Inhibition of NF-κB activation reduces the tissue effects of transgenic IL-13

Journal of Immunology

Volumn 179, Issue 10, 2007, Pages 7030-7041

  Chapoval, Svetlana P ^a,c   Al Garawi, Amal ^b,d   Lora, Jose M ^b,e   Strickland, Ian ^a   Ma, Bing ^a   Lee, Patty J ^a   Homer, Robert J ^a   Ghosh, Sankar ^a   Coyle, Anthony J ^b,f   Elias, Jack A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MILLENNIUM PHARMACEUTICALS INC   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d MCMASTER UNIVERSITY   (Canada)

^e ROCHE BIOSCIENCE   (United States)

^f MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 CHLORO 8 NICOTINAMIDO BETA CARBOLINE; ADENOVIRUS VECTOR; ANTENNAPEDIA PROTEIN; CASPASE; I KAPPA B ALPHA; I KAPPA B KINASE GAMMA; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 13; PROTEIN P50; CELL SURFACE RECEPTOR; FUSED HETEROCYCLIC RINGS; I KAPPA B KINASE; IL4RA PROTEIN, MOUSE; INHIBITOR OF APOPTOSIS PROTEIN; NBD PEPTIDE, MOUSE; PEPTIDE; PYRIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVATION; GENE MUTATION; IMMUNOTHERAPY; LUNG ALVEOLUS; LUNG FIBROSIS; LUNG LAVAGE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PATHOGENESIS; PNEUMONIA; PRIORITY JOURNAL; TISSUE INJURY; TISSUE REACTION; TRANSGENIC MOUSE; WILD TYPE; ADENOVIRUS; ANIMAL; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; IMMUNOLOGY; INFLAMMATION; MOUSE MUTANT; MUCUS; PATHOLOGY; RESPIRATORY TRACT ALLERGY; SIGNAL TRANSDUCTION; TH2 CELL;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CASPASES; HETEROCYCLIC COMPOUNDS, 3-RING; I-KAPPA B KINASE; INFLAMMATION; INHIBITOR OF APOPTOSIS PROTEINS; INTERLEUKIN-13; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MUCUS; NF-KAPPA B P50 SUBUNIT; PEPTIDES; PULMONARY ALVEOLI; PULMONARY FIBROSIS; PYRIDINES; RECEPTORS, CELL SURFACE; RESPIRATORY HYPERSENSITIVITY; SIGNAL TRANSDUCTION; TH2 CELLS;

EID: 38449120549     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.10.7030     Document Type: Article

References (66)

1. 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.
2. Zhu, Z., B. Ma, R. J. Homer, T. Zheng, and J. A. Elias. 2001. Use of the tetracycline-controlled transcriptional silencer (tTS) to eliminate transgene leak in inducible overexpression transgenic mice. J. Biol. Chem. 276: 25222-25229.
3. Elias, J. A., T. C. G. Lee, R. J. Homer, Q. Chen, B. Ma, M. Blackburn, and Z. Zhu. 2003. Transgenic modeling of interleukin-13 in the lung. Chest 123: 339S-345S.
4. Herrick, C. A., and K. Bottomly. 2003. To respond or not to respond: T cells in allergic asthma. Nat. Rev. Immunol. 3: 405-412.
5. Zheng, T., Z. Zhu, Z. Wang, R. J. Homer, B. Ma, R. J. Riese, H. A. Chapman, S. D. Shapiro, and J. A. Elias. 2000. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J. Clin. Invest. 106: 1081-1093.
6. 1. J. Exp. Med. 194: 809-821.
7. Gelb, A. F., and N. Zamel. 2000. Unsuspected pseudophysiologic emphysema in chronic persistent asthma. Am. J. Respir. Crit. Care Med. 162: 1778-1782.
8. Belperio, J. A., M. Dy, M. D. Burdick, Y. Y. Xue, K. Li, J. A. Elias, and M. P. Keane. 2002. Interaction of IL-13 and C10 in the pathogenesis of bleomycin-induced pulmonary fibrosis. Am. J. Respir. Cell. Mol. Biol. 27: 419-427.
9. Smyth, L. J. C., C. Machado, A. P. Upton, S. Good, M. Aufderheide, and B. A. Helm. 2000. Assessment of the molecular basis of the proallergenic effects of cigarette smoke. Environ. Sci. Technol. 34: 1370-1374.
10. van der Pouw Kraan, T. C., M. Kucukaycan, A. M. Bakker, J. M. Baggen, J. S. van der Zee, M. A. Dentener, E. F. Wouters, and C. L. Verweij. 2002. Chronic obstructive pulmonary disease is associated with the -1055 IL-13 promoter polymorphism. Genes Immun. 3: 436-439.
11. Hegab, A. E., T. Sakamoto, W. Saitoh, H. H. Massoud, H. M. Massoud, K. Hassanein, and K. Sekizawa. 2004. Polymorphisms of IL4, IL13, and ADRB2 genes in COPD. Chest 126: 1832-1839.
12. Jakubzick, C., E. S. Choi, S. L. Kunkel, H. Evanoff, F. J. Martinez, R. K. Puri, K. R. Flaherty, G. B. Toews, T. V. Colby, E. A. Kazerooni, et al. 2004. Augmented pulmonary IL-4 and IL-13 receptor subunit expression in idiopathic interstitial pneumonia. J. Clin. Pathol. 57: 477-486.
13. Kuperman, D. A., X. Huang, L. L. Koth, G. H. Chang, G. M. Dolganov, Z. Zhu, J. A. Elias, D. Sheppard, and D. J. Erle. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8: 885-889.
14. Lee, J. H., N. Kaminski, G. Dolganov, G. Grunig, L. Koth, C. Solomon, D. J. Erle, and D. Sheppard. 2001. Interleukin-13 induces dramatically different transcriptional programs in three human airway cell types. Am. J. Respir. Cell. Mol. Biol. 5: 74-85.
15. Lee, P. J., X. Zhang, P. Shan, B. Ma, C. G. Lee, R. J. Homer, Z. Zhu, M. Rincon, B. T. Mossman, and J. A. Elias. 2006. ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling in vivo. J. Clin. Invest. 16: 163-173.
16. May, J. M., and S. Ghosh. 1998. Signal transduction through NF-κB. Immunol. Today 19: 80-88.
17. Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109: S81-S96.
18. Hart, L. A., V. L. Krishnan, I. M. Adcock, P. J. Barnes, and K. F. Chung. 1998. Activation and localization of transcription factor, nuclear factor-κB, in asthma. Am. J. Respir. Crit. Care Med. 158: 1585-1592.
19. Gagliardo, R., P. Chanez, M. Mathieu, A. Bruno, G. Costanzo, C. Gougat, I. Vachier, J. Bousquet, G. Bonsignore, and A. M. Vignola. 2003. Persistent activation of nuclear factor-κB signaling pathway in severe uncontrolled asthma. Am. J. Respir. Crit. Care Med. 168: 1190-1198.
20. Bureau, F., S. Delhalle, G. Bonizzi, L. Fievez, S. Dogne, N. Kirschvink, A. Vanderplasschen, M. P. Merville, V. Bours, and P. Lekeux. 2000. Mechanisms of persistent NF-κB activity in the bronchi of an animal model of asthma. J. Immunol. 165: 5822-5830.
21. Poynter, M. E., C. G. Irvin, and Y. M. Janssen-Heininger. 2002. Rapid activation of nuclear factor-κB in airway epithelium in a murine model of allergic airway inflammation. Am. J. Pathol. 160: 1325-1334.
22. Yang, L., L. Cohn, D. H. Zhang, R. Homer, A. Ray, and P. Ray. 1998. Essential role of nuclear factor κB in the induction of eosinophilia in allergic airway inflammation. J. Exp. Med. 188: 1739-1750.
23. Das, J., C. H. Chen, L. Yang, L. Cohn, P. Ray, and A. Ray. 2001. A critical role for NF-κB in GATA3 expression and TH2 differentiation in allergic airway inflammation. Nat. Immunol. 2: 45-50.
24. Choi, I. W., D. K. Kim, H. M. Ko, and H. K. Lee. 2004. Administration of antisense phosphorothioate oligonucleotide to the p65 subunit of NF-κB inhibits established asthmatic reaction in mice. Int. Immunopharmacol. 4: 1817-1828.
25. Desmet, C., P. Gosset, B. Pajak, D. Cataldo, M. Bentires-Alj, P. Lekeux, and F. Bureau. 2004. Selective blockade of NF-κB activity in airway immune cells inhibits the effector phase of experimental asthma. J. Immunol. 173: 5766-5775.
26. Huang, T. J., I. M. Adcock, and K. F. Chung. 2001. A novel transcription factor inhibitor, SP100030, inhibits cytokine gene expression, but not airway eosinophilia or hyperresponsiveness in sensitized and allergen-exposed rat. Br. J. Pharmacol. 134: 1029-1036.
27. Henderson, W. R., Jr., E. Y. Chi, J. L. Teo, C. Nguyen, and M. Kahn. 2002. A small molecule inhibitor of redox-regulated NF-κB and activator protein-1 transcription blocks allergic airway inflammation in a mouse asthma model. J. Immunol. 169: 5294-5299.
28. Poynter, M. E., R. Cloots, T. van Woerkom, K. J. Butnor, P. Vacek, D. J. Taatjes, C. G. Irvin, and Y. M. Janssen-Heininger. 2004. NF-κB activation in airways modulates allergic inflammation but not hyperresponsiveness. J. Immunol. 173: 7003-7009.
29. Di Stefano, A., G. Caramori, F. L. Ricciardolo, A. Capelli, I. M. Adcock, and C. F. Donner. 2004. Cellular and molecular mechanisms in chronic obstructive pulmonary disease: an overview. Clin. Exp. Allergy 34: 1156-1167.
30. Yoshida, M., T. R. Korfhagen, and J. A. Whitsett. 2001. Surfactant protein D regulates NF-κB and matrix metalloproteinase production in alveolar macrophages via oxidant-sensitive pathways. J. Immunol. 166: 7514-7519.
31. Hideshima, T., D. Chauhan, P. Richardson, C. Mitsiades, N. Mitsiades, T. Hayashi, N. Munshi, L. Dang, A. Castro, V. Palombella, et al. 2002. NF-κB as a therapeutic target in multiple myeloma. J. Biol. Chem. 277: 16639-16647.
32. Lam, L. T., R. E. Davis, J. Pierce, M. Hepperle, Y. Xu, M. Hottelet, Y. Nong, D. Wen, J. Adams, L. Dang, and L. M. Staudt. 2005. Small molecule inhibitors of IκB kinase are selectively toxic for subgroups of diffuse large B-cell lymphoma defined by gene expression profiling. Clin. Cancer Res. 11: 28-40.
33. Oitzinger, W., R. Hofer-Warbinek, J. A. Schmid, Y. Koshelnick, B. R. Binder, and R. de Martin. 2001. Adenovirus-mediated expression of a mutant IκB kinase 2 inhibits the response of endothelial cells to inflammatory stimuli. Blood 97: 1611-1617.
34. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science 278: 860-866.
35. May, M. J., F. D'Acquisto, L. A. Madge, J. Glockner, J. S. Pober, and S. Ghosh. 2000. Selective inhibition of NF-κB activation by a peptide that blocks the interaction of NEMO with the IκB kinase complex. Science 289: 1550-1554.
36. Tas, S. W., E. C. de Jong, N. Hajji, M. J. May, S. Ghosh, M. J. Vervoordeldonk, and P. P. Tak. 2005. Selective inhibition of NF-κB in dendritic cells by the NEMO-binding domain peptide blocks maturation and prevents T cell proliferation and polarization. Eur. J. Immunol. 35: 1164-1174.
37. di Meglio, P., A. Ianaro, and S. Ghosh. 2005. Amelioration of acute inflammation by systemic administration of a cell-permeable peptide inhibitor of NF-κB activation. Arthritis Rheum. 52: 951-958.
38. Lora, J. M., D. M. Zhang, S. M. Liao, T. Burwell, A. M. King, P. A. Barker, L. Singh, M. Keaveney, J. Morgenstern, J. C. Gutierrez-Ramos, et al. 2005. Tumor necrosis factor-α triggers mucus production in airway epithelium through an IκB kinase β-dependent mechanism. J. Biol. Chem. 280: 36510-36517.
39. Chapoval, S. P., G. H. Nabozny, E. V. Marietta, E. L. Raymond, C. J. Krco, A. G. Andrews, and C. S. David. 1999. Short ragweed allergen induces eosinophilic lung disease in HLA-DQ transgenic mice. J. Clin. Invest. 103: 1707-1717.
40. Phillips, R. J., and S. Ghosh. 1997. Regulation of IκBβ in WEHI 231 mature B cells. Mol. Cell. Biol. 17: 4390-4396.
41. Wang, J., R. J. Homer, L. Hong, L. Cohn, C. G. Lee, S. Jung, and J. A. Elias. 2000. IL-11 selectively inhibits aeroallergen-induced pulmonary eosinophilia and Th2 cytokine production. J. Immunol. 165: 2222-2231.
42. Lanone, S., T. Zheng, Z. Zhu, W. Liu, C. G. Lee, B. Ma, Q. Chen, R. J. Homer, J. Wang, L. A. Rabach, et al. 2002. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J. Clin. Invest. 110: 463-474.
43. Zheng, T., M. J. Kang, K. Crothers, Z. Zhu, W. Liu, C. G. Lee, L. A. Rabach, H. A. Chapman, R. J. Homer, D. Aldous, et al. 2005. Role of cathepsin S-dependent epithelial cell apoptosis in IFN-γ-induced alveolar remodeling and pulmonary emphysema. J. Immunol. 174: 8106-8115.
44. Elias, J. A. 2004. The relationship between asthma and COPD: lessons from transgenic mice. Chest 126: 111S-116S.
45. Ma, B., Z. Zhu, R. J. Homer, C. Gerard, R. Strieter, and J. A. Elias. 2004. The C10/CCL6 chemokine and CCR1 play critical roles in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 172: 1872-1881.
46. Zhu, Z., B. Ma, T. Zheng, R. J. Homer, C. G. Lee, I. F. Charo, P. Noble, and J. A. Elias. 2002. IL-13-induced chemokine responses in the lung: role of CCR2 in the pathogenesis of IL-13-induced inflammation and remodeling. J. Immunol. 168: 2953-2962.
47. Lentsch, A. B., T. P. Shanley, V. Sarma, and P. A. Ward. 1997. In vivo suppression of NF-κB and Preservation of IκBα by interleukin-10 and interleukin-13. J. Clin. Invest. 100: 2443-2448.
48. Epinat, J.-C., and T. D. Gilmore. 1999. Diverse agents acts at multiple levels to inhibit the Rel/NF-κB signal transduction pathway. Oncogene 18: 6896-6909.
49. Fujioka, S., J. Niu, C. Schmidt, G. M. Sclabas, B. Peng, T. Uwagawa, Z. Li, D. B. Evans, J. L. Abbruzzese, and P. J. Chiao. 2004. NF-κB and AP-1 connection: mechanism of NF-κB-dependent regulation of AP-1 activity. Mol. Cell. Biol. 24: 7806-7819.
50. Jimi, E., K. Aoki, H. Saito, F. D'Acquisto, M. J. May, I. Nakamura, T. Sudo, T. Kojima, F. Okamoto, H. Fukushima, et al. 2004. Selective inhibition of NF-κB blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat. Med. 10: 617-624.
51. Elias, J. A., Z. Zhu, G. Chupp, and R. J. Homer. 1999. Airway remodeling in asthma. J. Clin. Invest. 104: 1001-1006.
52. Broide, D. H., T. Lawrence, T. Doherty, J. Y. Cho, M. Miller, K. McElwain, S. McElwain, and M. Karin. 2005. Allergen-induced peribronchial fibrosis and mucus production mediated by IκB kinase β-dependent genes in airway epithelium. Proc. Natl. Acad. Sci. USA 102: 17723-17728.
53. Zuhdi Alimam, M., F. M. Piazza, D. M. Selby, N. Letwin, L. Huang, and M. C. Rose. 2000. Muc-5/5ac mucin messenger RNA and protein expression is a marker of goblet cell metaplasia in murine airways. Am. J. Respir. Cell. Mol. Biol. 22: 253-260.
54. rsk pathway is required for Pseudomonas aeruginosa induced mucin overproduction in epithelial cells. Proc. Natl. Acad. Sci. USA 95: 5718-5723.
55. Blease, K., J. M. Schuh, C. Jakubzick, N. W. Lukacs, S. L. Kunkel, B. H. Joshi, R. K. Puri, M. H. Kaplan, and C. M. Hogaboam. 2002. STAT6-deficient mice develop airway hyperresponsiveness and peribronchial fibrosis during chronic fungal asthma. Am. J. Pathol. 160: 481-490.
56. Fujioka, S., C. Schmidt, G. M. Sclabas, Z. Li, H. Pelicano, B. Peng, A. Yao, J. Niu, W. Zhang, D. B. Evans, et al. 2004. Stabilization of p53 is a novel mechanism for proapoptotic function of NF-κB. J. Biol. Chem. 279: 27549-27559.
57. Takada, Y., Y. Kobayashi, and B. B. Aggarwal. 2005. Evodiamine abolishes constitutive and inducible NF-κB activation by inhibiting IκBα kinase activation, thereby suppressing NF-κB-regulated antiapoptotic and metastatic gene expression, up-regulating apoptosis, and inhibiting invasion. J. Biol. Chem. 280: 17203-17212.
58. Matsui, K., A. Fine, B. Zhu, A. Marshak-Rothstein, and S. T. Ju. 1998. Identification of two NF-κB sites in mouse CD95 ligand (Fas ligand) promoter: functional analysis in T cell hybridoma. J. Immunol. 161: 3469-3473.
59. Verhagen, A. M., E. J. Coulson, and D. L. Vaux. 2001. Inhibitor of apoptosis proteins and their relatives: IAPs and other BIRPs. Genome Biol. 2: 3009.1-3009.10.
60. Ekert, P. G., J. Silke, C. J. Hawkins, A. M. Verhagen, and D. L. Vaux. 2001. DIABLO promotes apoptosis by removing MIHA/XIAP from processed caspase 9. J. Cell. Biol. 152: 483-490.
61. Roy, N., Q. L. Deveraux, R. Takahashi, G. S. Salvesen, and J. C. Reed. 1997. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 16: 6914-6925.
62. Zimmermann, N., A. Mishra, N. E. King, P. C. Fulkerson, M. P. Doepker, N. M. Nikolaidis, L. E. Kindinger, E. A. Moulton, B. J. Aronow, and M. E. Rothenberg. 2004. Transcript signatures in experimental asthma: identification of STAT6-dependent and -independent pathways. J. Immunol. 172: 1815-1824.
63. Nelson, G., G. J. C. Wilde, D. G. Spiller, S. M. Kennedy, D. W. Ray, E. Sullivan, J. F. Unitt, and M. R. H. White. 2003. NF-κB signaling is inhibited by glucocorticoid receptor and STAT6 via distinct mechanisms. J. Cell. Sci. 116: 2495-2503.
64. Abu-Amer, Y. 2001. IL-4 abrogates osteoclastogenesis through STAT6-dependent inhibition of NF-κB. J. Clin. Invest. 107: 1375-1385.
65. Shen, C. H., and J. Stavnezer. 1998. Interaction of STAT6 and NF-κB: direct association and synergistic activation of interleukin-4-induced transcription. Mol. Cell. Biol. 18: 3395-3404.
66. Vodanovic-Jankovic, S., P. Hari, P. Jacobs, R. Komorowski, and W. R. Drobyski. 2006. NF-κB as a target for the prevention of graft-versus-host disease: comparative efficacy of bortezomib and PS-1145. Blood 107: 827-834.