A CD1d-dependent antagonist inhibits the activation of invariant NKT cells and prevents development of allergen-induced airway hyperreactivity

Journal of Immunology

Volumn 184, Issue 4, 2010, Pages 2107-2115

  Lombardi, Vincent ^a   Stock, Philippe ^b   Singh, Abinav K ^a   Kerzerho, Jerome ^a   Yang, Wen ^c   Sullivan, Barbara A ^d   Li, Xiangming ^e   Shiratsuchi, Takayuki ^e   Hnatiuk, Nathan E ^f   Howell, Amy R ^f   Yu, Karl O A ^g   Porcelli, Steven A ^g   Tsuji, Moriya ^e   Kronenberg, Mitchell ^d   Wilson, S Brian ^c   Akbari, Omid ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^e ROCKEFELLER UNIVERSITY   (United States)

^f UNIVERSITY OF CONNECTICUT   (United States)

^g ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; ANTIALLERGIC AGENT; CD1D ANTIGEN; DIPALMITOYLPHOSPHATIDYLETHANOLAMINE POLYETHYLENE GLYCOL; MITOGEN ACTIVATED PROTEIN KINASE; OVALBUMIN; UNCLASSIFIED DRUG; ALLERGEN; ALPHA-GALACTOSYLCERAMIDE; CD1D PROTEIN, HUMAN; CD1D1 PROTEIN, MOUSE; DPPE PEG2000; DPPE-PEG2000; GALACTOSYLCERAMIDE; IMMUNOSUPPRESSIVE AGENT; MACROGOL DERIVATIVE; PHOSPHATIDYLETHANOLAMINE;

AIRWAY HYPERREACTIVITY; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; LYMPHOCYTIC INFILTRATION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE; SENSITIZATION; SINGLE DRUG DOSE; T LYMPHOCYTE ACTIVATION; ANIMAL; BAGG ALBINO MOUSE; BINDING COMPETITION; BRONCHUS HYPERREACTIVITY; CELL LINE; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY;

ALLERGENS; ANIMALS; ANTIGENS, CD1D; BINDING, COMPETITIVE; BRONCHIAL HYPERREACTIVITY; CELL LINE; DISEASE MODELS, ANIMAL; FEMALE; GALACTOSYLCERAMIDES; HUMANS; IMMUNOSUPPRESSIVE AGENTS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; NATURAL KILLER T-CELLS; OVALBUMIN; PHOSPHATIDYLETHANOLAMINES; POLYETHYLENE GLYCOLS;

EID: 77949899445     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901208     Document Type: Article

References (54)

1. Centers for Disease Control and Prevention (CDC). 1998. Forecasted state-specific estimates of self-reported asthma prevalence - United States, 1998. MMWR Morb. Mortal. Wkly. Rep. 47: 1022-1025.
2. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyper-responsiveness. Annu. Rev. Immunol. 17: 255-281.
3. Robinson, D. S., Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A. M. Bentley, C. Corrigan, S. R. Durham, and A. B. Kay. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326: 298-304.
4. Grünig, G., M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley, and D. B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263.
5. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282: 2258-2261.
6. Martinez, F. D., A. L. Wright, L. M. Taussig, C. J. Holberg, M. Halonen, and W. J. Morgan; The Group Health Medical Associates. 1995. Asthma and wheezing in the first six years of life. N. Engl. J. Med. 332: 133-138.
7. Burrows, B., F. D. Martinez, M. Halonen, R. A. Barbee, and M. G. Cline. 1989. Association of asthma with serum IgE levels and skin-test reactivity to allergens. N. Engl. J. Med. 320: 271-277.
8. Illi, S., E. von Mutius, S. Lau, R. Nickel, B. Niggemann, C. Sommerfeld, and U. Wahn; Multicenter Allergy Study Group. 2001. The pattern of atopic sensitization is associated with the development of asthma in childhood. J. Allergy Clin. Immunol. 108: 709-714.
9. Akbari, O., J. L. Faul, E. G. Hoyte, G. J. Berry, J. Wahlström, M. Kronenberg, R. H. DeKruyff, and D. T. Umetsu. 2006. CD4+ invariant T-cell-receptor+ natural killer T cells in bronchial asthma. N. Engl. J. Med. 354: 1117-1129.
10. Akbari, O., P. Stock, E. Meyer, M. Kronenberg, S. Sidobre, T. Nakayama, M. Taniguchi, M. J. Grusby, R. H. DeKruyff, and D. T. Umetsu. 2003. Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 9: 582-588.
11. Lisbonne, M., S. Diem, A. de Castro Keller, J. Lefort, L. M. Araujo, P. Hachem, J. M. Fourneau, S. Sidobre, M. Kronenberg, M. Taniguchi, et al. 2003. Cutting edge: invariant V alpha 14 NKT cells are required for allergen-induced airway inflammation and hyperreactivity in an experimental asthma model. J. Immunol. 171: 1637-1641. (Pubitemid 36966444)
12. Sen, Y., B. Yongyi, H. Yuling, X. Luokun, H. Li, X. Jie, D. Tao, Z. Gang, L. Junyan, H. Chunsong, et al. 2005. V alpha 24-invariant NKT cells from patients with allergic asthma express CCR9 at high frequency and induce Th2 bias of CD3+ T cells upon CD226 engagement. J. Immunol. 175: 4914-4926. (Pubitemid 41456373)
13. Matangkasombut, P., G. Marigowda, A. Ervine, L. Idris, M. Pichavant, H. Y. Kim, T. Yasumi, S. B. Wilson, R. H. DeKruyff, J. L. Faul, et al. 2009. Natural killer T cells in the lungs of patients with asthma. J. Allergy Clin. Immunol. 123: 1181-1185.
14. Reynolds, C., J. Barkans, P. Clark, H. Kariyawasam, D. Altmann, B. Kay, and R. Boyton. 2009. Natural killer T cells in bronchial biopsies from human allergen challenge model of allergic asthma. J. Allergy Clin. Immunol. 124: 860-862, author reply 862.
15. Kronenberg, M., and L. Gapin. 2002. The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2: 557-568.
16. Cui, J., N. Watanabe, T. Kawano, M. Yamashita, T. Kamata, C. Shimizu, M. Kimura, E. Shimizu, J. Koike, H. Koseki, et al. 1999. Inhibition of T helper cell type 2 cell differentiation and immunoglobulin E response by ligand-activated Valpha14 natural killer T cells. J. Exp. Med. 190: 783-792.
17. Wilson, S. B., S. C. Kent, K. T. Patton, T. Orban, R. A. Jackson, M. Exley, S. Porcelli, D. A. Schatz, M. A. Atkinson, S. P. Balk, et al. 1998. Extreme Th1 bias of invariant Valpha24JalphaQ T cells in type 1 diabetes. Nature 391: 177-181.
18. Brigl, M., and M. B. Brenner. 2004. CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22: 817-890.
19. Cui, J., T. Shin, T. Kawano, H. Sato, E. Kondo, I. Toura, Y. Kaneko, H. Koseki, M. Kanno, and M. Taniguchi. 1997. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278: 1623-1626.
20. Naidenko, O. V., J. K. Maher, W. A. Ernst, T. Sakai, R. L. Modlin, and M. Kronenberg. 1999. Binding and antigen presentation of ceramide-containing glycolipids by soluble mouse and human CD1d molecules. J. Exp. Med. 190: 1069-1080.
21. Nieuwenhuis, E. E., S. Gillessen, R. J. Scheper, M. A. Exley, M. Taniguchi, S. P. Balk, J. L. Strominger, G. Dranoff, R. S. Blumberg, and S. B. Wilson. 2005. CD1d and CD1d-restricted iNKT-cells play a pivotal role in contact hypersensitivity. Exp. Dermatol. 14: 250-258.
22. Russano, A. M., E. Agea, L. Corazzi, A. D. Postle, G. De Libero, S. Porcelli, F. M. de Benedictis, and F. Spinozzi. 2006. Recognition of pollen-derived phosphatidyl-ethanolamine by human CD1d-restricted gamma delta T cells. J. Allergy Clin. Immunol. 117: 1178-1184.
23. Gregoriadis, G. 1995. Engineering liposomes for drug delivery: progress and problems. Trends Biotechnol. 13: 527-537.
24. Kamps, J. A., and G. L. Scherphof. 2004. Biodistribution and uptake of liposomes in vivo. Methods Enzymol. 387: 257-266.
25. Vo-Hoang, Y., L. Micouin, C. Ronet, G. Gachelin, and M. Bonin. 2003. Total enantioselective synthesis and in vivo biological evaluation of a novel fluorescent BODIPY alpha-galactosylceramide. ChemBioChem 4: 27-33.
26. Arreaza, G. A., M. J. Cameron, A. Jaramillo, B. M. Gill, D. Hardy, K. B. Laupland, M. J. Rapoport, P. Zucker, S. Chakrabarti, S. W. Chensue, et al. 1997. Neonatal activation of CD28 signaling overcomes T cell anergy and prevents autoimmune diabetes by an IL-4-dependent mechanism. J. Clin. Invest. 100: 2243-2253.
27. Molling, J. W., M. Moreno, H. J. van der Vliet, B. M. von Blomberg, A. J. van den Eertwegh, R. J. Scheper, and H. J. Bontkes. 2007. Generation and sustained expansion of mouse spleen invariant NKT cell lines with preserved cytokine releasing capacity. J. Immunol. Methods 322: 70-81.
28. Sidobre, S., and M. Kronenberg. 2002. CD1 tetramers: a powerful tool for the analysis of glycolipid-reactive T cells. J. Immunol. Methods 268: 107-121. (Pubitemid 35223112)
29. Yu, K. O., J. S. Im, P. A. Illarionov, R. M. Ndonye, A. R. Howell, G. S. Besra, and S. A. Porcelli. 2007. Production and characterization of monoclonal antibodies against complexes of the NKT cell ligand alpha-galactosylceramide bound to mouse CD1d. J. Immunol. Methods 323: 11-23.
30. Martin,T.R., N. P. Gerard, S. J. Galli, and J. M. Drazen. 1988. Pulmonary responses to bronchoconstrictor agonists in the mouse. J. Appl. Physiol. 64: 2318-2323.
31. Meyer, E. H., S. Goya, O. Akbari, G. J. Berry, P. B. Savage, M. Kronenberg, T. Nakayama, R. H. DeKruyff, and D. T. Umetsu. 2006. Glycolipid activation of invariant T cell receptor+ NK T cells is sufficient to induce airway hyperreactivity independent of conventional CD4+ T cells. Proc. Natl. Acad. Sci. U.S.A. 103: 2782-2787.
32. Stefanová, I., B. Hemmer, M. Vergelli, R. Martin, W. E. Biddison, and R. N. Germain. 2003. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 4: 248-254.
33. Akbari, O., R. H. DeKruyff, and D. T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2: 725-731.
34. Kim, J.-O., D.-H. Kim,W.-S. Chang, C. Hong, S.-H. Park, S. Kim, and C.-Y. Kang. 2004. Asthma is induced by intranasal coadministration of allergen and natural killer T-cell ligand in a mouse model. J. Allergy Clin. Immunol. 114: 1332-1338.
35. Rauch, J., J. Gumperz, C. Robinson, M. Sköld, C. Roy, D. C. Young, M. Lafleur, D. B. Moody, M. B. Brenner, C. E. Costello, and S. M. Behar. 2003. Structural features of the acyl chain determine self-phospholipid antigen recognition by a CD1d-restricted invariant NKT (iNKT) cell. J. Biol. Chem. 278: 47508-47515.
36. Akbari, O., P. Stock, A. K. Singh, V. Lombardi, W. L. Lee, G. J. Freeman, A. H. Sharpe, D. T. Umetsu, and R. H. Dekruyff. 2009. PD-L1 and PD-L2 modulate airway inflammation and iNKT-cell-dependent airway hyperreactivity in opposing directions. Mucosal. Immunol. (Epub ahead of print)
37. Terashima, A.,H.Watarai, S. Inoue, E. Sekine, R. Nakagawa, K. Hase, C. Iwamura, H. Nakajima, T. Nakayama, and M. Taniguchi. 2008. A novel subset of mouse NKT cells bearing the IL-17 receptor B responds to IL-25 and contributes to airway hyperreactivity. J. Exp. Med. 205: 2727-2733.
38. Stock, P., V. Lombardi, V. Kohlrautz, and O. Akbari. 2009. Induction of airway hyperreactivity by IL-25 is dependent on a subset of invariant NKT cells expressing IL-17RB. J. Immunol. 182: 5116-5122.
39. Kim, E. Y., J. T. Battaile, A. C. Patel, Y. You, E. Agapov, M. H. Grayson, L. A. Benoit, D. E. Byers, Y. Alevy, J. Tucker, et al. 2008. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14: 633-640.
40. Hamzaoui, A., S. Cheik Rouhou, H. Graïri, H. Abid, J. Ammar, H. Chelbi, and K. Hamzaoui. 2006. NKT cells in the induced sputum of severe asthmatics. Mediators Inflamm. 2006: 71214.
41. Yamamoto, H., Y. Okamoto, S. Horiguchi, N. Kunii, S. Yonekura, and T. Nakayama. 2007. Detection of natural killer T cells in the sinus mucosa from asthmatics with chronic sinusitis. Allergy 62: 1451-1455.
42. Jin, N., N. Miyahara, C. L. Roark, J. D. French, M. K. Aydintug, J. L. Matsuda, L. Gapin, R. L. O'Brien, E. W. Gelfand, and W. K. Born. 2007. Airway hyper-responsiveness through synergy of gammadelta T cells and NKT cells. J. Immunol. 179: 2961-2968.
43. Pichavant, M., S. Goya, E. H. Meyer, R. A. Johnston, H. Y. Kim, P. Matangkasombut, M. Zhu, Y. Iwakura, P. B. Savage, R. H. DeKruyff, et al. 2008. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J. Exp. Med. 205: 385-393.
44. Matangkasombut, P., M. Pichavant, T. Yasumi, C. Hendricks, P. B. Savage, R. H. Dekruyff, and D. T. Umetsu. 2008. Direct activation of natural killer T cells induces airway hyperreactivity in nonhuman primates. J. Allergy Clin. Immunol. 121: 1287-1289.
45. Fang, L., B. Adkins, V. Deyev, and E. R. Podack. 2008. Essential role of TNF receptor superfamily 25 (TNFRSF25) in the development of allergic lung inflammation. J. Exp. Med. 205: 1037-1048.
46. Kim, H. Y., M. Pichavant, P. Matangkasombut, Y. I. Koh, P. B. Savage, R. H. DeKruyff, and D. T. Umetsu. 2009. The development of airway hyperreactivity in T-bet-deficient mice requires CD1d-restricted NKT cells. J. Immunol. 182: 3252-3261.
47. Sloan-Lancaster, J., A. S. Shaw, J. B. Rothbard, and P. M. Allen. 1994. Partial T cell signaling: altered phospho-zeta and lack of zap70 recruitment in APLinduced T cell anergy. Cell 79: 913-922.
48. Dittel, B. N., I. Stefanova, R. N. Germain, and C. A. Janeway, Jr. 1999. Cross-antagonism of a T cell clone expressing two distinct T cell receptors. Immunity 11: 289-298.
49. Kersh, E. N., G. J. Kersh, and P. M. Allen. 1999. Partially phosphorylated T cell receptor zeta molecules can inhibit T cell activation. J. Exp. Med. 190: 1627-1636.
50. Steinke, J. W., and J. A. Culp. 2007. Leukotriene synthesis inhibitors versus antagonists: the pros and cons. Curr. Allergy Asthma Rep. 7: 126-133.
51. Valitutti, S., and A. Lanzavecchia. 1997. Serial triggering of TCRs: a basis for the sensitivity and specificity of antigen recognition. Immunol. Today 18: 299-304.
52. Stotz, S. H., L. Bolliger, F. R. Carbone, and E. Palmer. 1999. T cell receptor (TCR) antagonism without a negative signal: evidence from T cell hybridomas expressing two independent TCRs. J. Exp. Med. 189: 253-264.
53. Agea, E., A. Russano, O. Bistoni, R. Mannucci, I. Nicoletti, L. Corazzi, A. D. Postle, G. De Libero, S. A. Porcelli, and F. Spinozzi. 2005. Human CD1-restricted T cell recognition of lipids from pollens. J. Exp. Med. 202: 295-308.
54. Tsitoura, D. C., R. H. DeKruyff, J. R. Lamb, and D. T. Umetsu. 1999. Intranasal exposure to protein antigen induces immunological tolerance mediated by functionally disabled CD4+ T cells. J. Immunol. 163: 2592-2600.