Notch induces myofibroblast differentiation of alveolar epithelial cells via transforming growth factor-β-Smad3 pathway

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 1, 2011, Pages 136-144

  Aoyagi Ikeda, Kana ^a   Maeno, Toshitaka ^a   Matsui, Hiroki ^a,b   Ueno, Manabu ^a   Hara, Kenichiro ^a   Aoki, Yasuhiro ^a   Aoki, Fumiaki ^a   Shimizu, Takehisa ^a   Doi, Hiroshi ^a   Kawai Kowase, Keiko ^a   Iso, Tatsuya ^a   Suga, Tatsuo ^a   Arai, Masashi ^a   Kurabayashi, Masahiko ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b GUNMA UNIVERSITY   (Japan)

Author keywords

EMT; Myofibroblast; Notch; Pulmonary fibrosis; TGF

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; JAGGED1; LUCIFERASE; NOTCH1 RECEPTOR; NOTCH3 RECEPTOR; OCCLUDIN; PROTEIN ZO1; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UVOMORULIN; VIMENTIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERSTITIAL PNEUMONIA; LUNG ALVEOLUS CELL; LUNG FIBROSIS; MALE; MYOFIBROBLAST; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL LINE; CELL MOVEMENT; COCULTURE TECHNIQUES; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLASTS; GENE EXPRESSION REGULATION; MALE; MYOBLASTS; PHOSPHORYLATION; PULMONARY ALVEOLI; PULMONARY FIBROSIS; RATS; RATS, WISTAR; RECEPTORS, NOTCH; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

RATTUS;

EID: 80051502369     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0140OC     Document Type: Article

References (44)

1. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 2007;170:1807-1816. (Pubitemid 47339255)
2. Visscher DW, Myers JL. Histologic spectrum of idiopathic interstitial pneumonias. Proc Am Thorac Soc 2006;3:322-329. (Pubitemid 43845409)
3. Phan SH. Biology of fibroblasts and myofibroblasts. Proc Am Thorac Soc 2008;5:334-337. (Pubitemid 351520680)
4. Kim KK, Wei Y, Szekeres C, Kugler MC, Wolters PJ, Hill ML, Frank JA, Brumwell AN, Wheeler SE, Kreidberg JA, et al. Epithelial cell alpha3beta1 integrin links beta-catenin and Smad signaling to promote myofibroblast formation and pulmonary fibrosis. J Clin Invest 2009;119:213-224.
5. Hashimoto N, Jin H, Liu T, Chensue SW, Phan SH. Bone marrow-derived progenitor cells in pulmonary fibrosis. J Clin Invest 2004;113: 243-252. (Pubitemid 38544209)
6. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-1784. (Pubitemid 38063698)
7. Kisseleva T, Brenner DA. Mechanisms of fibrogenesis. Exp Biol Med (Maywood) 2008;233:109-122. (Pubitemid 351231543)
8. Serini G, Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 1999;250:273-283. (Pubitemid 29367440)
9. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002;3:349-363. (Pubitemid 34619269)
10. Xaubet A, Marin-Arguedas A, Lario S, Ancochea J, Morell F, Ruiz- Manzano J, Rodriguez-Becerra E, Rodriguez-Arias JM, Inigo P, Sanz S, et al. Transforming growth factor-beta1 gene polymorphisms are associated with disease progression in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2003;168:431-435. (Pubitemid 37046871)
11. Bartram U, Speer CP. The role of transforming growth factor beta in lung development and disease. Chest 2004;125:754-765. (Pubitemid 38223659)
12. Yu H, Königshoff M, Jayachandran A, Handley D, Seeger W, Kaminski N, Eickelberg O. Transgelin is a direct target of TGF-beta/Smad3-dependent epithelial cell migration in lung fibrosis. FASEB J 2008;22: 1778-1789. (Pubitemid 351811455)
13. Kaarteenaho-Wiik R, Paakko P, Sormunen R. Ultrastructural features of lung fibroblast differentiation into myofibroblasts. Ultrastruct Pathol 2009;33:6-15.
14. Zhang K, Flanders KC, Phan SH. Cellular localization of transforming growth factor-beta expression in bleomycin-induced pulmonary fibrosis. Am J Pathol 1995;147:352-361.
15. Khalil N, O'Connor RN, Unruh HW, Warren PW, Flanders KC, Kemp A, Bereznay OH, Greenberg AH. Increased production and immunohistochemical localization of transforming growth factor-beta in idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 1991;5:155-162.
16. Willis BC, Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007;293:L525-L534. (Pubitemid 47358808)
17. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 2006; 103:13180-13185. (Pubitemid 44338936)
18. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999;284:770-776. (Pubitemid 29291335)
19. Gridley T. Notch signaling in vascular development and physiology. Development 2007;134:2709-2718. (Pubitemid 47305050)
20. Iso T, Kedes L, Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 2003;194: 237-255. (Pubitemid 36176887)
21. Doi H, Iso T, Sato H, Yamazaki M, Matsui H, Tanaka T, Manabe I, Arai M, Nagai R, Kurabayashi M. Jagged1-selective notch signaling induces smooth muscle differentiation via a RBP-Jkappa-dependent pathway. J Biol Chem 2006;281:28555-28564. (Pubitemid 44506998)
22. Noseda M, Fu Y, Niessen K, Wong F, Chang L, McLean G, Karsan A. Smooth muscle alpha-actin is a direct target of Notch/CSL. Circ Res 2006;98:1468-1470. (Pubitemid 44297068)
23. Liu T, Hu B, Choi YY, Chung M, Ullenbruch M, Yu H, Lowe JB, Phan SH. Notch1 signaling in FIZZ1 induction of myofibroblast differentiation. Am J Pathol 2009;174:1745-1755.
24. Timmerman LA, Grego-Bessa J, Raya A, Bertrán E, Pérez-Pomares JM, Díez J, Aranda S, Palomo S, McCormick F, Izpisúa-Belmonte JC, et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 2004; 18:99-115. (Pubitemid 38090691)
25. Leong KG, Karsan A. Recent insights into the role of Notch signaling in tumorigenesis. Blood 2006;107:2223-2233. (Pubitemid 43345539)
26. Hinz B, Pittet P, Smith-Clerc J, Chaponnier C, Meister JJ. Myofibroblast development is characterized by specific cell-cell adherens junctions. Mol Biol Cell 2004;15:4310-4320. (Pubitemid 39122032)
27. Gu L, Zhu YJ, Yang X, Guo ZJ, Xu WB, Tian XL. Effect of TGF-beta/ Smad signaling pathway on lung myofibroblast differentiation. Acta Pharmacol Sin 2007;28:382-391.
28. Yoshida T, Sinha S, Dandré F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, Owens GK. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res 2003;92:856-864. (Pubitemid 36542526)
29. Iso T, Maeno T, Oike Y, Yamazaki M, Doi H, Arai M, Kurabayashi M. DLL4-selective Notch signaling induces ephrinB2 gene expression in endothelial cells. Biochem Biophys Res Commun 2006;341:708-714. (Pubitemid 43177547)
30. Iso T, Sartorelli V, Chung G, Shichinohe T, Kedes L, Hamamori Y. HERP, a new primary target of Notch regulated by ligand binding. Mol Cell Biol 2001;21:6071-6079. (Pubitemid 32737821)
31. Kawai-Kowase K, Ohshima T, Matsui H, Tanaka T, Shimizu T, Iso T, Arai M, Owens GK, Kurabayashi M. PIAS1 mediates TGFbeta-induced SM alpha-actin gene expression through inhibition of KLF4 function-expression by protein sumoylation. Arterioscler Thromb Vasc Biol 2009;29:99-106.
32. Nieto MA. The Snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 2002;3:155-166.
33. Niessen K, Fu Y, Chang L, Hoodless PA, McFadden D, Karsan A. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J Cell Biol 2008;182:315-325.
34. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM, Borok Z. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 2005;166:1321-1332. (Pubitemid 40586504)
35. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, Ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta Type I receptors. EMBO J 2002;21:1743-1753. (Pubitemid 34614630)
36. Rosendahl A, Pardali E, Speletas M, Ten Dijke P, Heldin CH, Sideras P. Activation of bone morphogenetic protein/Smad signaling in bronchial epithelial cells during airway inflammation. Am J Respir Cell Mol Biol 2002;27:160-169. (Pubitemid 34780795)
37. Gold LI, Sung JJ, Siebert JW, Longaker MT. Type I (RI) and Type II (RII) receptors for transforming growth factor-beta isoforms are expressed subsequent to transforming growth factor-beta ligands during excisional wound repair. Am J Pathol 1997;150:209-222. (Pubitemid 27027111)
38. Zavadil J, Cermak L, Soto-Nieves N, Böttinger EP. Integration of TGFbeta/ Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J 2004;23:1155-1165. (Pubitemid 38436879)
39. Blokzijl A, Dahlqvist C, Reissmann E, Falk A, Moliner A, Lendahl U, Ibáñ ez CF. Cross-talk between the Notch and TGF-beta signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J Cell Biol 2003;163:723-728. (Pubitemid 37517880)
40. Hautmann MB, Madsen CS, Owens GK. A transforming growth factor beta (TGFbeta) control element drives TGFbeta-induced stimulation of smooth muscle alpha-actin gene expression in concert with two CArG elements. J Biol Chem 1997;272:10948-10956.
41. Tomasek JJ, McRae J, Owens GK, Haaksma CJ. Regulation of alpha-smooth muscle actin expression in granulation tissue myofibroblasts is dependent on the intronic CArG element and the transforming growth factor-beta1 control element. Am J Pathol 2005;166:1343-1351. (Pubitemid 40586506)
42. Adam PJ, Regan CP, Hautmann MB, Owens GK. Positive- and negative-acting Kruppel-like transcription factors bind a transforming growth factor beta control element required for expression of the smooth muscle cell differentiation marker SM22alpha in vivo. J Biol Chem 2000;275:37798-37806. (Pubitemid 32004896)
43. Liu Y, Sinha S, Owens G. A transforming growth factor-beta control element required for SM alpha-actin expression in vivo also partially mediates GKLF-dependent transcriptional repression. J Biol Chem 2003;278:48004-48011. (Pubitemid 37523250)
44. Santana A, Saxena B, Noble NA, Gold LI, Marshall BC. Increased expression of transforming growth factor beta isoforms (beta 1, beta 2, beta 3) in bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 1995;13:34-44.