Inhibition of chronic airway inflammation and remodeling by Galectin-3 gene therapy in a murine model

Journal of Immunology

Volumn 176, Issue 3, 2006, Pages 1943-1950

  López, Esther ^a   Del Pozo, Victoria ^a   Miguel, Teresa ^a   Sastre, Beatriz ^a   Seoane, Carmen ^a   Civantos, Esther ^a   Llanes, Elena ^a   Baeza, M Luisa ^b   Palomino, Pilar ^a   Cárdaba, Blanca ^a   Gallardo, Soledad ^a   Manzarbeitia, Félix ^a   Zubeldia, José M ^b   Lahoz, Carlos ^a  

^a Hospital UniversitarioFundación Jiménez Díaz   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; CYTOKINE; GALECTIN 3; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; MESSENGER RNA; METHACHOLINE; OVALBUMIN; PLASMID DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHUS HYPERREACTIVITY; CHRONIC INFLAMMATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CYTOKINE RELEASE; EOSINOPHIL COUNT; GAL 3 GENE; GENE; GENE THERAPY; HISTOPATHOLOGY; LUNG FIBROSIS; LUNG LAVAGE; MALE; MUCUS SECRETION; NONHUMAN; PERIODIC ACID SCHIFF STAIN; PRIORITY JOURNAL; PROVOCATION TEST; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL ANALYSIS;

EID: 31144445789     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.3.1943     Document Type: Article

References (66)

1. Bousquet, J., P. K. Jeffery, W. W. Busse, M. Johnson, and A. M. Vignola. 2000. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 161: 1720-1745.
2. Jeffery, P. K., A. J. Wardlaw, F. C. Nelson, J. V. Collins, and A. B. Kay. 1989. Bronchial biopsies in asthma: an ultrastructural, quantitative study and correlation with hyperreactivity. Am. Rev. Respir. Dis. 140: 1745-1753.
3. Busse, W. W., and R. F. Lemanske. 2001. Asthma. N. Engl. J. Med. 344: 350-354.
4. Tattersfield A. E., A. J. Knox, J. R. Britton, and I. P. Hall. 2002. Asthma. Lancet 360: 1313-134.
5. Gleich, G. J., C. R. Adolphson, and K. M. Leiferman. 1993. The biology of the eosinophilic leukocyte. Annu. Rev. Med. 44: 85-101.
6. + T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia. Am. J. Respir. Cell. Mol. Biol. 10: 587-593.
7. Blyth, D. I., T. F. Wharton, M. S. Pedrick, T. J. Savage, and S. Sanjar. 2000. Airway subepithelial fibrosis in a murine model of atopic asthma: suppression by Dexamethasone or anti-interleukin-5 antibody. Am. J. Respir. Cell. Mol. Biol. 23: 241-246.
8. Flood-Page, P., A. Menzies-Gow, S. Phipps, S. Ying, A. Wangoo, M. S. Ludwig, N. Barnes, D. Robinson, and A. B. Kay. 2003. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J. Clin. Invest. 112: 1029-1036.
9. Cho, J. Y., M. Miller, K. J. Baek, J. W. Han, J. Nayar, S. Y. Lee, K. McElwain, S. McElwain, S. Friedman, and D. H. Broide. 2004. Inhibition of airway remodeling in IL-5-deficient mice. J. Clin. Invest. 113: 551-560.
10. Del Pozo, V., E. De Arruda-Chaves, B. De Andrés, B. Cárdaba, A. López-Farre, S. Gallardo, M. I. Cortegano, L. Vidarte, A. Jurado, P. Palomino, and C. Lahoz. 1997. Eosinophils transcribe and translate mRNA for inducible nitric oxide synthase. J. Immunol. 158: 859-864.
11. Martin, L. B., H. Kita, K. M. Leiferman, and G. J. Gleich. 1996. Eosinophils in allergy: role in disease, degranulation, and cytokines. Int. Arch. Allergy Immunol. 109: 207-215.
12. Rothenberg, M. E. 1998. Eosinophilia. N. Engl. J. Med. 338: 1592-154.
13. Broide, D. 2002. Fast flowing eosinophils: signals for stopping and stepping out of blood vessels. Am. J. Respir. Cell. Mol. Biol. 26: 637-640.
14. Sanderson, C. J. 1992. Interleukin-5, eosinophils and disease. Blood 79: 3101-3109.
15. Singh, A. D., and C. J. Sanderson. 1997. Anti-interleukin-5 strategies as a potential treatment for asthma. Thorax 52: 483-485.
16. Garlisi, C. G. 1992. IL-5 inhibition as a therapy for allergic disease. Pulm. Pharma. Ther. 12: 81-85.
17. Leckie, M. J., A. Brinke, J. Khan, Z. Diamant, B. J. O'Connor, C. M. Walls, A. K. Mathur, H. C. Cowley, K. F. Chung, R. Dukanovic, et al. 2000. Effects of and interleukin-5 blocking monoclonal antibody on eosinophils, airway hyperresponsiveness, and the late asthmatic response. Lancet 356: 2144-2148.
18. Flood-Page, P. T., A. N Menzies-Gow, A. B. Kay, and D. S. Robinson. 2003. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am. J. Respir. Crit. Care Med. 167: 199-204.
19. Kips, J. C., B. J. O'Connor, S. J. Langley, A. Woodcock, H. A. M. Kerstjens, D. S. Postma, M. Danzig, F. Cuss, and R. A. Pauwels. 2003. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am. J. Respir. Crit. Care Med. 167: 1655-1659.
20. O'Byrne, P. M., M. D. Inman, and K. Parameswaran. 2001. The trials and tribulations of IL-5, eosinophils, and allergic asthma. J. Allergy Clin. Immunol. 108: 503-508.
21. Kay, A. B., and A. Menzies-Gow. 2003. Eosinophils and interleukin-5: the debate continues. Am. J. Respir. Crit. Care Med. 167: 1586-1587.
22. Busse, W. W., and A. E. B. Kelly. 2003. Is the eosinophil a "Humpty Dumpty" cell in asthma? Am. J. Respir. Crit. Care Med. 167: 102-103.
23. Mauser, P. J., A. M. Pitman, X. Fernandez, S. K. Foran, G. K. Adams, W. Kreutner, R. W. Egan, and R. W. Chapman. 1995. Effects of an antibody to interleukin-5 in a monkey model of asthma. Am. J. Respir. Crit. Care Med. 152: 467-472.
24. Yu, C., A. B. Cantor, H. Yang, C. Browne, R. A. Wells, Y. Fujiwara, and S. H. Orkin. 2002. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J. Exp. Med. 195: 1387-1395.
25. Humbles, A. A., C. M. Lloyd, S. J. McMillan, D. S. Friend, G. Xanthou, E. E. McKenna, S. Ghiran, N. P. Gerard, C. Yu, S. H. Orkin, and C. Gerard. 2004. A critical role for eosinophils in allergic airways remodeling. Science 305: 1776-1779.
26. Mishra, A., S. P. Hogan, J. J. Lee, P. S. Foster, and M. E. Rothenberg. 1999. Fundamental signals that regulate eosinophil homing to the gastrointestinal tract. J. Clin. Invest. 103: 1719-1727.
27. Nutku, E., H. Aizawa, S. A. Hudson, and B. S. Bochner. 2003. Ligation of Siglec-8: a selective mechanism for induction of human eosinophil apoptosis. Blood 101: 5014-5020.
28. Djukanovic, R., S. J. Wilson, M. Kraft, N. N. Jarjour, M. Steel, K. Fan Chung, W. Bao, A. Fowler-Taylor, J. Matthews, W. W. Busse, et al. 2004. Effects of treatment with anti-immunoglobulin E antibody Omalizumab on airway inflammation in allergic asthma. Am. J. Respir. Crit. Care Med. 170: 583-593.
29. Cortegano, I., V. Del Pozo, B. Cárdaba, B. De Andrés, S. Gallardo, A. Del Amo, I. Arrieta, A. Jurado, P. Palomino, F. T. Liu and C. Lahoz. 1998. Galectin-3 down-regulates IL-5 gene expression on different cell types. J. Immunol. 161: 385-389.
30. Cortegano, I., V. Del Pozo, B. Cárdaba, I. Arrieta, S. Gallardo, M. Rojo, E. Aceituno, T. Takai, S. Verbeek, P. Palomino, and C. Lahoz. 2000. Interaction between Galectin-3 and FcγRII induces down-regulation of IL-5 gene: implication of the promote sequence IL-5 RE III. Glycobiology 10: 237-242.
31. Gritzmacher, C. A., M. W. Robertson, and F. T. Liu. 1988. IgE-binding protein: subcellular location and gene expression in many murine tissues and cells. J. Immunol. 141: 2801-2806.
32. Almkvist, J., and A. Karlsson. 2004. Galectins as inflammatory mediators. Glycoconj. J. 19: 575-581.
33. Rabinovich, G. A., L. G. Baum, N. Tinari, R. Paganelli, C. Natoli, F. T. Liu, and S. Iacobelli. 2002. Galectins and their ligands: amplifiers, silencers or turners of the inflammatory response? Trends Immunol. 23: 313-320.
34. Del Pozo, V., M. Rojo, M. L. Rubio, I. Cortegano, B. Cárdaba, S. Gallardo, M. Ortega, E. Civantos, E. López, M. Martín-Mosquero, et al. 2002. Gene therapy with Gal-3 inhibits bronchial obstruction and inflammation in antigen-challenged rats through interleukin-5 gene downregulation. Am. J. Respir. Crit. Care Med. 166: 732-737.
35. Shinagawa, K., and M. Kojima. 2003. Mouse model of airway remodeling. Am. J. Respir. Crit. Care Med. 168: 959-967.
36. Hattori, N., S. Mizuno, Y. Yoshida, K. Chin, M. Mishima, T. H. Sisson, R. H. Simon, T. Nakamura, and M. Miyake. 2004. The plasminogen activation system reduces fibrosis in the lung by hepatocyte growth factor-dependent mechanism. Am. J. Pathol. 164: 1091-1098.
37. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, G. L. Larsen, C. G. Irvin, and E. W. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156: 766-755.
38. Kumar, R. K., C. Herbert, P. S. Thomas, L. Wollin, R. Beume, M. Yang, D. C. Webb, and P. Foster. 2003. Inhibition of inflammation and remodeling by Roflumilast and Dexamethasone in murine chronic asthma. J. Pharmacol. Exp. Ther. 307: 349-355.
39. T. Tsuchiya, Y. Nishimura, T. Nishiuma, Y. Kotani, Y. Funada, S. Yoshimura, and M. Yokoyama. 2003. Airway remodeling of murine chronic antigen exposure model. J. Asthma 40: 935-944.
40. Redington, A. E. 2000. Fibrosis and airway remodelling. Clin. Exp. Allergy 30: 42-45.
41. Kumar, R. K., and P. S. Foster. 2002. Modeling allergic asthma in mice: Pitfalls and opportunities. Am. J. Respir. Crit. Care Med. 27: 267-272.
42. Williams, T. J. 2004. The eosinophil enigma. J. Clin. Invest. 113: 507-509.
43. Wardlaw, A. J., C. E. Brightling, R. Green, G. Woltmann, P. Bradding, and I. D. Pavord. 2002. New insights into the relationship between airway inflammation and asthma. Clin. Science 103: 201-211.
44. Wardlaw, A. J., F. S. Symon, and G. M. Walsh. 1994. Eosinophil adhesion in allergic inflammation. J. Allergy Clin. Immunol. 94: 1163-1171.
45. Owen, W. F., and F. Austen. 1994. Cytokine regulation of eosinophil mediated inflammatory reactions by modulation of eosinophil programmed cell death and subsequence priming for augmented function: eosinophils in allergy and inflammation. New York, Marcel Decker, pp 239-253.
46. Tanaka, H., M. Komai, K. Nagao, M. Ishizaki, D. Kajiwara, K. Takatsu, G. Delespesse, and H. Nagai. 2004. Role of interleukin-5 and eosinophils in allergen induced airway remodeling in mice. Am. J. Respir. Cell Mol. Biol. 31: 62-68.
47. Wood, L. J., H. D. Inman, R. H. Watson, R. Foley, J. A. Denburg, and P. M. O'Byrne. 1998. Changes in bone marrow inflammatory cell progenitors after inhaled allergen in asthmatic subjects. Am. J. Respir. Crit. Care Med. 157: 99-105.
48. Minshall, E. M., R. Schleimer, L. Cameron, M. Minncozzi, R. W. Egan, J. C. Gutierrez-Ramos, D. M. Eidelman, and Q. Hamid. 1998. Interleukin-5 expression in the bone marrow of sensitized Balb/c mice after allergen challenge. Am. J. Respir. Crit. Care Med. 158: 951-957.
49. Liu, L. Y., J. B. Sedgwick, M. E. Bates, R. F. Vrtis, J. E. Gern, H. Kita, N. N. Jarjour, W. W. Busse, and E. A. Kelly. 2002. Decreased expression of membrane IL-5 receptor α on human eosinophils. II. IL-5 down-modulates its receptor via a proteinase-mediated process. J. Immunol. 169: 6459-6466.
50. Zavorotinskaya, T., A. Tomkinson, and J. E. Murphy. 2003. Treatment of experimental asthma by long-term gene therapy directed against IL-4 and IL-13. Mol. Ther. 2: 155-162.
51. Pardoll, D. M., and A. M. Beckerleg. 1995. Exposing the immunology of naked DNA vaccines. Immunity 3: 165-169.
52. Hengge, U. R., P.S. Walker, and J. C. Vogel. 1996. Expression of naked DNA in human, pig, and mouse skin. J. Clin. Invest. 97: 2911-2916.
53. Mehlhop, P. D., M. Van de Rijn, A. B. Goldberg, J. P. Brewer, V. P. Kurup, T. R. Martin, and H. C. Oettgen. 1997. Allergen-induced bronchial hyperreactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc. Natl. Acad. Sci. USA 94: 1344-1349.
54. Kay, A. B., S. Phipps, and D. S. Robinson. 2004. A role for eosinophils in airway remodelling in asthma. Trends Immunol. 235: 1-6.
55. Robinson, D. S., A. Tsicopoulus, Q. Meng, S. Durham, A. B. Kay, and Q. Hamid. 1996. Increased interleukin-10 messenger RNA expression in atopic allergy and asthma. Am. J. Respir. Cell Mol. Biol. 14: 113-117.
56. Tillie-Leblond, I., J. Pugin, C. H. Marquete, C. Lamblin, F. Saulnier, A. Brichet, B. Wallaert, A. B. Tonnel, and P. Gosset. 1999. Balance between proinflammatory cytokines and their inhibitors in bronchial lavage from patients with status asthmaticus. Am. J. Respir. Crit. Care Med. 159: 487-494.
57. Gentil, D. A., A. Patel, C. Ollila, P. Fireman, A. Zeevi, W. J. Doyle, and D. P. Skoner. 1999. Diminished IL-10 production in subjects with allergy after infection with influenza A virus. J. Allergy Clin. Immunol. 103: 1045-1048.
58. Borish, L., A. Aarons, J. Rumbyrt, P. Cvietusa, J. Negri, and S. Wenzel. 1996. Interleukin-10 regulation in normal subjects and patients with asthma. J. Allergy Clin. Immunol. 97: 1288-1296.
59. Zhang, D. H., L. Yang, and A. Ray. 1988. Differential responsiveness of the IL-5 and IL-4 genes to transcription factor GATA-3. J. Immunol. 161: 3817-3821.
60. Rogan, D. F., D. J. Cousins, S. Santagelo, P. A. Ioannou, M. Antoniou, T. H. Lee, and D. Z. Staynov. 2004. Analysis of intergenic transcription in the human IL-4/IL-13 gene cluster. Proc. Natl. Acad. Sci. USA 101: 2446-2451.
61. Zuberi, R. I., D. K. Hsu, O. Kalayci, H. Y. Chen, H. K. Sheldon, L. Yu, J. R. Apgar, T. Kawakami, C. M. Lilly, and F. T. Liu. 2004. Critical role for Galectin-3 in airway inflammation and bronchial hyperresponsiveness in a murine model of asthma. Am. J. Pathol. 165: 2045-2053.
62. Li, X.-M., R. K. Chopra, T-Y. Chou, B. H. Schofield, M. Wills-Karp, and S. Huang. 1996. Mucosal IFN-γ gene transfer inhibits pulmonary allergic responses in mice. J. Immunol. 157: 3216-3219.
63. Hofstra, C. L., I. Van Ark, G. Hofman, F. P. Nijkamp, P. M. Jardieu, and A. J. M. Oosterhout. 1988. Differential effects of endogenous and exogenous Interferon-γ on immunoglobulin E, cellular infiltration and airway responsiveness in a murine model of allergic asthma. Am. J. Respir. Cell Mol. Biol. 19: 826-835.
64. Li, L., C. T. Liu, K. Wang, and Y. M. Pang. 2005. Inhibitory effects of Galectin-3 on the inflammatory cytokines and chemokines in guinea pig asthma models. Sichuan Da Xue Xue Bao Yi Xue Ban 36: 355-358.
65. Horner, A. A., K. Takabaysahi, J. M. Zubeldia, and E. Raz. 2002. Immunostimulatory DNA-based therapeutics for experimental and clinical allergy. Allergy 57: 24-29.
66. Broide, D. 2004. Immunomodulation and reversal of airway remodeling in asthma. Curr. Opin. Allergy Clin. Immunol. 4: 529-532.