TGF-β-activated kinase 1 (Tak1) mediates agonist-induced smad activation and linker region phosphorylation in embryonic craniofacial neural crest-derived cells

Journal of Biological Chemistry

Volumn 288, Issue 19, 2013, Pages 13467-13480

  Yumoto, Kenji ^a   Thomas, Penny S ^a   Lane, Jamie ^a   Matsuzaki, Kouichi ^b   Inagaki, Maiko ^c   Ninomiya Tsuji, Jun ^c   Scott, Gregory J ^d   Ray, Manas K ^d   Ishii, Mamoru ^e   Maxson, Robert ^e   Mishina, Yuji ^a   Kaartinen, Vesa ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIRTH DEFECTS; CRANIOFACIAL; LINKER REGION; MESENCHYMAL CELLS;

PHOSPHORYLATION;

CELL SIGNALING;

BONE MORPHOGENETIC PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; SMAD PROTEIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINEAGE; CLEFT PALATE; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FEMALE; GENE; GENE DELETION; INTRACELLULAR SIGNALING; MALE; MANDIBLE HYPOPLASIA; MAXILLA HYPOPLASIA; MEDIATOR; MESENCHYME CELL; MOLECULAR MECHANICS; MOUSE; NEURAL CREST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; SKULL MALFORMATION; TAK1 GENE;

BONE MORPHOGENETIC PROTEIN (BMP); CRANIOFACIAL BIRTH DEFECTS; CRANIOFACIAL DEVELOPMENT; EMBRYO; LINKER REGION PHOSPHORYLATION; SMAD TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA (TGFBETA);

AMINO ACID MOTIFS; ANIMALS; CELLS, CULTURED; CLEFT PALATE; ECTODERM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAD; MALE; MANDIBLE; MAP KINASE KINASE KINASES; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; NEURAL CREST; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD PROTEINS, RECEPTOR-REGULATED; TGF-BETA SUPERFAMILY PROTEINS; WNT1 PROTEIN;

EID: 84877705727     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.431775     Document Type: Article

References (47)

1. Blobe, G. C., Schiemann, W. P., and Lodish, H. F. (2000) Role of transforming growth factor β in human disease. N. Engl. J. Med. 342, 1350-1358
2. Massagué, J. (1998) TGF-β signal transduction. Annu. Rev. Biochem. 67, 753-791
3. Derynck, R., Zhang, Y., and Feng, X. H. (1998) Smads. Transcriptional activators of TGF-β responses. Cell 95, 737-740
4. Derynck, R., and Zhang, Y. E. (2003) Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577-584
5. Daly, A. C., Randall, R. A., and Hill, C. S. (2008) Transforming growth factor β-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Mol. Cell. Biol. 28, 6889-6902
6. Matsuzaki, K., Kitano, C., Murata, M., Sekimoto, G., Yoshida, K., Uemura, Y., Seki, T., Taketani, S., Fujisawa, J., and Okazaki, K. (2009) Smad2 and Smad3 phosphorylated at both linker and COOH-terminal regions transmit malignant TGF-β signal in later stages of human colorectal cancer. Cancer Res. 69, 5321-5330
7. Alarcón, C., Zaromytidou, A. I., Xi, Q., Gao, S., Yu, J., Fujisawa, S., Barlas, A., Miller, A. N., Manova-Todorova, K., Macias, M. J., Sapkota, G., Pan, D., and Massagué, J. (2009) Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways. Cell 139, 757-769
8. Kretzschmar, M., Liu, F., Hata, A., Doody, J., and Massagué, J. (1997) The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995
9. Aragón, E., Goerner, N., Zaromytidou, A. I., Xi, Q., Escobedo, A., Massagué, J., and Macias, M. J. (2011)ASmad action turnover switch operated by WW domain readers of a phosphoserine code. Genes Dev. 25, 1275-1288
10. Gao, S., Alarcón, C., Sapkota, G., Rahman, S., Chen, P. Y., Goerner, N., Macias, M. J., Erdjument-Bromage, H., Tempst, P., and Massagué, J. (2009) Ubiquitin ligase Nedd4L targets activated Smad2/3 to limit TGF-β signaling. Mol. Cell 36, 457-468
11. Sorrentino, A., Thakur, N., Grimsby, S., Marcusson, A., von Bulow, V., Schuster, N., Zhang, S., Heldin, C. H., and Landström, M. (2008) The type I TGF-β receptor engages TRAF6 to activate TAK1 in a receptor kinaseindependent manner. Nat. Cell Biol. 10, 1199-1207
12. Yamashita, M., Fatyol, K., Jin, C., Wang, X., Liu, Z., and Zhang, Y. E. (2008) TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-β. Mol. Cell 31, 918-924
13. Wang, C., Deng, L., Hong, M., Akkaraju, G. R., Inoue, J., and Chen, Z. J. (2001) TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351
14. Gingery, A., Bradley, E. W., Pederson, L., Ruan, M., Horwood, N. J., and Oursler, M. J. (2008) TGF-β coordinately activates TAK1/MEK/AKT/NFκB and SMAD pathways to promote osteoclast survival. Exp. Cell Res. 314, 2725-2738
15. Hoffmann, A., Preobrazhenska, O., Wodarczyk, C., Medler, Y., Winkel, A., Shahab, S., Huylebroeck, D., Gross, G., and Verschueren, K. (2005) Transforming growth factor-β-activated kinase-1 (TAK1), a MAP3K, interacts with Smad proteins and interferes with osteogenesis in murine mesenchymal progenitors. J. Biol. Chem. 280, 27271-27283
16. Holm, T. M., Habashi, J. P., Doyle, J. J., Bedja, D., Chen, Y., van Erp, C., Lindsay, M. E., Kim, D., Schoenhoff, F., Cohn, R. D., Loeys, B. L., Thomas, C. J., Patnaik, S., Marugan, J. J., Judge, D. P., and Dietz, H. C. (2011) Noncanonical TGFβ signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science 332, 358-361
17. Iwata, J., Hacia, J. G., Suzuki, A., Sanchez-Lara, P. A., Urata, M., and Chai, Y. (2012) Modulation of noncanonical TGF-β signaling prevents cleft palate in Tgfbr2 mutant mice. J. Clin. Invest. 122, 873-885
18. Cardoso, S., Robertson, S. P., and Daniel, P. B. (2012) TGFBR1 mutations associated with Loeys-Dietz syndrome are inactivating. J. Recept. Signal. Transduct. Res. 32, 150-155
19. Loeys, B. L., Chen, J., Neptune, E. R., Judge, D. P., Podowski, M., Holm, T., Meyers, J., Leitch, C. C., Katsanis, N., Sharifi, N., Xu, F. L., Myers, L. A., Spevak, P. J., Cameron, D. E., De Backer, J., Hellemans, J., Chen, Y., Davis, E. C., Webb, C. L., Kress, W., Coucke, P., Rifkin, D. B., De Paepe, A. M., and Dietz, H. C. (2005) A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat. Genet. 37, 275-281
20. Larsson, J., Goumans, M. J., Sjöstrand, L. J., van Rooijen, M. A., Ward, D., Levéen, P., Xu, X., ten Dijke, P., Mummery, C. L., and Karlsson, S. (2001) Abnormal angiogenesis but intact hematopoietic potential in TGF-β type I receptor-deficient mice. EMBO J. 20, 1663-1673
21. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K., and McMahon, A. P. (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8, 1323-1326
22. Yu, L., Gu, S., Alappat, S., Song, Y., Yan, M., Zhang, X., Zhang, G., Jiang, Y., Zhang, Z., Zhang, Y., and Chen, Y. (2005) Shox2-deficient mice exhibit a rare type of incomplete clefting of the secondary palate. Development 132, 4397-4406
23. Liu, W., Lan, Y., Pauws, E., Meester-Smoor, M. A., Stanier, P., Zwarthoff, E. C., and Jiang, R. (2008) The Mn1 transcription factor acts upstream of Tbx22 and preferentially regulates posterior palate growth in mice. Development 135, 3959-3968
24. Bellusci, S., Furuta, Y., Rush, M. G., Henderson, R., Winnier, G., and Hogan, B. L. (1997) Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124, 53-63
25. Dudas, M., Nagy, A., Laping, N. J., Moustakas, A., and Kaartinen, V. (2004) Tgf-β3-induced palatal fusion is mediated by Alk-5/Smad pathway. Dev. Biol. 266, 96-108
26. Harlow, E., and Lane, D. (1988) Antibodies: A Laboratory Manual, pp. 481-482, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
27. Thomas, P. S., Kim, J., Nunez, S., Glogauer, M., and Kaartinen, V. (2010) Neural crest cell-specific deletion of Rac1 results in defective cell-matrix interactions and severe craniofacial and cardiovascular malformations. Dev. Biol. 340, 613-625
28. Nagy, A., Gertsenstein, M., Vintersten, K., and Behringer, R. (2003) Manipulating the Mouse Embryo: A Laboratory Manual, pp. 687-691, 3rd Ed., Academic Press, New York
29. Ishii, M., Arias, A. C., Liu, L., Chen, Y. B., Bronner, M. E., and Maxson, R. E. (2012) A stable cranial neural crest cell line from mouse. Stem Cells Dev. 21, 3069-3080
30. Zhang, Z., Song, Y., Zhao, X., Zhang, X., Fermin, C., and Chen, Y. (2002) Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. Development 129, 4135-4146
31. Hilliard, S. A., Yu, L., Gu, S., Zhang, Z., and Chen, Y. P. (2005) Regional regulation of palatal growth and patterning along the anterior-posterior axis in mice. J. Anat. 207, 655-667
32. Liu, W., Sun, X., Braut, A., Mishina, Y., Behringer, R. R., Mina, M., and Martin, J. F. (2005) Distinct functions for Bmp signaling in lip and palate fusion in mice. Development 132, 1453-1461
33. Han, J., Mayo, J., Xu, X., Li, J., Bringas, P., Jr., Maas, R. L., Rubenstein, J. L., and Chai, Y. (2009) Indirect modulation of Shh signaling by Dlx5 affects the oral-nasal patterning of palate and rescues cleft palate in Msx1-null mice. Development 136, 4225-4233
34. Rice, R., Spencer-Dene, B., Connor, E. C., Gritli-Linde, A., McMahon, A. P., Dickson, C., Thesleff, I., and Rice, D. P. (2004) Disruption of Fgf10/Fgfr2b-coordinated epithelial-mesenchymal interactions causes cleft palate. J. Clin. Invest. 113, 1692-1700
35. Baek, J. A., Lan, Y., Liu, H., Maltby, K. M., Mishina, Y., and Jiang, R. (2011) Bmpr1a signaling plays critical roles in palatal shelf growth and palatal bone formation. Dev. Biol. 350, 520-531
36. Massagué, J., Seoane, J., and Wotton, D. (2005) Smad transcription factors. Genes Dev. 19, 2783-2810
37. Wang, G., Matsuura, I., He, D., and Liu, F. (2009) Transforming growth factor-β-inducible phosphorylation of Smad3. J. Biol. Chem. 284, 9663-9673
38. Wrighton, K. H., and Feng, X. H. (2008) To (TGF)β or not to (TGF)β. Fine-tuning of Smad signaling via post-translational modifications. Cell. Signal. 20, 1579-1591
39. Yamaguchi, K., Shirakabe, K., Shibuya, H., Irie, K., Oishi, I., Ueno, N., Taniguchi, T., Nishida, E., and Matsumoto, K. (1995) Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 270, 2008-2011
40. Ito, Y., Yeo, J. Y., Chytil, A., Han, J., Bringas, P., Jr., Nakajima, A., Shuler, C. F., Moses, H. L., and Chai, Y. (2003) Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 130, 5269-5280
41. Dudas, M., Kim, J., Li, W. Y., Nagy, A., Larsson, J., Karlsson, S., Chai, Y., and Kaartinen, V. (2006) Epithelial and ectomesenchymal role of the type I TGF-β receptor ALK5 during facial morphogenesis and palatal fusion. Dev. Biol. 296, 298-314
42. Iwata, J., Tung, L., Urata, M., Hacia, J. G., Pelikan, R., Suzuki, A., Ramenzoni, L., Chaudhry, O., Parada, C., Sanchez-Lara, P. A., and Chai, Y. (2012) Fibroblast growth factor 9 (FGF9)-pituitary homeobox 2 (PITX2) pathway mediates transforming growth factor β (TGFβ) signaling to regulate cell proliferation in palatal mesenchyme during mouse palatogenesis. J. Biol. Chem. 287, 2353-2363
43. Economou, A. D., Ohazama, A., Porntaveetus, T., Sharpe, P. T., Kondo, S., Basson, M. A., Gritli-Linde, A., Cobourne, M. T., and Green, J. B. (2012) Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat. Genet. 44, 348-351
44. Song, Z., Liu, C., Iwata, J., Gu, S., Suzuki, A., Sun, C., He, W., Shu, R., Li, L., Chai, Y., and Chen, Y. (2013) Mice with Tak1 deficiency in neural crest lineage exhibit cleft palate associated with abnormal tongue development. J. Biol. Chem. 288, 10440-10450
45. Shim, J. H., Greenblatt, M. B., Xie, M., Schneider, M. D., Zou, W., Zhai, B., Gygi, S., and Glimcher, L. H. (2009) TAK1 is an essential regulator of BMP signalling in cartilage. EMBO J. 28, 2028-2041
46. Hough, C., Radu, M., and Doré, J. J. (2012) Tgf-β induced Erk phosphorylation of Smad linker region regulates Smad signaling. PLoS One 7, e42513
47. Cohen-Solal, K. A., Merrigan, K. T., Chan, J. L., Goydos, J. S., Chen, W., Foran, D. J., Liu, F., Lasfar, A., and Reiss, M. (2011) Constitutive Smad linker phosphorylation in melanoma. A mechanism of resistance to transforming growth factor-β-mediated growth inhibition. Pigment Cell Melanoma Res. 24, 512-524