TAK1 plays a major role in growth factor-induced phenotypic modulation of airway smooth muscle

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 301, Issue 5, 2011, Pages

  Pera, Tonio ^a   Sami, Riham ^a   Zaagsma, Johan ^a   Meurs, Herman ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Airway smooth muscle contractility; Airway smooth muscle proliferation; Asthma; Chronic obstructive pulmonary disease; Mitogen activated protein kinase kinase kinase family

Indexed keywords

7 OXOZEAENOL; ALPHA SMOOTH MUSCLE ACTIN; BOVINE SERUM ALBUMIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATELET DERIVED GROWTH FACTOR; PROTEIN SERINE THREONINE KINASE INHIBITOR; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOVINE TRACHEAL SMOOTH MUSCLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; DRUG INHIBITION; HUMAN; HUMAN CELL; HUMAN TRACHEAL SMOOTH MUSCLE; LUNG ALVEOLUS CELL; LUNG ALVEOLUS WALL; MUSCLE CONTRACTILITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACTINS; AIRWAY REMODELING; ANIMALS; ASTHMA; BLOTTING, WESTERN; CATTLE; CELL PROLIFERATION; DNA REPLICATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE KINASE KINASES; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PLASMIDS; PLATELET-DERIVED GROWTH FACTOR; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SIGNAL TRANSDUCTION; TRACHEA; TRANSFECTION; ZEARALENONE;

EID: 80055119714     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00017.2011     Document Type: Article

References (54)

1. Amishima M, Munakata M, Nasuhara Y, Sato A, Takahashi T, Homma Y, Kawakami Y. Expression of epidermal growth factor and epidermal growth factor receptor immunoreactivity in the asthmatic human airway. Am J Respir Crit Care Med 157: 1907-1912, 1998.
2. Aubert JD, Hayashi S, Hards J, Bai TR, Pare PD, Hogg JC. Plateletderived growth factor and its receptor in lungs from patients with asthma and chronic airflow obstruction. Am J Physiol Lung Cell Mol Physiol 266: L655-L663, 1994.
3. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
4. Bradham CA, Hatano E, Brenner DA. Dominant-negative TAK1 induces c-Myc and G0 exit in liver. Am J Physiol Gastrointest Liver Physiol 281: G1279-G1289, 2001.
5. Chen L, Xiong S, She H, Lin SW, Wang J, Tsukamoto H. Iron causes interactions of TAK1, p21ras, and phosphatidylinositol 3-kinase in caveolae to activate IkB kinase in hepatic macrophages. J Biol Chem 282: 5582-5588, 2007.
6. Dekkers BG, Schaafsma D, Nelemans SA, Zaagsma J, Meurs H. Extracellular matrix proteins differentially regulate airway smooth muscle phenotype and function. Am J Physiol Lung Cell Mol Physiol 292: L1405-L1413, 2007.
7. Dekkers BGJ, Maarsingh H, Meurs H, Gosens R. Airway structural components drive airway smooth muscle remodeling in asthma. Proc Am Thorac Soc 6: 683-692, 2009.
8. Ear T, Fortin CF, Simard FA, McDonald PP. Constitutive association of TGF-β-activated kinase 1 with the IκB kinase complex in the nucleus and cytoplasm of human neutrophils and its impact on downstream processes. J Immunol 184: 3897-3906, 2010.
9. Ebina M, Takahashi T, Chiba T, Motomiya M. Cellular hypertrophy and hyperplasia of airway smooth muscles underlying bronchial asthma. A 3-D morphometric study. Am Rev Respir Dis 148: 720-726, 1993.
10. Eggen BJ, Benus GF, Folkertsma S, Jonk LJ, Kruijer W. TAK1 activation of the mouse JunB promoter is mediated through a CCAAT box and NF-Y. FEBS Lett 506: 267-271, 2001.
11. Gosens R, Meurs H, Bromhaar MM, McKay S, Nelemans SA, Zaagsma J. Functional characterization of serum- and growth factorinduced phenotypic changes in intact bovine tracheal smooth muscle. Br J Pharmacol 137: 459-466, 2002.
12. Gosens R, Nelemans SA, Grootte Bromhaar MM, McKay S, Zaagsma J, Meurs H. Muscarinic M3-receptors mediate cholinergic synergism ofmitogenesis in airway smooth muscle. Am J Respir Cell Mol Biol 28: 257-262, 2003.
13. Gosens R, Schaafsma D, Meurs H, Zaagsma J, Nelemans SA. Role of Rho-kinase in maintaining airway smooth muscle contractile phenotype. Eur J Pharmacol 483: 71-78, 2004.
14. Gosens R, Roscioni SS, Dekkers BGJ, Pera T, Schmidt M, Schaafsma D, Zaagsma J, Meurs H. Pharmacology of airway smooth muscle proliferation. Eur J Pharmacol 585: 385-397, 2008.
15. Halayko AJ, Salari H, Ma X, Stephens NL. Markers of airway smooth muscle cell phenotype. Am J Physiol Lung Cell Mol Physiol 270: L1040-L1051, 1996.
16. Halayko AJ, Solway J. Molecular mechanisms of phenotypic plasticity in smooth muscle cells. J Appl Physiol 90: 358-368, 2001.
17. Hirst SJ, Twort CH, Lee TH. Differential effects of extracellular matrix proteins on human airway smooth muscle cell proliferation and phenotype. Am J Respir Cell Mol Biol 23: 335-344, 2000.
18. Irie T, Muta T, Takeshige K. TAK1 mediates an activation signal from toll-like receptor(s) to nuclear factor-κB in lipopolysaccharide-stimulated macrophages. FEBS Lett 467: 160-164, 2000.
19. Jadrich JL, O'Connor MB, Coucouvanis E. Expression of TAK1, a mediator of TGF-β and BMP signaling, during mouse embryonic development. Gene Expr Patterns 3: 131-134, 2003.
20. Jadrich JL, O'Connor MB, Coucouvanis E. The TGFb activated kinase TAK1 regulates vascular development in vivo. Development 133: 1529-1541, 2006.
21. Kale VP. Differential activation of MAPK signaling pathways by TGF-b1 forms the molecular mechanism behind its dose-dependent bidirectional effects on hematopoiesis. Stem Cells Dev 13: 27-38, 2004.
22. Kale VP, Vaidya AA. Molecular mechanisms behind the dose-dependent differential activation of MAPK pathways induced by transforming growth actor-beta1 in hematopoietic cells. Stem Cells Dev 13: 536-547, 2004.
23. Karpova AY, Abe MK, Li J, Liu PT, Rhee JM, Kuo WL, Hershenson B. MEK1 is required for PDGF-induced ERK activation and DNA synthesis in tracheal myocytes. Am J Physiol Lung Cell Mol Physiol 272: L558-L565, 1997.
24. Kelleher MD, Abe MK, Chao TS, Jain M, Green JM, Solway J, Rosner MR, Hershenson MB. Role of MAP kinase activation in bovine tracheal smooth muscle mitogenesis. Am J Physiol Lung Cell Mol Physiol 268: L894-L901, 1995.
25. Komatsu Y, Shibuya H, Takeda N, Ninomiya-Tsuji J, Yasui T, Miyado K, Sekimoto T, Ueno N, Matsumoto K, Yamada G. Targeted disruption of the Tab1 gene causes embryonic lethality and defects in cardiovascular and lung morphogenesis. Mech Dev 119: 239-249, 2002.
26. Krymskaya VP, Orsini MJ, Eszterhas AJ, Brodbeck KC, Benovic JL, Panettieri RA Jr, Penn RB. Mechanisms of proliferation synergy by receptor tyrosine kinase and G protein-coupled receptor activation in human airway smooth muscle. Am J Respir Cell Mol Biol 23: 546-554, 2000.
27. Lee JH, Johnson PR, Roth M, Hunt NH, Black JL. ERK activation and mitogenesis in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 280: L1019-L1029, 2001.
28. Matsumoto-Ida M, Takimoto Y, Aoyama T, Akao M, Takeda T, Kita T. Activation of TGF-β1-TAK1-p38 MAPK pathway in spared cardiomyocytes is involved in left ventricular remodeling after myocardial infarction in rats. Am J Physiol Heart Circ Physiol 290: H709-H715, 2006.
29. Ninomiya-Tsuji J, Kajino T, Ono K, Ohtomo T, Matsumoto M, Shiina M, Mihara M, Tsuchiya M, Matsumoto K. A resorcylic acid lactone, 5Z-7-oxozeaenol, prevents inflammation by inhibiting the catalytic activity of TAK1 MAPK kinase kinase. J Biol Chem 278: 18485-18490, 2003.
30. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue Ji Cao Z, Matsumoto K. The kinase TAK1 can activate the NIK-IκB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398: 252-256, 1999.
31. Nishimura M, Shin MS, Singhirunnusorn P, Suzuki S, Kawanishi M, Koizumi K, Saiki I, Sakurai H. TAK1-mediated serine/threonine phosphorylation of EGFR via p38/ERK: NF-κB-independent survival pathways in TNF-α signaling. Mol Cell Biol 29: 5529-5539, 2009.
32. Ohkawara B, Shirakabe K, Hyodo-Miura J, Matsuo R, Ueno N, Matsumoto K, Shibuya H. Role of the TAK1-NLK-STAT3 pathway in TGF-b-mediated mesoderm induction. Genes Dev 18: 381-386, 2004.
33. Omori E, Matsumoto K, Zhu S, Smart RC, Ninomiya-Tsuji J. Ablation of TAK1 upregulates reactive oxygen species and selectively kills tumor cells. Cancer Res 70: 8417-8425, 2010.
34. Orsini MJ, Krymskaya VP, Eszterhas AJ, Benovic JL, Panettieri RA Jr, Penn RB. MAPK superfamily activation in human airway smooth muscle: mitogenesis requires prolonged p42/p44 activation. Am J Physiol Lung Cell Mol Physiol 277: L479-L488, 1999.
35. Pera T, Gosens R, Lesterhuis AH, Sami R, Toorn M, Zaagsma J, Meurs H. Cigarette smoke and lipopolysaccharide induce a proliferative airway smooth muscle phenotype. Respir Res 11: 48, 2010.
36. Postma DS, Kerstjens HA. Characteristics of airway hyperresponsiveness in asthma and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 158: S187-S192, 1998.
37. Rawlins P, Mander T, Sadeghi R, Hill S, Gammon G, Foxwell B, Wrigley S, Moore M. Inhibition of endotoxin-induced TNF-α production in macrophages by 5Z-7-oxo-zeaenol and other fungal resorcylic acid lactones. Int J Immunopharmacol 21: 799-814, 1999.
38. Reijmerink NE, Bottema RW, Kerkhof M, Gerritsen J, Stelma FF, Thijs C, van Schayck CP, Smit HA, Brunekreef B, Koppelman GH, Postma DS. TLR-related pathway analysis: novel gene-gene interactions in the development of asthma and atopy. Allergy 65: 199-207, 2010.
39. Safina A, Ren MQ, Vandette E, Bakin AV. TAK1 is required for TGF-β1-mediated regulation of matrix metalloproteinase-9 and metastasis. Oncogene 27: 1198-1207, 2007.
40. Sakurai H, Miyoshi H, Toriumi W, Sugita T. Functional interactions of transforming growth factor β-activated kinase 1 with IkB kinases to stimulate NF-kB activation. J Biol Chem 274: 10641-10648, 1999.
41. Sakurai H, Shigemori N, Hasegawa K, Sugita T. TGF-β-activated kinase 1 stimulates NF-κB activation by an NF-κB-inducing kinaseindependent mechanism. Biochem Biophys Res Commun 243: 545-549, 1998.
42. Sato S, Sanjo H, Takeda K, Ninomiya-Tsuji J, Yamamoto M, Kawai T, Matsumoto K, Takeuchi O, Akira S. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 6: 1087-1095, 2005.
43. Sato S, Sanjo H, Tsujimura T, Ninomiya-Tsuji J, Yamamoto M, Kawai T, Takeuchi O, Akira S. TAK1 is indispensable for development of T cells and prevention of colitis by the generation of regulatory T cells. Int Immunol 18: 1405-1411, 2006.
44. Schaafsma D, McNeill KD, Stelmack GL, Gosens R, Baarsma HA, Dekkers BG, Frohwerk E, Penninks JM, Sharma P, Ens KM, Nelemans SA, Zaagsma J, Halayko AJ, Meurs H. Insulin increases the expression of contractile phenotypic markers in airway smooth muscle. Am J Physiol Cell Physiol 293: C429-C439, 2007.
45. Shim JH, Xiao C, Paschal AE, Bailey ST, Rao P, Hayden MS, Lee KY, Bussey C, Steckel M, Tanaka N, Yamada G, Akira S, Matsumoto K, Ghosh S. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 19: 2668-2681, 2005.
46. Shim JH, Greenblatt MB, Xie M, Schneider MD, Zou W, Zhai B, Gygi S, Glimcher LH. TAK1 is an essential regulator of BMP signalling in cartilage. EMBO J 28: 2028-2041, 2009.
47. Takeda N, Kondo M, Ito S, Ito Y, Shimokata K, Kume H. Role of RhoA inactivation in reduced cell proliferation of human airway smooth muscle by simvastatin. Am J Respir Cell Mol Biol 35: 722-729, 2006.
48. Takehana K, Sato S, Kobayasi T, Maeda T. A radicicol-related macrocyclic nonaketide compound, antibiotic LL-Z1640-2, inhibits the JNK/ p38 pathways in signal-specific manner. Biochem Biophys Res Commun 257: 19-23, 1999.
49. Terada Y, Nakashima O, Inoshita S, Kuwahara M, Sasaki S, Marumo F. TGF-β-activating kinase-1 inhibits cell cycle and expression of cyclin D1 and A in LLC-PK1 cells. Kidney Int 56: 1378-1390, 1999.
50. Tomlinson PR, Wilson JW, Stewart AG. Inhibition by salbutamol of the proliferation of human airway smooth muscle cells grown in culture. Br J Pharmacol 111: 641-647, 1994.
51. Wan YY, Chi H, Xie M, Schneider MD, Flavell RA. The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat Immunol 7: 851-858, 2006.
52. Woodruff PG, Dolganov GM, Ferrando RE, Donnelly S, Hays SR, Solberg OD, Carter R, Wong HH, Cadbury PS, Fahy JV. Hyperplasia of smooth muscle in mild to moderate asthma without changes in cell size or gene expression. Am J Respir Crit Care Med 169: 1001-1006, 2004.
53. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270: 2008-2011, 1995.
54. Zhang D, Gaussin V, Taffet GE, Belaguli NS, Yamada M, Schwartz RJ, Michael LH, Overbeek PA, Schneider MD. TAK1 is activated in the myocardium after pressure overload and is sufficient to provoke heart failure in transgenic mice. Nat Med 6: 556-563, 2000.