MMP induced by Gr-1+ cells are crucial for recruitment of Th cells into the airways

European Journal of Immunology

Volumn 39, Issue 8, 2009, Pages 2281-2292

  Jung, Yong Woo ^a,c   Zindl, Carlene L ^b   Lai, Jen Feng ^b   Weaver, Casey T ^a,b   Chaplin, David D ^b  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Airway inflammation; Asthma; MMP; Tissue inhibitor of matrix metalloproteinases

Indexed keywords

ANTIGEN; COLLAGEN; GELATINASE B; MATRIX METALLOPROTEINASE; MESSENGER RNA; MONOCLONAL ANTIBODY; NEUTROPHIL COLLAGENASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; CHEMOKINE RECEPTOR; GELATIN; GR 1 PROTEIN, MOUSE; GR-1 PROTEIN, MOUSE; OVALBUMIN; PROTEINASE INHIBITOR;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CONTROLLED STUDY; ENZYME INHIBITION; EOSINOPHILIA; GENE EXPRESSION REGULATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; RESPIRATORY TRACT INFLAMMATION; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; CELL MOTION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; EOSINOPHIL; GENE EXPRESSION; GENETICS; HELPER CELL; IMMUNOLOGY; INFLAMMATION; LUNG; METABOLISM; PATHOLOGY; RESPIRATORY SYSTEM; TH1 CELL; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL MOVEMENT; COLLAGEN; EOSINOPHILS; GELATIN; GENE EXPRESSION; INFLAMMATION; LUNG; MATRIX METALLOPROTEINASE 8; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; OVALBUMIN; PROTEASE INHIBITORS; RECEPTORS, CHEMOKINE; RESPIRATORY SYSTEM; RNA, MESSENGER; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS; TH2 CELLS; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 70249092568     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838985     Document Type: Article

References (44)

1. Liu, A. H., Endotoxin exposure in allergy and asthma: reconciling a paradox. J. Allergy Clin. Immunol. 2002. 109: 379-392.
2. Bradley, B. L., Azzawi, M., Jacobson, M., Assoufi, B., Collins, J. V., Irani, A. M., Schwartz, L. B. et al., 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. 1991. 88: 661-674.
3. Gibson, P. G., Simpson, J. L. and Saltos, N., Heterogeneity of airway inflammation in persistent asthma: evidence of neutrophilic inflammation and increased sputum interleukin-8. Chest 2001. 119: 1329-1336. (Pubitemid 32686012)
4. Kelly, E. A., Busse, W. W. and Jarjour, N. N., Increased matrix metalloproteinase-9 in the airway after allergen challenge. Am. J. Respir. Crit. Care Med. 2000. 162: 1157-1161.
5. Koh, Y. Y., Dupuis, R., Pollice, M., Albertine, K. H., Fish, J. E. and Peters, S. P., Neutrophils recruited to the lungs of humans by segmental antigen challenge display a reduced chemotactic response to leukotriene B4. Am. J. Respir. Cell Mol. Biol. 1993. 8: 493-499.
6. Lommatzsch, M., Julius, P., Kuepper, M., Garn, H., Bratke, K., Irmscher, S., Luttmann, W. et al., The course of allergen-induced leukocyte infiltration in human and experimental asthma. J. Allergy Clin. Immunol. 2006. 118: 91-97.
7. Nocker, R. E., Out, T. A., Weller, F. R., Mul, E. P., Jansen, H. M. and van der Zee, J. S., Influx of neutrophils into the airway lumen at 4h after segmental allergen challenge in asthma. Int. Arch. Allergy Immunol. 1999. 119: 45-53.
8. Lagasse, E. and Weissman, I. L., Flow cytometric identification of murine neutrophils and monocytes. J. Immunol. Methods 1996. 197: 139-150. (Pubitemid 26342018)
9. Dalod, M., Hamilton, T., Salomon, R., Salazar-Mather, T. P., Henry, S. C., Hamilton, J. D. and Biron, C. A., Dendritic cell responses to early murine cytomegalovirus infection: subset functional specialization and differential regulation by interferon alpha/beta. J. Exp. Med. 2003. 197: 885-898.
10. Nakano, H., Yanagita, M. and Gunn, M. D., CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J. Exp. Med. 2001. 194: 1171-1178.
11. Bronte, V., Apolloni, E., Cabrelle, A., Ronca, R., Serafini, P., Zamboni, P., Restifo, N. P. and Zanovello, P., Identification of a CD11b(+)/Gr-1(+)/ CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood 2000. 96: 3838-3846.
12. Mordue, D. G. and Sibley, L. D., A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J. Leukoc. Biol. 2003. 74: 1015-1025.
13. Tepper, R. I., Coffman, R. L. and Leder, P., An eosinophil-dependent mechanism for the antitumor effect of interleukin-4. Science 1992. 257: 548-551.
14. Stoppacciaro, A., Melani, C., Parenza, M., Mastracchio, A., Bassi, C., Baroni, C., Parmiani, G. and Colombo, M. P., Regression of an established tumor genetically modified to release granulocyte colony-stimulating factor requires granulocyte-T cell cooperation and T cell-produced interferon gamma. J. Exp. Med. 1993. 178: 151-161.
15. Lee, S., Zheng, M., Kim, B. and Rouse, B. T., Role of matrix metalloproteinase-9 in angiogenesis caused by ocular infection with herpes simplex virus. J. Clin. Invest. 2002. 110: 1105-1111.
16. Sitia, G., Isogawa, M., Iannacone, M., Campbell, I. L., Chisari, F. V. and Guidotti, L. G., MMPs are required for recruitment of antigen-nonspecific mononuclear cells into the liver by CTLs. J. Clin. Invest. 2004. 113: 1158-1167.
17. Sitia, G., Isogawa, M., Kakimi, K., Wieland, S. F., Chisari, F. V. and Guidotti, L. G., Depletion of neutrophils blocks the recruitment of antigen-nonspecific cells into the liver without affecting the antiviral activity of hepatitis B virus-specific cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 2002. 99: 13717-13722.
18. Park, S. J., Wiekowski, M. T., Lira, S. A. and Mehrad, B., Neutrophils regulate airway responses in a model of fungal allergic airways disease. J. Immunol. 2006. 176: 2538-2545. (Pubitemid 43201705)
19. Sternlicht, M. D. and Werb, Z., How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 2001. 17: 463-516.
20. Baronas-Lowell, D., Lauer-Fields, J. L., Borgia, J. A., Sferrazza, G. F., AlGhoul, M., Minond, D. and Fields, G. B., Differential modulation of human melanoma cell metalloproteinase expression by alpha2beta1 integrin and CD44 triple-helical ligands derived from type IV collagen. J. Biol. Chem. 2004. 279: 43503-43513.
21. Saleem, M., Kweon, M. H., Johnson, J. J., Adhami, V. M., Elcheva, I., Khan, N., Bin Hafeez, B. et al., S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc. Natl. Acad. Sci. USA 2006. 103: 14825-14830.
22. Kruidenier, L., MacDonald, T. T., Collins, J. E., Pender, S. L. and Sanderson, I. R., Myofibroblast matrix metalloproteinases activate the neutrophil chemoattractant CXCL7 from intestinal epithelial cells. Gastroenterology 2006. 130: 127-136. (Pubitemid 43049843)
23. Randolph, D. A., Carruthers, C. J., Szabo, S. J., Murphy, K. M. and Chaplin, D. D., Modulation of airway inflammation by passive transfer of allergen-specific Th1 and Th2 cells in a mouse model of asthma. J. Immunol. 1999. 162: 2375-2383.
24. Jung, Y. W., Schoeb, T. R., Weaver, C. T. and Chaplin, D. D., Antigen and lipopolysaccharide play synergistic roles in the effector phase of airway inflammation in mice. Am. J. Pathol. 2006. 168: 1425-1434.
25. Su, S. B., Grajewski, R. S., Luger, D., Agarwal, R. K., Silver, P. B., Tang, J., Tuo, J. et al., Altered chemokine profile associated with exacerbated autoimmune pathology under conditions of genetic interferon-gamma deficiency. Invest. Ophthalmol. Vis. Sci. 2007. 48: 4616-4625.
26. Leppert, D., Waubant, E., Galardy, R., Bunnett, N. W. and Hauser, S. L., T cell gelatinases mediate basement membrane transmigration in vitro. J. Immunol. 1995. 154: 4379-4389.
27. Han, Y. P., Nien, Y. D. and Garner, W. L., Tumor necrosis factor-alpha-induced proteolytic activation of pro-matrix metalloproteinase-9 by human skin is controlled by down-regulating tissue inhibitor of metalloproteinase-1 and mediated by tissue-associated chymotrypsin-like proteinase. J. Biol. Chem. 2002. 277: 27319-27327.
28. Dalod, M., Salazar-Mather, T. P., Malmgaard, L., Lewis, C., Asselin-Paturel, C., Briere, F., Trinchieri, G. and Biron, C. A., Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 2002. 195: 517-528.
29. de Heer, H. J., Hammad, H., Soullie, T., Hijdra, D., Vos, N., Willart, M. A., Hoogsteden, H. C. and Lambrecht, B. N., Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 2004. 200: 89-98.
30. Cundall, M., Sun, Y., Miranda, C., Trudeau, J. B., Barnes, S. and Wenzel, S. E., Neutrophil-derived matrix metalloproteinase-9 is increased in severe asthma and poorly inhibited by glucocorticoids. J. Allergy Clin. Immunol. 2003. 112: 1064-1071.
31. Hermant, B., Bibert, S., Concord, E., Dublet, B., Weidenhaupt, M., Vernet, T. and Gulino-Debrac, D., Identification of proteases involved in the proteolysis of vascular endothelium cadherin during neutrophil transmigration. J. Biol. Chem. 2003. 278: 14002-14012.
32. Vermaelen, K. Y., Cataldo, D., Tournoy, K., Maes, T., Dhulst, A., Louis, R., Foidart, J. M. et al., Matrix metalloproteinase-9-mediated dendritic cell recruitment into the airways is a critical step in a mouse model of asthma. J. Immunol. 2003. 171: 1016-1022. (Pubitemid 36871418)
33. McMillan, S. J., Kearley, J., Campbell, J. D., Zhu, X. W., Larbi, K. Y., Shipley, J. M., Senior, R. M. et al., Matrix metalloproteinase-9 deficiency results in enhanced allergen-induced airway inflammation. J. Immunol. 2004. 172: 2586-2594. (Pubitemid 38182410)
34. Kumagai, K., Ohno, I., Okada, S., Ohkawara, Y., Suzuki, K., Shinya, T., Nagase, H. et al., Inhibition of matrix metalloproteinases prevents allergen-induced airway inflammation in a murine model of asthma. J. Immunol. 1999. 162: 4212-4219. (Pubitemid 29314809)
35. Lee, K. S., Jin, S. M., Kim, S. S. and Lee, Y. C., Doxycycline reduces airway inflammation and hyperresponsiveness in a murine model of toluene diisocyanate-induced asthma. J. Allergy Clin. Immunol. 2004. 113: 902-909.
36. Bosse, M., Chakir, J., Rouabhia, M., Boulet, L. P., Audette, M. and Laviolette, M., Serum matrix metalloproteinase-9: tissue inhibitor of metalloproteinase-1 ratio correlates with steroid responsiveness in moderate to severe asthma. Am. J. Respir. Crit. Care Med. 1999. 159: 596-602.
37. Mattos, W., Lim, S., Russell, R., Jatakanon, A., Chung, K. F. and Barnes, P. J., Matrix metalloproteinase-9 expression in asthma: effect of asthma severity, allergen challenge, and inhaled corticosteroids. Chest 2002. 122: 1543-1552. (Pubitemid 35366062)
38. Vignola, A. M., Riccobono, L., Mirabella, A., Profita, M., Chanez, P., Bellia, V., Mautino, G. et al., Sputum metalloproteinase-9/tissue inhibitor of metalloproteinase-1 ratio correlates with airflow obstruction in asthma and chronic bronchitis. Am. J. Respir. Crit. Care Med. 1998. 158: 1945-1950.
39. Murphy, K. M., Heimberger, A. B. and Loh, D. Y., Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 1990. 250: 1720-1723.
40. Randolph, D. A., Stephens, R., Carruthers, C. J. and Chaplin, D. D., Cooperation between Th1 and Th2 cells in a murine model of eosinophilic airway inflammation. J. Clin. Invest. 1999. 104: 1021-1029.
41. Fleming, T. J., Fleming, M. L. and Malek, T. R., Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J. Immunol. 1993. 151: 2399-2408.
42. Pagenstecher, A., Stalder, A. K. and Campbell, I. L., RNase protection assays for the simultaneous and semiquantitative analysis of multiple murine matrix metalloproteinase (MMP) and MMP inhibitor mRNAs. J. Immunol. Methods 1997. 206: 1-9. (Pubitemid 27395859)
43. Oh, L. Y., Larsen, P. H., Krekoski, C. A., Edwards, D. R., Donovan, F., Werb, Z. and Yong, V. W., Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 1999. 19: 8464-8475. (Pubitemid 30226765)
44. Heo, J. H., Lucero, J., Abumiya, T., Koziol, J. A., Copeland, B. R. and del Zoppo, G. J., Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1999. 19: 624-633.