Overexpression of fibroblast growth factor-10 during both inflammatory and fibrotic phases attenuates bleomycin-induced pulmonary fibrosis in mice

American Journal of Respiratory and Critical Care Medicine

Volumn 180, Issue 5, 2009, Pages 424-436

  Gupte, Varsha V ^a   Ramasamy, Suresh K ^a   Reddy, Raghava ^a   Lee, Jooeun ^a   Weinreb, Paul H ^b   Violette, Shelia M ^c   Guenther, Andreas ^d   Warburton, David ^a   Driscoll, Barbara ^a   Minoo, Parviz ^a   Bellusci, Saverio ^a,e  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b BIOGEN   (United States)

^c Stromedix Inc   (United States)

^d JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^e CHILDREN S HOSPITAL LOS ANGELES   (United States)

Author keywords

Alveolar epithelial progenitors; Bleomycin; Fgf10; Fibrosis; Transforming growth factor 1

Indexed keywords

BLEOMYCIN; COLLAGEN; DOXYCYCLINE; FIBROBLAST GROWTH FACTOR 10; GELATINASE A; SURFACTANT PROTEIN C; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FGF10 GENE; GENE; GENE OVEREXPRESSION; INFLAMMATION; LUNG ALVEOLUS CELL TYPE 2; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; LUNG LAVAGE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLEOMYCIN; DISEASE MODELS, ANIMAL; DOXYCYCLINE; FIBROBLAST GROWTH FACTOR 10; LUNG; MICE; MICE, TRANSGENIC; PNEUMONIA; PULMONARY ALVEOLI; PULMONARY FIBROSIS; REFERENCE VALUES; RESPIRATORY MUCOSA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 69249113479     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200811-1794OC     Document Type: Article

References (50)

1. Kim DS, Collard HR, King TE Jr. Classification and natural history of the idiopathic interstitial pneumonias. Proc Am Thorac Soc 2006;3:285-292.
2. American Thoracic Society, European Respiratory Society. Idiopathic pulmonary fibrosis: diagnosis and treatment [international consensus statement]. Am J Respir Crit Care Med 2000;161:646-664.
3. Korfei M, Ruppert C, Mahavadi P, Henneke I, Markart P, Koch M, Lang G, Fink L, Bohle RM, Seeger W, et al. Epithelial endoplasmic reticulum stress and apoptosis in sporadic idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2008;178:838-846.
4. Thannickal VJ, Toews GB, White ES, Lynch JP III, Martinez FJ. Mechanisms of pulmonary fibrosis. Annu Rev Med 2004;55:395-417.
5. Young L, Adamson IY. Epithelial-fibroblast interactions in bleomycin-induced lung injury and repair. Environ Health Perspect 1993;101:56-61.
6. Serrano-Mollar A, Nacher M, Gay-Jordi G, Closa D, Xaubet A, Bulbena O. Intratracheal transplantation of alveolar type II cells reverses bleomycin-induced lung fibrosis. Am J Respir Crit Care Med 2007;176:1261-1268.
7. Ramasamy SK, Mailleux AA, Gupte VV, Mata F, Sala FG, Veltmaat JM, Del Moral PM, De Langhe S, Parsa S, Kelly LK, et al. Fgf10 dosage is critical for the amplification of epithelial cell progenitors and for the formation of multiple mesenchymal lineages during lung development. Dev Biol 2007;307:237-247.
8. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, et al. Fgf10 is essential for limb and lung formation. Nat Genet 1999;21:138-141.
9. Hokuto I, Perl AK, Whitsett JA. FGF signaling is required for pulmonary homeostasis following hyperoxia. Am J Physiol Lung Cell Mol Physiol 2004;286:L580-L587.
10. Marchand-Adam S, Plantier L, Bernuau D, Legrand A, Cohen M, Marchal J, Soler P, Leseche G, Mal H, Aubier M, et al. Keratinocyte growth factor expression by fibroblasts in pulmonary fibrosis: poor response to interleukin-1b. Am J Respir Cell Mol Biol 2005;32:470-477.
11. Igarashi M, Finch PW, Aaronson SA. Characterization of recombinant human fibroblast growth factor (FGF)-10 reveals functional similarities with keratinocyte growth factor (FGF-7). J Biol Chem 1998;273:13230-13235.
12. Jimenez PA, Rampy MA. Keratinocyte growth factor-2 accelerates wound healing in incisional wounds. J Surg Res 1999;81:238-242.
13. Upadhyay D, Correa-Meyer E, Sznajder JI, Kamp DW. FGF-10 prevents mechanical stretch-induced alveolar epithelial cell DNA damage via MAPK activation. Am J Physiol Lung Cell Mol Physiol 2003;284:L350-L359.
14. Clark JC, Tichelaar JW, Wert SE, Itoh N, Perl AK, Stahlman MT, Whitsett JA. FGF-10 disrupts lung morphogenesis and causes pulmonary adenomas in vivo. Am J Physiol Lung Cell Mol Physiol 2001;280:L705-L715.
15. Parsa S, Ramasamy SK, De Langhe S, Gupte VV, Haigh JJ, Medina D, Bellusci S. Terminal end bud maintenance in mammary gland is dependent upon FGFR2b signaling. Dev Biol 2008;317:121-131.
16. 6 monoclonal antibodies: distinct ligand-mimetic and nonligand-mimetic classes. J Biol Chem 2004;279:17875-17887.
17. Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 1988;41:467-470.
18. Lee J, Reddy R, Barsky L, Weinberg K, Driscoll B. Contribution of proliferation and DNA damage repair to alveolar epithelial type 2 cell recovery from hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006;290:L685-L694.
19. Yoshimura S, Nishimura Y, Nishiuma T, Yamashita T, Kobayashi K, Yokoyama M. Overexpression of nitric oxide synthase by the endothelium attenuates bleomycin-induced lung fibrosis and impairs MMP-9/TIMP-1 balance. Respirology 2006;11:546-556.
20. Jules-Elysee K, White DA. Bleomycin-induced pulmonary toxicity. Clin Chest Med 1990;11:1-20.
21. Chung MP, Monick MM, Hamzeh NY, Butler NS, Powers LS, Hunninghake GW. Role of repeated lung injury and genetic background in bleomycin-induced fibrosis. Am J Respir Cell Mol Biol 2003;29:375-380.
22. von Boehmer H. Notch in lymphopoiesis and T cell polarization. Nat Immunol 2005;6:641-642.
23. Kotsianidis I, Nakou E, Bouchliou I, Tzouvelekis A, Spanoudakis E, Steiropoulos P, Sotiriou I, Aidinis V, Margaritis D, Tsatalas C, Bouros D. Global impairment of CD41CD251FOXP31 regulatory T cells in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2009;179:1121-1130.
24. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, et al. The integrin avb6 binds and activates latent TGF-b1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999;96:319-328.
25. Gueders MM, Foidart JM, Noel A, Cataldo DD. Matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs in the respiratory tract: potential implications in asthma and other lung diseases. Eur J Pharmacol 2006;533:133-144.
26. Ito I, Nagai S, Handa T, Muro S, Hirai T, Tsukino M, Mishima M. Matrix metalloproteinase-9 promoter polymorphism associated with upper lung dominant emphysema. Am J Respir Crit Care Med 2005;172:1378-1382.
27. Miyazaki H, Kuwano K, Yoshida K, Maeyama T, Yoshimi M, Fujita M, Hagimoto N, Yoshida R, Nakanishi Y. The perforin mediated apoptotic pathway in lung injury and fibrosis. J Clin Pathol 2004;57:1292-1298.
28. Moore BB, Hogaboam CM. Murine models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008;294:L152-L160.
29. Post M, Souza P, Liu J, Tseu I, Wang J, Kuliszewski M, Tanswell AK. Keratinocyte growth factor and its receptor are involved in regulating early lung branching. Development 1996;122:3107-3115.
30. Guo L, Degenstein L, Fuchs E. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev 1996;10:165-175.
31. Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multiorgan development. Biochem Biophys Res Commun 2000;277:643-649.
32. Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 1997;124:4867-4878.
33. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. Receptor specificity of the fibroblast growth factor family: the complete mammalian FGF family. J Biol Chem 2006;281:15694-15700.
34. Yano T, Deterding RR, Simonet WS, Shannon JM, Mason RJ. Keratinocyte growth factor reduces lung damage due to acid instillation in rats. Am J Respir Cell Mol Biol 1996;15:433-442.
35. Deterding RR, Havill AM, Yano T, Middleton SC, Jacoby CR, Shannon JM, Simonet WS, Mason RJ. Prevention of bleomycin-induced lung injury in rats by keratinocyte growth factor. Proc Assoc Am Physicians 1997;109:254-268.
36. Yi ES, Williams ST, Lee H, Malicki DM, Chin EM, Yin S, Tarpley J, Ulich TR. Keratinocyte growth factor ameliorates radiation- and bleomycin-induced lung injury and mortality. Am J Pathol 1996;149:1963-1970.
37. Sugahara K, Iyama K, Kuroda MJ, Sano K. Double intratracheal instillation of keratinocyte growth factor prevents bleomycin-induced lung fibrosis in rats. J Pathol 1998;186:90-98.
38. Guo J, Yi ES, Havill AM, Sarosi I, Whitcomb L, Yin S, Middleton SC, Piguet P, Ulich TR. Intravenous keratinocyte growth factor protects against experimental pulmonary injury. Am J Physiol 1998;275:L800-L805.
39. Chaudhary NI, Schnapp A, Park JE. Pharmacologic differentiation of inflammation and fibrosis in the rat bleomycin model. Am J Respir Crit Care Med 2006;173:769-776.
40. Zhao Y, Geverd DA. Regulation of SMAD3 expression in bleomycin-induced pulmonary fibrosis: a negative feedback loop of TGF-β signaling. Biochem Biophys Res Commun 2002;294:319-323.
41. Gauldie J, Kolb M, Sime PJ. A new direction in the pathogenesis of idiopathic pulmonary fibrosis? Respir Res 2002;3:1.
42. Strieter RM. Inflammatory mechanisms are not a minor component of the pathogenesis of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2002;165:1206-1207.
43. Pogach MS, Cao Y, Millien G, Ramirez MI, Williams MC. Key developmental regulators change during hyperoxia-induced injury and recovery in adult mouse lung. J Cell Biochem 2007;100:1415-1429.
44. Kolb M, Margetts PJ, Anthony DC, Pitossi F, Gauldie J. Transient expression of IL-1β induces acute lung injury and chronic repair leading to pulmonary fibrosis. J Clin Invest 2001;107:1529-1536.
45. Bonniaud P, Kolb M, Galt T, Robertson J, Robbins C, Stampfli M, Lavery C, Margetts PJ, Roberts AB, Gauldie J. Smad3 null mice develop airspace enlargement and are resistant to TGF-β-mediated pulmonary fibrosis. J Immunol 2004;173:2099-2108.
46. Bonniaud P, Margetts PJ, Ask K, Flanders K, Gauldie J, Kolb M. TGF-β and smad3 signaling link inflammation to chronic fibrogenesis. J Immunol 2005;175:5390-5395.
47. 1 stimulates pulmonary fibrosis and inflammation via a Bax-dependent, Bid-activated pathway that involves matrix metalloproteinase-12. J Biol Chem 2007;282:7723-7732.
48. Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol 1998;201:125-134.
49. Bhushan A, Itoh N, Kato S, Thiery JP, Czernichow P, Bellusci S, Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001;128:5109-5117.
50. Hart A, Papadopoulou S, Edlund H. Fgf10 maintains notch activation, stimulates proliferation, and blocks differentiation of pancreatic epithelial cells. Dev Dyn 2003;228:185-193.