Signal transducer and activator of transcription 6 controls chemokine production and T helper cell type 2 cell trafficking in allergic pulmonary inflammation

Journal of Experimental Medicine

Volumn 193, Issue 9, 2001, Pages 1087-1096

  Mathew, Anuja ^a   MacLean, James A ^a   DeHaan, Elliot ^a   Tager, Andrew M ^a   Green, Francis H Y ^b   Luster, Andrew D ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Asthma; Cytokines; Eosinophil; Knockout mouse; Transcription factor

Indexed keywords

CHEMOKINE; STAT6 PROTEIN;

ALLERGIC PNEUMONITIS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; ASTHMA; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; EOSINOPHILIA; KNOCKOUT MOUSE; LYMPHOCYTE DIFFERENTIATION; MOUSE; MUCUS; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TH2 CELL;

ANIMALS; ANTIGENS; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOKINES; CYTOKINES; EOSINOPHILS; GENE EXPRESSION PROFILING; GOBLET CELLS; LUNG; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; MUCUS; OVALBUMIN; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR; TH2 CELLS; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS;

EID: 0035821221     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.193.9.1087     Document Type: Article

References (47)

1. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17:255-281.
2. Del Prete, G.F., M. De Carli, M.M. D'Elios, P. Maestrelli, M. Ricci, L. Fabbri, and S. Romagnani. 1993. Allergen exposure induces the activation of allergen-specific Th2 cells in the airway mucosa of patients with allergic respiratory disorders. Eur. J. Immunol. 23:1445-1449.
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. Eng. J. Med. 326: 298-304.
4. Walker, C., E. Bode, L. Boer, T. Hansel, K. Blaser, and C. Virchow, Jr. 1992. Allergic and nonallergic asthmatics have distinct patterns of T-cell activation and cytokine production in peripheral blood and bronchoalveolar lavage. Am. Rev. Respir. Dis. 146:109-115.
5. Bruselle, G.J., G. Kips, G. Bluethmann, and R. Pauwels. 1995. Allergen-induced airway inflammation and bronchial responsiveness in wildtype and IL-4 deficient mice. Am. J. Respir. Cell Biol. 12:254-259.
6. Foster, P.S., S.P. Hogan, A.J. Ramsay, K.I. Matthaei, and I.G. Young. 1996. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J. Exp. Med. 183:195-201.
7. Grunig, 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.
8. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T.Y. Neben, C.L. Karp, and D. Donaldson. 1998. IL-13: a central mediator of allergic asthma. Science. 282:2258-2251.
9. Cohn, L., R.J. Homer, A. Marinov, J. Rankin, and K. Bottomly. 1997. Induction of airway mucus production by T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J. Exp. Med. 186:1737-1747.
10. Li, L., Y. Xia, A. Nguyen, L. Feng, and D. Lo. 1998. Th2-induced eotaxin expression and eosinophilia coexist with Th1 responses at the effector stage of lung inflammation. J. Immunol. 161:3128-3135.
11. Li, X., B.H. Schofield, Q. Wang, K. Kim, and S. Huang. 1998. Induction of pulmonary allergic responses by antigen-specific Th2 cells. J. Immunol. 160:1378-1384.
12. Wurster, A.L., T. Tanaka, and M.J. Grusby. 2000. The biology of Stat4 and Stat6. Oncogene. 19:2577-2584.
13. Kaplan, M.H., U. Schindler, S.T. Smiley, and M.J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity. 4:313-319.
14. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, N. Kashiwamura, N. Nakanishi, T. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signaling. Nature, 380:627-630.
15. Leonard, W.J., and J.J. O'Shea. 1998. JAKS and STATs: biological implications. Annu. Rev. Immunol. 16:293-322.
16. Akimoto, T., F. Numata, M. Tamura, Y. Takata, N. Higashida, T. Takashi, K. Takeda, and S. Akira. 1998. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187:1537-1542.
17. Kuperman, D.B., M. Schofield, M. Wills-Karp, and M. Grusby. 1998. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J. Exp. Med. 187:939-948.
18. Tomkinson, A., A. Kanehiro, N. Rabinovitch, A. Joetham, G. Cieslewicz, and E. W. Gelfand. 1999. The failure of STAT6-deficient mice to develop airway eosinophilia and airway hyperresponsiveness is overcome by interleukin-5. Am. J. Respir. Crit. Care Med. 160:1283-1291.
19. MacLean, J.A., R. Ownbey, and A.D. Luster. 1996. T cell-dependent regulation of eotaxin in antigen-induced pulmonary eosinopbilia. J. Exp. Med. 184:1461-1469.
20. Heath, H., S. Qin, P. Rao, L. Wu, G. LaRosa, N. Kassam, P.D. Ponath, and C.R. Mackay, 1997. Chemokine receptor usage by human eosinophils: the importance of CCR3 demonstrated using an antagonistic monoclonal antibody. J. Clin. Invest. 99:178-184.
21. Sallusto, F., A. Lanzavecchia, and C.R. Mackay. 1998. Chemokines and chemokine receptors in T-cell priming and Th1/Th2-inediated responses. Immunol. Today. 19:568-574.
22. Zhang, S., N.W. Lukacs, V.A. Lawless, S.L. Kunkel, and M.H. Kaplan. 2000. Cutting edge: differential expression of chemokines in Th1 and Th2 cells is dependent on Stat6 but not Stat4. J. Immunol. 165:10-14.
23. Wilson, S.D., P.R. Burd, P.R. Billings, C.A. Martin, and M. Dorf. 1988. The expression and regulation of a potential lymphokine gene (TCA3) in CD4 and CD8 T cell clones. J. Immunol. 141:1563-1570.
24. Gleich, G.J. 1990. The eosinophil and bronchial asthma: current understanding. J. Allergy Clin. Immunol. 85:422-136.
25. Weller, P.F. 1991. The immunobiology of eosinophils. N. Engl. J. Med. 324:1110-1118.
26. Sanderson, C.J. 1992. Interleukin-5, eosinophils. and disease. Blood. 79:3101-3109.
27. Temann, U.A., B. Prasad, M.W. Gallup, C. Basbaum, S.B. Ho, R.A. Flavell, and J.A. Rankin. 1997. A novel role for murine IL-4 in vivo: induction of MUC5AC gene expression and mucin hypersecretion. Am. J. Respir. Cell Mol. Biol. 16:471-478.
28. McInnes, A., and D.M. Rennick. 1988. Interleukin-4 induces cultured monocytes/macrophages to form multinucleated giant cells. J. Exp. Med. 167:598-611.
29. Zhu, Z., R.J. Homer, Z. Wang, Q. Chen, G.P. Geba, J. Wang, Y. Zhang, and J.A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103:779-788.
30. Lee, J.L., M.P. McGarry, S.C. Farmer, K.L. Denzler, K.A. Larson, P.E. Carrigan, I.E. Brenneise, M.A. Horton, A. Haczku, E.W. Gelfand, et al. 1997. IL-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J. Exp. Med. 185:2143-2156.
31. D'Ambrosio, D., A. Iellem, L. Colantonio, B. Clissi, R. Pardi, and F. Sinigagha. 2000. Localization of Th-cell subsets in inflammation: differential thresholds for extravasation of Th1 and Th2 cells. Immunol. Today. 21:183-186.
32. Austrup, F., D. Vestweber, E. Borges, M. Lohning, R. Brauer, U. Herz, H. Renz, R. Hallmann, A. Scheffold, A. Radbruch, and A. Hamann. 1997. P-and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflamed tissues. Nature. 385:81-83.
33. Borges, E., W. Tietz, M. Steegmaier, T. Moll, R. Hallmann, A. Hamann, and D. Vestweber. 1997. P-selectin glycoprotein ligand-1 (PSGL-1) on T helper 1 but not on T helper 2 cells binds to P-selectin and supports migration into inflamed skin. J. Exp. Med. 185:573-578.
34. - T cells. J. Exp. Med. 189: 1765-1776.
35. Palmer-Crocker, R.L., C.C.W. Hughes, and J.S. Pober, 1996. IL-4 and IL-13 activate JAK2 tyrosine and Stat6 in cultured human vascular endothelial cells through a common pathway that does not involve the γ-c chain. J. Clin. Invest. 98:604-609.
36. Chvatchko, Y., A.J. Hoogewerf, A. Meyer, S. Alouani, P. Juillard, R. Buser, F. Conquet, A.E. Proudfoot, T.N. Wells, and C.A. Power. 2000. A key role for CC chemokine receptor 4 in lipopolysaccharide-induced endotoxic shock. J. Exp. Med. 191:1755-1764.
37. Gonzalo, J.A., Y. Pan, C.M. Lloyd, G.Q. Jia, G. Yu, B. Dussault, C.A. Powers, A.E. Proudfoot, A.J. Coyle, D. Gearing, and J.C. Gutierrez-Ramos. 1999. Mouse monocyte-derived chemokine is involved in airway hyperreactivity and lung inflammation. J. Immunol. 163:403-411.
38. Lloyd, C.M., T. Delaney, T. Nguyen, J. Tian, A.C. Martinez, A.J. Coyle, and J.C. Gutierrez-Ramos. 2000. CC chemokine receptor (CCR)3/eotaxin is followed by CCR4/ monocyte-derived chemokine in mediating pulmonary T helper lymphocyte type 2 recruitment arter serial antigen challenge in vivo. J. Exp. Med. 191:265-274.
39. Rothenberg, M.E., J.A. MacLean, E. Pearlman, A.D. Luster, and P. Leder. 1997. Targeted disruption of the chemokine eotaxin only partially reduces antigen induced tissue eosinophilia. J. Exp. Med. 185:785-790.
40. Garcia-Zepeda, E.A., M.E. Rothenberg, R.T. Ownbey, J. Celestin, P. Leder, and A.D. Luster. 1996. Human eotaxin is specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat. Med. 4:449-456.
41. Mochizuki, M., J. Bartels, A.I. Mallet, E. Christophers, and J.M. Schroder. 1998. IL-4 induces eotaxin: a possible mechanism of selective eosinophil recruitment in helminth infection and atopy. J. Immunol. 160:60-68.
42. Stellato, C., S. Matsukura, A. Fal, J. White, L.A. Beck, D. Proud, and R.P. Schleimer. 1999. Differential regulation of epithelial-derived C-C cheinokine expression by IL-4 and the glucocorticoid budesonide. J. Immunol. 163:5624-5632.
43. Li, L., Y. Xia, A. Nguyen, Y.H. Lai, L. Feng, T.R. Mosmann, and D. Lo. 1999. Effects of Th2 cytokines on chemokine expression in the lung: IL-13 induces eotaxin expression by airway epithelial cells. J. Immunol. 162:2477-2487.
44. Shinkai, A., H. Yoshsue, M. Koike, E. Shoji, S. Nakagawa, A. Saito, T. Takeda, S. Imabeppu, Y. Kato, H. Nobuo, et al. 1999. A novel human CC chemokine eotaxin-3, which is expressed in IL-4 stimulated vascular endothelial cells, exhibits potent activity toward eosinophils. J Immunol. 163:1602-1610.
45. Zimmermann, N., S.P. Hogan, A. Mishra, E. Brandt, T.R. Bodette, S.M. Pope, F. Finkelman, and M.E. Rothenberg. 2000. Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J. Immunol. 165:5839-5846.
46. Matsukura, S., C. Stellato, J.R. Plitt, C. Bickel, K. Miura, S.N. Georas, V. Casolaro, and R.P. Schleimer. 1999. Activation of eotaxin gene transcription by NF-κB and STAT6 in human airway epithelial cells. J. Immunol. 163:6876-6883.
47. Sekiya, T., M. Miyamasu, M. Imanishi, H. Yamada, T. Nakajima, M. Yamaguchi, T. Fujisawa, R. Pawankar, Y. Sano, K. Ohta, et al. 2000. Inducible expression of a Th2-type CC chemokine thymus-and activation-regulated chemokine by human bronchial epithelial cells. J. Immunol. 165:2205-2213.