM, C.M. (2001a). IL-18 modulates chronic fungal asthma in a murine model; putative involvement of Toll-like receptor-2. Inflamm. Res., 50, 552-560.
8. BLEASE, K., MEHRAD, B., LUKACS, N.W., KUNKEL, S.L., STANDIFORD, T.J. & HOGABOAM, C.M. (2001b). Antifungal and airway remodeling roles for murine monocyte chemoattractant protein-1/CCL2 during pulmonary exposure to Asperigillus fumigatus conidia. J. Immunol., 166, 1832-1842.
9. BLEASE, K., MEHRAD, B., STANDIFORD, T.J., LUKACS, N.W., KUNKEL, S.L., CHENSUE, S.W., LU, B., GERARD, C.J. & HOGABOAM, C.M. (2000). Airway remodeling is absent in CCR1-/- mice during chronic fungal allergic airway disease. J. Immunol., 165, 1564-1572.
10. CHANTRY, D. & BURGESS, L.E. (2002). Chemokines in allergy. Curr. Drug Targets Inflamm. Allergy, 1, 109-116.
11. EDER, W., KLIMECKI, W., YU, L., VON MUTIUS, E., RIEDLER, J., BRAUN-FAHRLANDER, C., NOWAK, D. & MARTINEZ, F.D. (2004). Toll-like receptor 2 as a major gene for asthma in children of European farmers. J. Allergy Clin. Immunol., 113, 482-488.
12. EVANOFF, H., BURDICK, M.D., MOORE, S.A., KUNKEL, S.L. & STRIETER, R.M. (1992). A sensitive ELISA for the detection of human monocyte chemoattractant protein-1 (MCP-1). Immunol. Invest., 21, 39-49.
13. GRUNIG, G., CORRY, D.B., LEACH, M.W., SEYMOUR, B.W., KURUP, V.P. & RENNICK, D.M. (1997). Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J. Exp. Med., 185, 1089-1099.
14. HALLMAN, M., RAMET, M. & EZEKOWITZ, R.A. (2001). Toll-like receptors as sensors of pathogens. Pediatr. Res., 50, 315-321.
15. HAYASHI, T., BECK, L., ROSSETTO, C., GONG, X., TAKIKAWA, O., TAKABAYASHI, K., BROIDE, D.H., CARSON, D.A. & RAZ, E. (2004). Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J. Clin. Invest., 114, 270-279.
16. HESSELGESSER, J., NG, H.P., LIANG, M., ZHENG, W., MAY, K., BAUMAN, J.G., MONAHAN, S., ISLAM, I., WEI, G.P., GHANNAM, A., TAUB, D.D., ROSSER, M., SNIDER, R.M., MORRISSEY, M.M., PEREZ, H.D. & HORUK, R. (1998). Identification and characterization of small molecule functional antagonists of the CCR1 chemokine receptor. J. Biol. Chem., 273, 15687-15692.
17. HOGABOAM, C.M., BLEASE, K., MEHRAD, B., STEINHAUSER, M.L., STANDIFORD, T.J., KUNKEL, S.L. & LUKACS, N.W. (2000). Chronic airway hyperreactivity, goblet cell hyperplasia, and peribronchial fibrosis during allergic airway disease induced by Aspergillus fumigatus. Am. J. Pathol., 156, 723-732.
18. HOGABOAM, C.M., BLEASE, K. & SCHUH, J.M. (2003). Cytokines and chemokines in allergic bronchopulmonary aspergillosis (ABPA) and experimental Aspergillus-induced allergic airway or asthmatic disease. Front Biosci., 8, e147-e156.
19. HOGABOAM, C.M., GALLINAT, C.S., TAUB, D.D., STRIETER, R.M., KUNKEL, S.L. & LUKACS, N.W. (1999). Immunomodulatory role of C10 chemokine in a murine model of allergic bronchopulmonary aspergillosis. J. Immunol., 162, 6071-6079.
20. HORUK, R., CLAYBERGER, C., KRENSKY, A.M., WANG, Z., GRONE, H.J., WEBER, C., WEBER, K.S., NELSON, P.J., MAY, K., ROSSER, M., DUNNING, L., LIANG, M., BUCKMAN, B., GHANNAM, A., NG, H.P., ISLAM, I., BAUMAN, J.G., WEI, G.P., MONAHAN, S., XU, W., SNIDER, R.M., MORRISSEY, M.M., HESSELGESSER, J. & PEREZ, H.D. (2001a). A non-peptide functional antagonist of the CCR1 chemokine receptor is effective in rat heart transplant rejection. J. Biol. Chem., 276, 4199-4204.
21. HORUK, R., SHUREY, S., NG, H.P., MAY, K., BAUMAN, J.G., ISLAM, I., GHANNAM, A., BUCKMAN, B., WEI, G.P., XU, W., LIANG, M., ROSSER, M., DUNNING, L., HESSELGESSER, J., SNIDER, R.M., MORRISSEY, M.M., PEREZ, H.D. & GREEN, C. (2001b). CCR1-specific non-peptide antagonist: efficacy in a rabbit allograft rejection model. Immunol. Lett., 76, 193-201.
22. LIANG, M., MALLARI, C., ROSSER, M., NG, H.P., MAY, K., MONAHAN, S., BAUMAN, J.G., ISLAM, I., GHANNAM, A., BUCKMAN, B., SHAW, K., WEI, G.P., XU, W., ZHAO, Z., HO, E., SHEN, J., OANH, H., SUBRAMANYAM, B., VERGONA, R., TAUB, D., DUNNING, L., HARVEY, S., SNIDER, R.M., HESSELGESSER, J., MORRISSEY, M.M. & PEREZ, H.D. (2000a). Identification and characterization of a potent, selective, and orally active antagonist of the CC chemokine receptor-1. J. Biol. Chem., 275, 19000-19008.
23. LIANG, M., ROSSER, M., NG, H.P., MAY, K., BAUMAN, J.G., ISLAM, I., GHANNAM, A., KRETSCHMER, P.J., PU, H., DUNNING, L., SNIDER, R.M., MORRISSEY, M.M., HESSELGESSER, J., PEREZ, H.D. & HORUK, R. (2000b). Species selectivity of a small molecule antagonist for the CCRl chemokine receptor. Eur. J. Pharmacol, 389, 41-49.
24. LLOYD, C.M. & RANKIN, S.M. (2003). Chemokines in allergic airway disease. Curr. Opin. Pharmacol., 3, 443-448.
25. MAMBULA, S.S., SAU, K., HENNEKE, P., GOLENBOCK, D.T. & LEVITZ, S.M. (2002). Toll-like receptor (TLR) signaling in response to Aspergillus fumigatus. J. Biol. Chem., 277, 39320-39326.
26. MEHRAD, B., STRIETER, R.M., MOORE, T.A., TSAI, W.C., LIRA, S.A. & STANDIFORD, T.J. (1999). CXC chemokine receptor-2 ligands are necessary components of neutrophil-mediated host defense in invasive pulmonary aspergillosis. J. Immunol., 163, 6086-6094.
27. MEHRAD, B., WIEKOWSKI, M., MORRISON, B.E., CHEN, S.C., CORONEL, E.C., MANFRA, D.J. & LIRA, S.A. (2002). Transient lung-specific expression of the chemokine KC improves outcome in invasive aspergillosis. Am. J. Respir. Crit. Care Med., 166, 1263-1268.
28. MEIER, A., KIRSCHNING, C.J., NIKOLAUS, T., WAGNER, H., HEESEMANN, J. & EBEL, F. (2003). Toll-like receptor (TLR) 2 and TLR4 are essential for Aspergillus-induced activation of murine macrophages. Cell Microbiol, 5, 561-570.
29. NAGASE, H., MIYAMASU, M., YAMAGUCHI, M., FUJISAWA, T., KAWASAKI, H., OHTA, K., YAMAMOTO, K., MORITA, Y. & HIRAI, K. (2001). Regulation of chemokine receptor expression in eosinophils. Int. Arch. Allergy Immunol., 125 (Suppl 1), 29-32.
30. NESS, T.L., HOGABOAM, C.M., STRIETER, R.M. & KUNKEL, S.L. (2003). Immunomodulatory role of CXCR2 during experimental septic peritonitis. J. Immunol., 171, 3775-3784.
31. NG, H.P., MAY, K., BAUMAN, J.G., GHANNAM, A., ISLAM, I., LIANG, M., HORUK, R., HESSELGESSER, J., SNIDER, R.M., PEREZ, H.D. & MORRISSEY, M.M. (1999). Discovery of novel nonpeptide CCR1 receptor antagonists. J. Med. Chem., 42, 4680-4694.
32. OWEN, C. (2001). Chemokine receptors in airway disease: which receptors to target? Pulm. Pharmacol. Ther., 14, 193-202.
33. PHILIPPE, B., IBRAHIM-GRANET, O., PREVOST, M.C., GOUGEROT-POCIDALO, M.A., SANCHEZ PEREZ, M., VAN DER MEEREN, A. & LATGE, J.P. (2003). Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect, Immun., 71, 3034-3042.
34. POWER, C.A. & PROUDFOOT, A.E. (2001). The chemokine system: novel broad-spectrum therapeutic targets. Curr. Opin. Pharmacol., 1, 417-424.
35. PROUDFOOT, A.E., POWER, C.A., ROMMEL, C. & WELLS, T.N. (2003). Strategies for chemokine antagonists as therapeutics. Semin. Immunol., 15, 57-65.
36. REDECKE, V., HACKER, H., DATTA, S.K., FERMIN, A., PITHA, P.M., BROIDE, D.H. & RAZ, E. (2004). Cutting edge: activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J. Immunol., 172, 2739-2743.
37. ROMAGNANI, S. (2002). Cytokines and chemoattractants in allergic inflammation. Mol. Immunol., 38, 881-885.
38. SABROE, I., PECK, M.J., VAN KEULEN, B.J., JORRITSMA, A., SIMMONS, G., CLAPHAM, P.R., WILLIAMS, T.J. & PEASE, J.E. (2000). A small molecule antagonist of chemokine receptors CCR1 and CCR3. Potent inhibition of eosinophil function and CCR3-mediated HIV-1 entry. J. Biol. Chem., 275, 25892-25985.
39. SCHUH, J.M., BLEASE, K., BRUHL, H., MACK, M. & HOGABOAM, C.M. (2003a). Intrapulmonary targeting of RANTES/CCL5-responsive cells prevents chronic fungal asthma. Em. J. Immunol., 33, 3080-3090.
40. SCHUH, J.M., BLEASE, K. & HOGABOAM, C.M. (2002a). The role of CC chemokine receptor 5 (CCR5) and RANTES/CCL5 during chronic fungal asthma in mice. FASEB J., 16, 228-230.
41. SCHUH, J.M., BLEASE, K., KUNKEL, S.L. & HOGABOAM, C.M. (2003b). Chemokines and cytokines: axis and allies in asthma and allergy. Cytokine Growth Factor Rev., 14, 503-510.
42. SCHUH, J.M., POWER, C.A., PROUDFOOT, A.E., KUNKEL, S.L., LUKACS, N.W. & HOGABOAM, C.M. (2002b). Airway hyperresponsiveness, but not airway remodeling, is attenuated during chronic pulmonary allergic responses to Aspergillus in CCR4-/-mice. FASEB J., 16, 1313-1315.
43. STEVENS, D.A., MOSS, R.B., KURUP, V.P., KNUTSEN, A.P., GREENBERGER, P., JUDSON, M.A., DENNING, D.W., CRAMERI, R., BRODY, A.S., LIGHT, M., SKOV, M., MAISH, W. & MASTELLA, G. (2003). Allergic bronchopulmonary aspergillosis in cystic fibrosis - state of the art: Cystic Fibrosis Foundation Consensus Conference. Clin. Infect. Dis., 37 (Suppl 3), S225-S264.
44. TAKEUCHI, O., KAWAI, T., SANJO, H., COPELAND, N.G., GILBERT, D.J., JENKINS, N.A., TAKEDA, K. & AKIRA, S. (1999). TLR6: a novel member of an expanding toll-like receptor family. Gene, 231, 59-65.
45. ZIMMERMANN, N., HOGAN, S.P., MISHRA, A., BRANDT, E.B., BODETTE, T.R., POPE, S.M., FINKELMAN, F.D. & ROTHENBERG, M.E. (2000). Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J. Immunol, 165, 5839-5846.