Induction of airway mucus production by T helper 2 (Th2) cells: A critical role for interleukin 4 in cell recruitment but not mucus production

Journal of Experimental Medicine

Volumn 186, Issue 10, 1997, Pages 1737-1747

  Cohn, Lauren ^a   Homer, Robert J ^a,b   Marinov, Anthony ^a   Rankin, John ^b   Bottomly, Kim ^a,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Vet Admin Coop Studies Group   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 10; RECOMBINANT INTERLEUKIN 4; RECOMBINANT INTERLEUKIN 5; T LYMPHOCYTE RECEPTOR;

AIRWAY OBSTRUCTION; ANIMAL CELL; ANIMAL MODEL; ARTICLE; ASTHMA; BRONCHUS BIOPSY; BRONCHUS HYPERREACTIVITY; BRONCHUS MUCUS; CONTROLLED STUDY; HELPER CELL; INFLAMMATORY DISEASE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION;

ADOPTIVE TRANSFER; ANIMALS; BRONCHI; CELL MOVEMENT; EPITOPES; INFLAMMATION; INTERLEUKIN-4; LUNG; LYMPHOCYTE ACTIVATION; LYMPHOCYTE TRANSFUSION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; MUCUS; OVALBUMIN; STAINING AND LABELING; TH2 CELLS;

EID: 0030689729     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.10.1737     Document Type: Article

References (53)

1. James, A., and N. Carroll. 1995. Theoretical effects of mucus gland discharge on airway resistance in asthma. Chest. 107: 110S.
2. Moreno, R.H., J.C. Hogg, and P.D. Pare. 1986. Mechanics of airway narrowing. Am. Rev. Respir. Dis. 133:1171-1180.
3. Tanizaki, Y., H. Kitani, M. Okazaki, T. Mifune, F. Mitsunobu, and I. Kimura. 1993. Mucus hypersecretion and eosiophils in bronchoalveolar lavage fluid in adult patients with bronchial asthma. J. Asthma. 30:257-262.
4. Fahy, J.V., D.J. Steiger, J. Liu, C.B. Basbaum, W.E. Finkbeiner, and H.A. Boushey. 1993. Markers of mucus secretion and DNA levels in induced sputum from asthmatics and from healthy subjects. Am. Rev. Respir. Dis. 147:1132-1137.
5. Lundgren, J.D., R.T. Davey, B. Lundgren, J. Mullol, Z. Marom, C. Logun, J. Baraniuk, M.A. Kaliner, and J.H. Shelhamer. 1991. Eosinphil cationic protein stimulates and major basic protein inhibits airway mucus secretion. J. Allergy Clin. Immunol. 87:689-698.
6. Wanner, A., M. Salathe, and T. O'Riordan. 1996. Mucociliary clearance in the airways. Am. J. Respir. Crit. Care Med. 154:1868-1902.
7. Temann, U.A., B.G. Prasad, M.W., 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.
8. Lee, J.J., 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. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J. Exp. Med. 185:2143-2156.
9. 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.
10. Wilson, J.W., R. Djukanovic, P.H. Howarth, and S.T. Holgate. 1992. Lymphocyte activation in bronchoalveolar lavage and peripheral blood in atopic asthma. Am. Rev. Respir. Dis. 145:958-960.
11. Bentley, A.M., Q. Meng, D.S. Robinson, Q. Hamid, A.B. Kay, and S.R. Durham. 1993. Increases in activated T lymphocytes, eosinophils, and cytokine mRNA expression for interleukin-5 and granulocyte/macrophage colony-stimulating factor in bronchial biopsies after allergen inhalation challenge in atopic asthmatics. Am. J. Respir. Cell Mol. Biol. 8:35-42.
12. Olivenstein, R., P.M. Renzi, L.J. Xu, J.P. Yang, and J.G. Martin. 1994. Effects of W3/25 monoclonal antibody on pulmonary inflammation and the late airway response in Brown-Norway rats. Am. Rec. Respir. Dis. 149:528a. (Abstr.).
13. Nakajima, H., I. Iwamoto, S. Tomoe, R. Matsumara, H. Tomioka, K. Takatsu, and S. Yoshida. 1992. CD4+ T-lymphocytes and interleukin-5 mediate antigen-induced eosinophil infiltration into mouse trachea. Am. Rev. Respir Dis. 146: 374-377.
14. Cher, D., and T. Mosmann. 1987. Two types of murine helper T cell clone: II. Delayed type hypersensitivity is mediated by Th1 clones. J. Immunol. 138:3688-3694.
15. Stout, R., and K. Bottomly. 1989. Antigen-specific activation of effector macrophages by IFN-γ producing (Th1) T cell clones. Failure of IL4 producing (Th2) T cell clones to activate effector function in macrophages. J. Immunol. 142: 760-765.
16. Kim, J., A. Woods, E. Becker-Dunn, and K. Bottomly. 1985. Distinct functional phenotypes of cloned Ia-restricted helper T cells. J. Exp. Med. 162:188-201.
17. Killar, L., G. MacDonald, J. West, A. Woods, and K. Bottomly. 1987. Cloned Ia restricted T cells that do not produce IL4/BSF-1 fail to help antigen specific B cells. J. Immunol. 138:1674-1679.
18. Mosmann, T.R., H. Cherwinski, M.W. Bond, M.A. Giedlin, and R.L. Coffman. 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136:2348-2357.
19. Kuhn, R., K. Rajewsky, and W. Muller. 1991. Generation and analysis of IL4 deficient mice. Science (Wash. DC). 254: 707-710.
20. Finkelman, F.D., I.M. Katona, J.F. Urban, C.M. Snapper, Jr., J. Ohara, and P. W.E. 1986. Suppression of in vivo polyclonal IgE responses by monoclonal antibody to the lymphokine B cell stimulatory factor 1. Proc. Natl. Acad. Sci. USA. 83:9675-9683.
21. Stevens, T.L., A. Bossie, V.M. Sanders, R. Fernandez-Botran, R. Coffman, T.R. Mosmann, and E. Vitetta. 1988. Regulation of antibody isotypic secretion by subsets of antigen-specific helper T cells. Nature (Lond.). 334:255-258.
22. Resnick, M.B., and P.F. Weller. 1993. Mechanisms of eosinophil recruitment. Am. J. Respir. Cell Mol. Biol. 8:349-355.
23. Hamid, Q., M. Azzawi, S. Ying, R. Moqbel, A.J. Wardlaw, C.J. Corrigan, B. Bradley, S.R. Durham, J.V. Collins, P.K. Jeffery et al. 1991. Expression of mRNA for interleukin-5 in mucosal bronchial biopsies from asthma. J. Clin. Invent 87: 1541-1546.
24. Bradley, B.L., M. Azzawi, M. Jacobson, B. Assoufi, J.V. Collins, A.M. Irani, L.B. Schwartz, S.R. Durham, P.K. Jeffery, and A.B. Kay. 1991. Eosinophils, T-lymphocytes, mast cells, neutrophils, and macrophages in bronchial biopsy specimens from atopic subjects with asthma: comparison with biopsy specimens from atopic subjects without asthma and normal control subjects and relationship to bronchial hyperresponsiveness. J. Allergy Clin. Immunol. 88:661-674.
25. Poulter, L.W., C. Power, and C. Burke. 1990. The relationship between bronchial immunopathology and hyperresponsiveness in asthma. Eur. Respir. Journal. 3:792-799.
26. Calhoun, W.J., K.L. Hinton, and R.E. Friedenheim. 1995. Evidence for simultaneous Th1 and Th2 lymphocyte activation in allergic asthma following segmental antigen challenge. Am. J. Respir. Crit. Care Med. 151:778a.(Abstr.).
27. Cembrzynska-Nowak, M., E. Szklarz, A.D. Inglot, and J.A. Teodorczyk-Injeyan. 1993. Elevated release of tumor necrosis factor-alpha and interferon-gamma by bronchoalveolar leukocytes from patients with bronchial asthma. Am. Rev. Respir. Dis. 147:291-295.
28. Corrigan, C.J., and A.B. Kay. 1990. CD4 T-lymphocyte activation in acute severe asthma. Relationship to disease severity and atopic status. Am. Rev. Respir. Dis. 141:970-977.
29. Krug, N., J. Madden, A.E. Redington, P. Lackie, R. Dhukanovic, U. Schauer, S.T. Holgate, A.J. Frew, and P.H. Howarth. 1996. T cell cytokine profile evaluated at the single cells level in BAL and blood in allergic asthma. Am. J. Respir. Cell Mol. Biol. 14:319-326.
30. Murphy, K.M., A.B. Heimberger, and D.Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+ CD8+ TCR lo thymocytes in vivo. Science (Wash. DC). 250: 1720-1723.
31. + T lymphocytes to peptide antigen in vivo. J Immunol. 151: 6742-6750.
32. Ledbetter, J.A., and L.A. Herzenberg. 1979. Xenogenic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol. Rev. 47:63-90.
33. Landais, D., B.N. Beck, J.-M. Buerstedde, S. Degraw, D. Klein, N. Koch, D. Murphy, M. Pierres, T. Tada, K. Yamamoto et al. 1987. The assignment of chain specificities for anti-Ia monoclonal antibodies using L cell transfectants. J. Immunol. 137:3002-3005.
34. Dialynas, D.P., D.B. Wilde, P. Marrack, A. Pierres, K.A. Wall, W. Havran, G. Otten, M.R. Loken, M. Pierres, J. Kappler, and F.W. Fitch. 1983. Characterization of the murine antigenic determinant, L3T4a, recognized by a monoclonal antibody GK1.5: Expression of L3T4a by functional T cell clones appears to correlate primarily with Class II MHC antigen-reactivity. Immunol. Rev. 74:29-56.
35. Jones, B. 1983. Evidence that the Thy-1 molecule is a target for T cell mitogenic antibody against brain-associated antigens. Eur. J. Immunol. 13:678-684.
36. Ohara, J., and W.E. Paul. 1985. Production of a monoclonal antibody to and molecular characterization of B-cell stimulatory factor-1. Nature (Lond.). 315:333-336.
37. Cherwinski, H.M., J.H. Schumacher, K.D. Brown, and T.R. Mosmann. 1987. Two types of mouse helper T cell clone: III Further differences in lymphokine synthesis between Th1 and Th2 clones revealed by RNA hybridization, functionally monospecific bioassays, and monoclonal antibodies. J. Exp. Med. 166:1229-1244.
38. Marrack, P., R. Shimonkevitz, C. Hannum, K. Haskins, and J. Kappler. 1983. The major histocompatibility complex-restricted antigen receptor on T cells. J. Exp. Med. 158:1635-1646.
39. Wong, S., S. Guerder, I. Visintin, E. Reich, K.E. Swenson, R.A. Vlavell, and C.A. Janeway. 1995. Expression of the costimulator molecule B7-1 in pancreatic B-cells accelerates diabetes in the NOD mouse. Diabetes. 44:326-329.
40. Weibel, E.R. 1979. Sterologic Methods. Academic Press, London, pp. 9-159.
41. Swain, S.L. 1994. Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity. 1:543-552.
42. Rossi G.A., O. Sacco, B. Balbi, S. Oddera, T. Mattioni, S. Corte, C. Ravazzoni, and L. Allegra. 1990. Human ciliated bronchial epithelial cells: expression of the HLA-DR antigens and of the alpha gene, modulation of the HLA-DR antigens by gamma interferon and antigen presenting cell function in the MLR. Am. J. Respir. Cell Mol. Biol. 3:431-439.
43. Noben-Trauth, N., P. Kropf, and I. Muller. 1996. Susceptibility to Leishmania major infection in interleukin-4-deficient mice. Science (Wash. DC). 271:987-990.
44. Nakajima H., H. Sano, T. Nishimura, S. Yoshida, and I. Iwamoto. 1994. Role of VCAM-1/VLA-4 and ICAM-1 interactions in antigen-induced eosinophil and T cell recruitment into the tissue. J. Exp. Med. 179:1145-1154.
45. Neumann, B., T. Machleidt, A. Lifka, K. Pfeffer, V. Deitmar, T. W. Mak, B. Holzmann, and M. Kronke. 1996. Crucial role of 55-kilodalton TNF receptor in TNF-induced adhesion molecule expression and leukocyte organ infiltration. J. Immunol. 156:1587-1593.
46. Murphy E., K. Shibuya, N. Hosken, P. Openshaw, V. Maino, K. Davis, K. Murphy, and A. O'Garra. 1996. Reversibility of T helper 1 and 2 populations is lost after long-term stimulation J. Immunol. 158:2648-2653.
47. Lundgren, J.D., and J.H. Shelhamer. 1990. Pathogenesis of airway mucus hypersecretion. J. Allergy Clin. Immunol. 85: 399-417.
48. Coyle, A.J., G. Le Gros, C. Bertrand, S. Tsuyuki, C.H. Heusser, M. Kopf, and G.P. Anderson. 1995. Interleukin-4 is required for the induction of lung Th2 mucosal immunity. Am. J. Respir. Cell Mol. Biol. 13:54-59.
49. Hogan, S.P., A. Mould, H. Kikutani, A.J. Ramsay, and P.S. Foster. 1997. Aeroallergen-induced eosinophilic inflammation, lung damage, and airways hyperreactivity in mice can occur independently of IL-4 and allergen-specific immunoglobulins. J. Clin. Invest. 99:1326-1339.
50. Gonzalo, J.A., C.M. Lloyd, L. Kremer, E. Finger, C. Martinez-A., M.H. Siegelman, M. Cybulsky, and J.C. Gutierrez-Ramos. 1996. Eosinophil recruitment to the lung in a murine model of allergic inflammation: the role of T cells, chemokines, and adhesion molecules. J. Clin. Invest. 98:2332-2345.
51. Lukacs, N.W., R.M. Streiter, K. Warmington, P. Lincoln, S.W. Chensue, and S.L. Kunkel. 1997. Differential recruitment of leukocyte populations and alteration of airway hyperreactivity by C-C family chemokines in allergic airway inflammation. J. Immunol. 158:4398-4404.
52. Budhecha, S., R.K. Albert, E. Chi, and D.B. Lewis. 1997. Kinetic relationship between IL-4 and muc5 gene expression with presence of airway mucus in a murine asthma model. Am. J. Respir Crit. Care Med. 155:756a. (Abstr.).
53. Henderson, W.R., D.B. Lewis, R.K. Albert, Y. Zhang, W.J.E. Lamm, G.K.S. Chiang, F. Jones, P. Eriksen, Y.T. Tien, M. Jonas, and E. Chi. 1996. The importance of leukotrienes in airway inflammation in a mouse model of asthma. J. Exp. Med. 184:1483-1494.