Smad3 null mice develop airspace enlargement and are resistant to TGF-β-mediated pulmonary fibrosis

Journal of Immunology

Volumn 173, Issue 3, 2004, Pages 2099-2108

  Bonniaud, Philippe ^a,b   Kolb, Martin ^a,c   Galt, Tom ^a   Robertson, Jennifer ^a   Robbins, Clinton ^a   Stamfli, Martin ^a   Lavery, Carol ^a   Margetts, Peter J ^a   Roberts, Anita B ^d   Gauldie, Jack ^a,e  

^a MCMASTER UNIVERSITY   (Canada)

^b DIJON UNIVERSITY HOSPITAL   (France)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d NATIONAL CANCER INSTITUTE   (United States)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CONNECTIVE TISSUE GROWTH FACTOR; GELATINASE B; MACROPHAGE ELASTASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROCOLLAGEN; PROCOLLAGEN 3A1; PROTEINASE INHIBITOR; SMAD2 PROTEIN; SMAD3 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGRADATION; DISEASE COURSE; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TRANSFER; KNOCKOUT MOUSE; LUNG ALVEOLUS; LUNG FIBROSIS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE REPAIR;

EID: 3242799550     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.3.2099     Document Type: Article

References (62)

1. McAnulty, R. J., and G. J. Laurent. 1995. Pathogenesis of lung fibrosis and potential new therapeutic strategies. Exp. Nephrol. 3:96.
2. Hogg, J. C., and R. M. Senior. 2002. Chronic obstructive pulmonary disease. 2. Pathology and biochemistry of emphysema. Thorax 57:830.
3. Lasky, J. A., and A. R. Brody. 2000. Interstitial fibrosis and growth factors. Environ. Health Perspect. 108:751.
4. Gauldie, J., M. Kolb, and P. J. Sime. 2002. A new direction in the pathogenesis of idiopathic pulmonary fibrosis? Respir. Res. 3:1.
5. Wells, R. G. 2000. Fibrogenesis V: TGF-β signaling pathways. Am. J. Physiol. 279:G845.
6. Sime, P. J., Z. Xing, F. L. Graham, K. G. Csaky, and J. Gauldie. 1997. Adenovector-mediated gene transfer of active transforming growth factor-β1 induces prolonged severe fibrosis in rat lung. J. Clin. Invest. 100:768.
7. Kolb, M., P. J. Margetts, P. J. Sime, and J. Gauldie. 2001. Proteoglycans decorin and biglycan differentially modulate TGF-β-mediated fibrotic responses in the lung. Am. J. Physiol 280:L1327.
8. Selman, M., T. E. King, and A. Pardo. 2001. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann. Intern. Med. 134:136.
9. Nagase, H., and J. F. Woessner, Jr. 1999. Matrix metalloproteinases. J. Biol. Chem. 274:21491.
10. 6-mediated TGF-β activation causes Mmp12-dependent emphysema. Nature 422:169.
11. Corbel, M., S. Caulet-Maugendre, N. Germain, S. Molet, V. Lagente, and E. Boichot. 2001. Inhibition of bleomycin-induced pulmonary fibrosis in mice by the matrix metalloproteinase inhibitor batimastat. J. Pathol 193:538.
12. Roberts, A. B. 2002. The ever-increasing complexity of TGF-β signaling. Cytokine Growth Factor Rev. 13:3.
13. Roberts, A. B. 1999. TGF-β signaling from receptors to the nucleus. Microbes Infect. 1:1265.
14. Datto, M. B., J. P. Frederick, L. Pan, A. J. Borton, Y. Zhuang, and X. F. Wang. 1999. Targeted disruption of Smad3 reveals an essential role in transforming growth factor β-mediated signal transduction. Mol. Cell. Biol. 19:2495.
15. Roberts, A. B., E. Piek, E. P. Bottinger, G. Ashcroft, J. B. Mitchell, and K. C. Flanders. 2001. Is Smad3 a major player in signal transduction pathways leading to fibrogenesis? Chest 120:435.
16. Verrecchia, F., M. L. Chu, and A. Mauviel. 2001. Identification of novel TGF-β/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J. Biol. Chem. 276:17058.
17. Ashcroft, G. S., X. Yang, A. B. Glick, M. Weinstein, J. L. Letterio, D. E. Mizel, M. Anzano, T. Greenwell-Wild, S. M. Wahl, C. Deng, and A. B. Roberts. 1999. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1:260.
18. Flanders, K. C., C. D. Sullivan, M. Fujii, A. Sowers, M. A. Anzano, A. Arabshahi, C. Major, C. Deng, A. Russo, J. B. Mitchell, and A. B. Roberts. 2002. Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am. J. Pathol. 160:1057.
19. Zhao, J., W. Shi, Y. L. Wang, H. Chen, P. Bringas, Jr., M. B. Datto, J. P. Frederick, X. F. Wang, and D. Warburton. 2002. Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am. J. Physiol. 282:L585.
20. Nakao, A., M. Fujii, R. Matsumura, K. Kumano, Y. Saito, K. Miyazono, and I. Iwamoto. 1999. Transient gene transfer and expression of Smad7 prevents bleomycin-induced lung fibrosis in mice. J. Clin. Invest. 104:5.
21. Yang, X., J. J. Letterio, R. J. Lechleider, L. Chen, R. Hayman, H. Gu, A. B. Roberts, and C. Deng. 1999. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J. 18:1280.
22. Bett, A. J., W. Haddara, L. Prevec, and F. L. Graham. 1994. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. USA 91:8802.
23. Kolb, M., P. J. Margetts, T. Galt, P. J. Sime, Z. Xing, M. Schmidt, and J. Gauldie. 2001. Transient transgene expression of decorin in the lung reduces the fibrotic response to bleomycin. Am. J. Respir. Crit. Care Med. 163:770.
24. Stegemann, H., and K. Stalder. 1967. Determination of hydroxyproline. Clin. Chim. Acta 18:267.
25. Kolb, M., P. Bonniaud, T. Galt, P. J. Sime, M. M. Kelly, P. J. Margetts, and J. Gauldie. 2002. Differences in the fibrogenic response after transfer of active transforming growth factor-β1 gene to lungs of "fibrosis- prone" and "fibrosis-resistant" mouse strains. Am. J. Respir. Cell Mol. Biol. 27:141.
26. Zhao, J., P. J. Sime, P. Bringas, Jr., J. D. Tefft, S. Buckley, D. Bu, J. Gauldie, and D. Warburton. 1999. Spatial-specific TGF-β1 adenoviral expression determines morphogenetic phenotypes in embryonic mouse lung. Eur. J. Cell Biol. 78:715.
27. Datto, M., and X. F. Wang. 2000. The Smads: transcriptional regulation and mouse models. Cytokine Growth Factor Rev. 11:37.
28. Kucich, U., J. C. Rosenbloom, W. R. Abrams, and J. Rosenbloom. 2002. Transforming growth factor-β stabilizes elastin mRNA by a pathway requiring active Smads, protein kinase C-δ,and p38. Am. J. Respir. Cell Mol. Biol. 26:183.
29. Itoh, S., M. Thorikay, M. Kowanetz, A. Moustakas, F. Itoh, C. H. Heldin, and P. ten Dijke. 2003. Elucidation of Smad requirement in transforming growth factor-β type 1 receptor-induced responses. J. Biol. Chem. 278:3751.
30. Hautamaki, R. D., D. K. Kobayashi, R. M. Senior, and S. D. Shapiro. 1997. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277:2002.
31. D'Armiento, J., S. S. Dalal, Y. Okada, R. A. Berg, and K. Chada. 1992. Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell 71:955.
32. Finlay, G. A., L. R. O'Driscoll, K. J. Russell, E. M. D'Arcy, J. B. Masterson, M. X. FitzGerald, and C. M. O'Connor. 1997. Matrix metalloproteinase expression and production by alveolar macrophages in emphysema. Am. J. Respir. Crit. Care Med. 156:240.
33. Russell, R. E., A. Thorley, S. V. Culpitt, S. Dodd, L. E. Donnelly, C. Demattos, M. Fitzgerald, and P. J. Barnes. 2002. Alveolar macrophage-mediated elastolysis: roles of matrix metalloproteinases, cysteine, and serine proteases. Am. J. Physiol. 283:L867.
34. Russell, R. E., S. V. Culpitt, C. DeMatos, L. Donnelly, M. Smith, J. Wiggins, and P. J. Barnes. 2002. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 26:602.
35. Lim, S., N. Roche, B. G. Oliver, W. Mattos, P. J. Barnes, and K. Fan Chung. 2000. Balance of matrix metalloprotease-9 and tissue inhibitor of metalloprotease-1 from alveolar macrophages in cigarette smokers: regulation by interleukin-10. Am. J. Respir. Crit. Care Med. 162:1355.
36. Shibata, Y., Z. Zsengeller, K. Otake, N. Palaniyar, and B. C. Trapnell. 2001. Alveolar macrophage deficiency in osteopetrotic mice deficient in macrophage colony-stimulating factor is spontaneously corrected with age and associated with matrix metalloproteinase expression and emphysema. Blood 98:2845.
37. Wert, S. E., M. Yoshida, A. M. LeVine, M. Ikegami, T. Jones, G. F. Ross, J. H. Fisher, T. R. Korfhagen, and J. A. Whitsett. 2000. Increased metalloproteinase activity, oxidant production, and emphysema in surfactant protein D gene-inactivated mice. Proc. Natl. Acad. Sci. USA 97:5972.
38. Leco, K. J., P. Waterhouse, O. H. Sanchez, K. L. Gowing, A. R. Poole, A. Wakeham, T. W. Mak, and R. Khokha. 2001. Spontaneous airspace enlargement in the lungs of mice lacking tissue inhibitor of metalloproteinases-3 (TIMP-3). J. Clin. Invest. 108:817.
39. Feinberg, M. W., M. K. Jain, F. Werner, N. E. Sibinga, P. Wiesel, H. Wang, J. N. Topper, M. A. Perrella, and M. E. Lee. 2000. Transforming growth factor-β1 inhibits cytokine-mediated induction of human metalloelastase in macrophages. J. Biol Chem. 275:25766.
40. Werner, F., M. K. Jain, M. W. Feinberg, N. E. Sibinga, A. Pellacani, P. Wiesel, M. T. Chin, J. N. Topper, M. A. Perrella, and M. E. Lee. 2000. Transforming growth factor-β1 inhibition of macrophage activation is mediated via Smad3. J. Biol. Chem. 275:36653.
41. Tajirian, T., J. W. Dennis, and C. J. Swallow. 2000. Regulation of human monocyte proMMP-9 production by fetuin, an endogenous TGF-β antagonist. J. Cell. Physiol. 185:174.
42. Yu, Q., and I. Stamenkovic. 2000. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis. Genes Dev. 14:163.
43. Santibanez, J. F., J. Guerrero, M. Quintanilla, A. Fabra, and J. Martinez. 2002. Transforming growth factor-β1 modulates matrix metalloproteinase-9 production through the Ras/MAPK signaling pathway in transformed keratinocytes. Biochem. Biophys. Res. Commun. 296:267.
44. Underwood, D. C., R. R. Osborn, S. Bochnowicz, E. F. Webb, D. J. Rieman, J. C. Lee, A. M. Romanic, J. L. Adams, D. W. Hay, and D. E. Griswold. 2000. SB239063, a p38 MAPK inhibitor, reduces neutrophilia, inflammatory cytokines, MMP-9, and fibrosis in lung. Am. J. Physiol. 279:L895.
45. Piek, E., W. J. Ju, J. Heyer, D. Escalante-Alcalde, C. L. Stewart, M. Weinstein, C. Deng, R. Kucherlapati, E. P. Bottinger, and A. B. Roberts. 2001. Functional characterization of transforming growth factor β signaling in Smad2- and Smad3-deficient fibroblasts. J. Biol. Chem. 276:19945.
46. Kolb, M., P. J. Margetts, D. C. Anthony, F. Pitossi, and J. Gauldie. 2001. Transient expression of IL-1β induces acute lung injury and chronic repair leading to pulmonary fibrosis. J. Clin. Invest. 107:1529.
47. Moussad, E. E., and D. R. Brigstock. 2000. Connective tissue growth factor: what's in a name? Mol. Genet. Metab. 71:276.
48. Chen, Y., I. E. Blom, S. Sa, R. Goldschmeding, D. J. Abraham, and A. Leask. 2002. CTGF expression in mesangial cells: involvement of SMADs, MAP kinase, and PKC. Kidney Int. 62:1149.
49. Kucich, U., J. C. Rosenbloom, D. J. Herrick, W. R. Abrams, A. D. Hamilton, S. M. Sebti, and J. Rosenbloom. 2001. Signaling events required for transforming growth factor-β stimulation of connective tissue growth factor expression by cultured human lung fibroblasts. Arch. Biochem. Biophys. 395:103.
50. Hayashi, T., W. G. Stetler-Stevenson, M. V. Fleming, N. Fishback, M. N. Koss, L. A. Liotta, V. J. Ferrans, and W. D. Travis. 1996. Immunohistochemical study of metalloproteinases and their tissue inhibitors in the lungs of patients with diffuse alveolar damage and idiopathic pulmonary fibrosis. Am. J. Pathol. 149:1241.
51. Perez-Ramos, J., M. de Lourdes Segura-Valdez, B. Vanda, M. Selman, and A. Pardo. 1999. Matrix metalloproteinases 2, 9, and 13, and tissue inhibitors of metalloproteinases 1 and 2 in experimental lung silicosis. Am. J. Respir. Crit. Care Med. 160:1274.
52. Pardo, A., M. Selman, R. Ramirez, C. Ramos, M. Montano, G. Stricklin, and G. Raghu. 1992. Production of collagenase and tissue inhibitor of metalloproteinases by fibroblasts derived from normal and fibrotic human lungs. Chest 102:1085.
53. Selman, M., V. Ruiz, S. Cabrera, L. Segura, R. Ramirez, R. Barrios, and A. Pardo. 2000. TIMP-1, -2, -3, and -4 in idiopathic pulmonary fibrosis: a prevailing nondegradative lung microenvironment? Am. J. Physiol. 279:L562.
54. Madtes, D. K., A. L. Elston, L. A. Kaback, and J. G. Clark. 2001. Selective induction of tissue inhibitor of metalloproteinase-1 in bleomycin-induced pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 24:599.
55. Ortiz, L. A., J. Lasky, E. Gozal, V. Ruiz, G. Lungarella, E. Cavarra, A. R. Brody, M. Friedman, A. Pardo, and M. Selman. 2001. Tumor necrosis factor receptor deficiency alters matrix metalloproteinase 13/tissue inhibitor of metalloproteinase 1 expression in murine silicosis. Am. J. Respir. Crit. Care Med. 163:244.
56. Dennler, S., S. Itoh, D. Vivien, P. ten Dijke, S. Huet, and J. M. Gauthier. 1998. Direct binding of Smad3 and Smad4 to critical TGFβ-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17:3091.
57. Datta, P. K., M. C. Blake, and H. L. Moses. 2000. Regulation of plasminogen activator inhibitor-1 expression by transforming growth factor-β-induced physical and functional interactions between smads and Sp1. J. Biol. Chem. 275:40014.
58. Mason, J. M., H. P. Xu, S. K. Rao, A. Leask, M. Barcia, J. Shan, R. Stephenson, and S. Tabibzadeh. 2002. Lefty contributes to the remodeling of extracellular matrix by inhibition of connective tissue growth factor and collagen mRNA expression and increased proteolytic activity in a fibrosarcoma model. J. Biol. Chem. 277:407.
59. Ulloa, L., and S. Tabibzadeh. 2001. Lefty inhibits receptor-regulated Smad phorphorylation induced by the activated transforming growth factor-β receptor. J. Biol. Chem. 276:21397.
60. Zhao, Y., and D. A. Geverd. 2002. Regulation of Smad3 expression in bleomycin-induced pulmonary fibrosis: a negative feedback loop of TGF-β signaling;. Biochem. Biophys. Res. Commun. 294:319.
61. Joos, L., J. Q. He, M. B. Shepherdson, J. E. Connett, N. R. Anthonisen, P. D. Pare, and A. J. Sandford. 2002. The role of matrix metalloproteinase polymorphisms in the rate of decline in lung function. Hum. Mol. Genet. 11:569.
62. Wang, D., T. Kanuma, F. Takama, H. Mizumuma, Y. Ibuki, N. Wake, A. Mogi, Y. Shitara, K. Hagiwara, and S. Takenoshita. 1999. Mutation analysis of the Smad3 gene in human ovarian cancers. Int. J. Oncol. 15:949.