c-Jun N-terminal kinase 1 promotes transforming growth factor-β1- induced epithelial-to-mesenchymal transition via control of linker phosphorylation and transcriptional activity of Smad3

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 4, 2011, Pages 571-581

  Van Der Velden, Jos L J ^a   Alcorn, John F ^a   Guala, Amy S ^a   Badura, Elsbeth C H L ^a   Janssen Heininger, Yvonne M W ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

c Jun N terminal kinase 1; Epithelial to mesenchymal transition; Smad3; Transforming growth factor 1

Indexed keywords

CALVASCULIN; CARG BOX BINDING FACTOR A; FIBRONECTIN 1; HIGH MOBILITY GROUP A2; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; STRESS ACTIVATED PROTEIN KINASE 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENETIC TRANSCRIPTION; LUNG ALVEOLUS EPITHELIUM; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ANIMALS; BINDING SITES; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUNG; MICE; MUTANT PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 79953761687     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0282OC     Document Type: Article

References (50)

1. Strieter RM, Mehrad B. New mechanisms of pulmonary fibrosis. Chest 2009;136:1364-1370.
2. 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)
3. 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)
4. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through Smad proteins. Nature 1997;390:465-471.
5. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700. (Pubitemid 36724933)
6. Macias-Silva M, Abdollah S, Hoodless PA, Pirone R, Attisano L, Wrana JL. MADR2 is a substrate of the TGFbeta receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 1996;87:1215-1224. (Pubitemid 27010105)
7. Dennler S, Goumans MJ, ten Dijke P. Transforming growth factor beta signal transduction. J Leukoc Biol 2002;71:731-740.
8. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003;425:577-584. (Pubitemid 37280136)
9. Engel ME, McDonnell MA, Law BK, Moses HL. Interdependent Smad and JNK signaling in transforming growth factor-beta-mediated transcription. J Biol Chem 1999;274:37413-37420.
10. Hocevar BA, Prunier C, Howe PH. Disabled-2 (dab2) mediates transforming growth factor beta (TGFbeta)-stimulated fibronectin synthesis through TGFbeta-activated kinase 1 and activation of the JNK pathway. J Biol Chem 2005;280:25920-25927. (Pubitemid 40962305)
11. Kretzschmar M, Doody J, Timokhina I, Massague J. A mechanism of repression of TGFbeta/Smad signaling by oncogenic ras. Genes Dev 1999;13:804-816. (Pubitemid 29169840)
12. de Caestecker MP, Yahata T, Wang D, Parks WT, Huang S, Hill CS, Shioda T, Roberts AB, Lechleider RJ. The Smad4 activation domain (SAD) is a proline-rich, p300-dependent transcriptional activation domain. J Biol Chem 2000;275:2115-2122. (Pubitemid 30060840)
13. de Caestecker MP, Parks WT, Frank CJ, Castagnino P, Bottaro DP, Roberts AB, Lechleider RJ. Smad2 transduces common signals from receptor serine-threonine and tyrosine kinases. Genes Dev 1998;12:1587-1592. (Pubitemid 28299510)
14. Mori S, Matsuzaki K, Yoshida K, Furukawa F, Tahashi Y, Yamagata H, Sekimoto G, Seki T, Matsui H, Nishizawa M, et al. TGF-beta and HGF transmit the signals through JNK-dependent Smad2/3 phosphorylation at the linker regions. Oncogene 2004;23:7416-7429. (Pubitemid 39382144)
15. Wang G, Long J, Matsuura I, He D, Liu F. The Smad3 linker region contains a transcriptional activation domain. Biochem J 2005;386:29-34. (Pubitemid 40289221)
16. Alcorn JF, Guala AS, van der Velden J, McElhinney B, Irvin CG, Davis RJ, Janssen-Heininger YM. Jun n-terminal kinase 1 regulates epithelial-to- mesenchymal transition induced by TGF-beta1. J Cell Sci 2008;121:1036-1045. (Pubitemid 351639422)
17. Alcorn JF, van der Velden J, Brown AL, McElhinney B, Irvin CG, Janssen-Heininger YM. c-Jun N-terminal kinase 1 is required for the development of pulmonary fibrosis. Am J Respir Cell Mol Biol 2009;40:422-432.
18. 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-beta-mediated pulmonary fibrosis. J Immunol 2004;173:2099-2108. (Pubitemid 38971648)
19. Roberts AB, Tian F, Byfield SD, Stuelten C, Ooshima A, Saika S, Flanders KC. Smad3 is key to TGF-beta-mediated epithelial-to-mesenchymal transition, fibrosis, tumor suppression and metastasis. Cytokine Growth Factor Rev 2006;17:19-27. (Pubitemid 43117513)
20. Wu R, Smith D. Continuous multiplication of rabbit tracheal epithelial cells in a defined, hormone-supplemented medium. In Vitro 1982;18:800-812. (Pubitemid 13166487)
21. Malkinson AM, Dwyer-Nield LD, Rice PL, Dinsdale D. Mouse lung epithelial cell lines - tools for the study of differentiation and the neoplastic phenotype. Toxicology 1997;123:53-100. (Pubitemid 27414556)
22. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 2006;174:175-183. (Pubitemid 44079853)
23. Venkov CD, Link AJ, Jennings JL, Plieth D, Inoue T, Nagai K, Xu C, Dimitrova YN, Rauscher FJ, Neilson EG. A proximal activator of transcription in epithelial-mesenchymal transition. J Clin Invest 2007;117:482-491. (Pubitemid 46203977)
24. 2-terminal kinase. Proc Natl Acad Sci USA 1997;94:7337-7342.
25. Lei K, Nimnual A, Zong WX, Kennedy NJ, Flavell RA, Thompson CB, Bar-Sagi D, Davis RJ. The bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol Cell Biol 2002;22:4929-4942.
26. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 2000;19:1745-1754. (Pubitemid 30204386)
27. 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.
28. Thuault S, Tan EJ, Peinado H, Cano A, Heldin CH, Moustakas A. HMGA2 and Smads co-regulate Snail1 expression during induction of epithelial-to- mesenchymal transition. J BiolChem2008;283:33437-33446.
29. 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)
30. Saika S, Kono-Saika S, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Flanders KC, Yoo J, Anzano M, Liu CY, et al. Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 2004;164:651-663. (Pubitemid 38364679)
31. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 2003;112:1486-1494. (Pubitemid 38056275)
32. Hackett TL, Warner SM, Stefanowicz D, Shaheen F, Pechkovsky DV, Murray LA, Argentieri R, Kicic A, Stick SM, Bai TR, et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-β1. Am J Respir Crit Care Med 2009;180:122-133.
33. Phanish MK, Wahab NA, Colville-Nash P, Hendry BM, Dockrell ME. The differential role of Smad2 and Smad3 in the regulation of profibrotic TGFbeta1 responses in human proximal-tubule epithelial cells. Biochem J 2006;393:601-607. (Pubitemid 43099100)
34. Hoot KE, Lighthall J, Han G, Lu SL, Li A, Ju W, Kulesz-Martin M, Bottinger E, Wang XJ. Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression. J Clin Invest 2008;118:2722-2732.
35. Runyan CE, Hayashida T, Hubchak S, Curley JF, Schnaper HW. Role of SARA (Smad anchor for receptor activation) in maintenance of epithelial cell phenotype. J Biol Chem 2009;284:25181-25189.
36. Verrecchia F, Tacheau C, Wagner EF, Mauviel A. A central role for the JNK pathway in mediating the antagonistic activity of pro-inflammatory cytokines against transforming growth factor-beta-driven Smad3/4-specific gene expression. J Biol Chem 2003;278:1585-1593. (Pubitemid 36801388)
37. Kamaraju AK, Roberts AB. Role of Rho/ROCK and p38 map kinase pathways in transforming growth factor-beta-mediated Smad-dependent growth inhibition of human breast carcinoma cells in vivo. J Biol Chem 2005;280:1024-1036.
38. Matsuura I, Wang G, He D, Liu F. Identification and characterization of ERK MAP kinase phosphorylation sites in Smad3. Biochemistry 2005;44:12546-12553. (Pubitemid 41324345)
39. Wrighton KH, Willis D, Long J, Liu F, Lin X, Feng XH. Small C-terminal domain phosphatases dephosphorylate the regulatory linker regions of Smad2 and Smad3 to enhance transforming growth factor-beta signaling. J Biol Chem 2006;281:38365-38375. (Pubitemid 46041960)
40. Jablonska E, Markart P, Zakrzewicz D, Preissner KT, Wygrecka M. Transforming growth factor-beta1 induces expression of human coagulation factor XII via Smad3 and JNK signaling pathways in human lung fibroblasts. J Biol Chem 2010;285:11638-11651.
41. Dennler S, Prunier C, Ferrand N, Gauthier JM, Atfi A. c-Jun inhibits transforming growth factor beta-mediated transcription by repressing Smad3 transcriptional activity. J Biol Chem 2000;275:28858-28865.
42. Eferl R, Hasselblatt P, Rath M, Popper H, Zenz R, Komnenovic V, Idarraga MH, Kenner L, Wagner EF. Development of pulmonary fibrosis through a pathway involving the transcription factor FRA-2/AP-1. Proc Natl Acad Sci USA 2008;105:10525-10530.
43. Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, Kitani A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med 2006;12:99-106. (Pubitemid 43050083)
44. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998;17:3091-3100.
45. Ross S, Hill CS. How the Smads regulate transcription. Int J Biochem Cell Biol 2008;40:383-408. (Pubitemid 351241229)
46. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J, Pietras K, Virtanen I, Philipson L, Leopold PL, et al. A Snail1-Smad3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 2009;11:943-950.
47. Masszi A, Speight P, Charbonney E, Lodyga M, Nakano H, Szaszi K, Kapus A. Fate-determining mechanisms in epithelial-myofibroblast transition: major inhibitory role for Smad3. J Cell Biol 2010;188:383-399.
48. Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F, Ifedigbo E, Xu X, Oury TD, Kaminski N, et al. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 2006;203:2895-2906. (Pubitemid 46026167)
49. Yoshida K, Kuwano K, Hagimoto N, Watanabe K, Matsuba T, Fujita M, Inoshima I, Hara N. MAP kinase activation and apoptosis in lung tissues from patients with idiopathic pulmonary fibrosis. J Pathol 2002;198:388-396. (Pubitemid 35277390)
50. Shi-Wen X, Rodriguez-Pascual F, Lamas S, Holmes A, Howat S, Pearson JD, Dashwood MR, du Bois RM, Denton CP, Black CM, et al. Constitutive Alk5-independent c-Jun N-terminal kinase activation contributes to endothelin-1 overexpression in pulmonary fibrosis: evidence of an autocrine endothelin loop operating through the endothelin A and B receptors. Mol Cell Biol 2006;26:5518-5527.