Smad4-irf6 genetic interaction and TGFβ-mediated IRF6 signaling cascade are crucial for palatal fusion in mice

Development (Cambridge)

Volumn 140, Issue 6, 2013, Pages 1220-1230

  Iwata, Jun ichi ^a   Suzuki, Akiko ^a   Pelikan, Richard C ^a   Ho, Thach Vu ^a   Sanchez Lara, Pedro A ^b,c   Urata, Mark ^a,c   Dixon, Michael J ^d   Chai, Yang ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

IRF6; Mouse; Palatal fusion; TGF

Indexed keywords

INTERFERON REGULATORY FACTOR 6; PROTEIN P21; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL GENETICS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPITHELIUM; GENE INTERACTION; GENE SEQUENCE; HAPLOINSUFFICIENCY; MOUSE; NONHUMAN; ORGANOGENESIS; PALATE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PTERYGIUM; SIGNAL TRANSDUCTION; VAN DER WOUDE SYNDROME;

ANIMALS; ANIMALS, NEWBORN; CELL FUSION; CELLS, CULTURED; EMBRYO, MAMMALIAN; EPISTASIS, GENETIC; FEMALE; HUMANS; INTERFERON REGULATORY FACTORS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGANOGENESIS; PALATE; PREGNANCY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84874548797     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.089615     Document Type: Article

References (55)

1. Andrabi, S., Bekheirnia, M. R., Robbins-Furman, P., Lewis, R. A., Prior, T. W. and Potocki, L. (2011). SMAD4 mutation segregating in a family with juvenile polyposis, aortopathy, and mitral valve dysfunction. Am. J. Med. Genet. A. 155, 1165-1169.
2. Black, B. L. and Olson, E. N. (1998). Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14, 167-196.
3. Cai, B. H., Chao, C. F., Lu, M. H., Lin, H. C. and Chen, J. Y. (2012). A half-site of the p53-binding site on the keratin 14 promoter is specifically activated by p63. J. Biochem. 152, 99-110.
4. Chen, R. H., Su, Y. H., Chuang, R. L. and Chang, T. Y. (1998). Suppression of transforming growth factor-beta-induced apoptosis through a phosphatidylinositol 3-kinase/Akt-dependent pathway. Oncogene 17, 1959-1968.
5. Cuervo, R. and Covarrubias, L. (2004). Death is the major fate of medial edge epithelial cells and the cause of basal lamina degradation during palatogenesis. Development 131, 15-24.
6. Denissova, N. G., Pouponnot, C., Long, J., He, D. and Liu, F. (2000). Transforming growth factor beta -inducible independent binding of SMAD to the Smad7 promoter. Proc. Natl. Acad. Sci. USA 97, 6397-6402.
7. Dixon, M. J., Marazita, M. L., Beaty, T. H. and Murray, J. C. (2011). Cleft lip and palate: understanding genetic and environmental influences. Nat. Rev. Genet. 12, 167-178.
8. el-Deiry, W. S., Kern, S. E., Pietenpol, J. A., Kinzler, K. W. and Vogelstein, B. (1992). Definition of a consensus binding site for p53. Nat. Genet. 1, 45-49.
9. Fakhouri, W. D., Rhea, L., Du, T., Sweezer, E., Morrison, H., Fitzpatrick, D., Yang, B., Dunnwald, M. and Schutte, B. C. (2012). MCS9.7 enhancer activity is highly, but not completely, associated with expression of Irf6 and p63. Dev. Dyn. 241, 340-349.
10. Ferretti, E., Li, B., Zewdu, R., Wells, V., Hebert, J. M., Karner, C., Anderson, M. J., Williams, T., Dixon, J., Dixon, M. J. et al. (2011). A conserved Pbx-Wnt- p63-Irf6 regulatory module controls face morphogenesis by promoting epithelial apoptosis. Dev. Cell 21, 627-641.
11. Fujii, Y., Shimizu, T., Kusumoto, M., Kyogoku, Y., Taniguchi, T. and Hakoshima, T. (1999). Crystal structure of an IRF-DNA complex reveals novel DNA recognition and cooperative binding to a tandem repeat of core sequences. EMBO J. 18, 5028-5041.
12. Funato, N., Nakamura, M., Richardson, J. A., Srivastava, D. and Yanagisawa, H. (2012). Tbx1 regulates oral epithelial adhesion and palatal development. Hum. Mol. Genet. 21, 2524-2537.
13. Gallione, C. J., Richards, J. A., Letteboer, T. G., Rushlow, D., Prigoda, N. L., Leedom, T. P., Ganguly, A., Castells, A., Ploos van Amstel, J. K., Westermann, C. J. et al. (2006). SMAD4 mutations found in unselected HHT patients. J. Med. Genet. 43, 793-797.
14. Giehl, K., Seidel, B., Gierschik, P., Adler, G. and Menke, A. (2000). TGFbeta1 represses proliferation of pancreatic carcinoma cells which correlates with Smad4-independent inhibition of ERK activation. Oncogene 19, 4531-4541.
15. Han, J. and Molkentin, J. D. (2000). Regulation of MEF2 by p38 MAPK and its implication in cardiomyocyte biology. Trends Cardiovasc. Med. 10, 19-22.
16. He, F., Xiong, W., Wang, Y., Li, L., Liu, C., Yamagami, T., Taketo, M. M., Zhou, C. and Chen, Y. (2011). Epithelial Wnt/β-catenin signaling regulates palatal shelf fusion through regulation of Tgfβ3 expression. Dev. Biol. 350, 511-519.
17. Hocevar, B. A., Brown, T. L. and Howe, P. H. (1999). TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4- independent pathway. EMBO J. 18, 1345-1356.
18. Hu, P. P., Shen, X., Huang, D., Liu, Y., Counter, C. and Wang, X. F. (1999). The MEK pathway is required for stimulation of p21(WAF1/CIP1) by transforming growth factor-beta. J. Biol. Chem. 274, 35381-35387.
19. Ingraham, C. R., Kinoshita, A., Kondo, S., Yang, B., Sajan, S., Trout, K. J., Malik, M. I., Dunnwald, M., Goudy, S. L., Lovett, M. et al. (2006). Abnormal skin, limb and craniofacial morphogenesis in mice deficient for interferon regulatory factor 6 (Irf6). Nat. Genet. 38, 1335-1340.
20. 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.
21. Iwata, J., Ezaki, J., Komatsu, M., Yokota, S., Ueno, T., Tanida, I., Chiba, T., Tanaka, K. and Kominami, E. (2006). Excess peroxisomes are degraded by autophagic machinery in mammals. J. Biol. Chem. 281, 4035-4041.
22. Iwata, J., Hosokawa, R., Sanchez-Lara, P. A., Urata, M., Slavkin, H. and Chai, Y. (2010). Transforming growth factor-beta regulates basal transcriptional regulatory machinery to control cell proliferation and differentiation in cranial neural crest-derived osteoprogenitor cells. J. Biol. Chem. 285, 4975-4982.
23. Iwata, J., Parada, C. and Chai, Y. (2011). The mechanism of TGF-β signaling during palate development. Oral Dis. 17, 733-744.
24. 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.
25. Kang, J. S., Liu, C. and Derynck, R. (2009). New regulatory mechanisms of TGF- beta receptor function. Trends Cell Biol. 19, 385-394.
26. Koillinen, H., Lahermo, P., Rautio, J., Hukki, J., Peyrard-Janvid, M. and Kere, J. (2005). A genome-wide scan of non-syndromic cleft palate only (CPO) in Finnish multiplex families. J. Med. Genet. 42, 177-184.
27. Kondo, S., Schutte, B. C., Richardson, R. J., Bjork, B. C., Knight, A. S., Watanabe, Y., Howard, E., de Lima, R. L., Daack-Hirsch, S., Sander, A. et al. (2002). Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat. Genet. 32, 285-289.
28. Kouwenhoven, E. N., van Heeringen, S. J., Tena, J. J., Oti, M., Dutilh, B. E., Alonso, M. E., de la Calle-Mustienes, E., Smeenk, L., Rinne, T., Parsaulian, L. et al. (2010). Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet. 6, e1001065.
29. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
30. Laurikkala, J., Mikkola, M. L., James, M., Tummers, M., Mills, A. A. and Thesleff, I. (2006). p63 regulates multiple signalling pathways required for ectodermal organogenesis and differentiation. Development 133, 1553-1563.
31. Letra, A., Fakhouri, W., Fonseca, R. F., Menezes, R., Kempa, I., Prasad, J. L., McHenry, T. G., Lidral, A. C., Moreno, L., Murray, J. C. et al. (2012). Interaction between IRF6 and TGFA genes contribute to the risk of nonsyndromic cleft lip/palate. PLoS ONE 7, e45441.
32. Little, H. J., Rorick, N. K., Su, L. I., Baldock, C., Malhotra, S., Jowitt, T., Gakhar, L., Subramanian, R., Schutte, B. C., Dixon, M. J. et al. (2009). Missense mutations that cause Van der Woude syndrome and popliteal pterygium syndrome affect the DNA-binding and transcriptional activation functions of IRF6. Hum. Mol. Genet. 18, 535-545.
33. Massagué, J. (2012). TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 13, 616-630.
34. Moretti, F., Marinari, B., Lo Iacono, N., Botti, E., Giunta, A., Spallone, G., Garaffo, G., Vernersson-Lindahl, E., Merlo, G., Mills, A. A. et al. (2010). A regulatory feedback loop involving p63 and IRF6 links the pathogenesis of 2 genetically different human ectodermal dysplasias. J. Clin. Invest. 120, 1570-1577.
35. Mossey, P. A., Little, J., Munger, R. G., Dixon, M. J. and Shaw, W. C. (2009). Cleft lip and palate. Lancet 374, 1773-1785.
36. Pauws, E., Hoshino, A., Bentley, L., Prajapati, S., Keller, C., Hammond, P., Martinez-Barbera, J. P., Moore, G. E. and Stanier, P. (2009). Tbx22null mice have a submucous cleft palate due to reduced palatal bone formation and also display ankyloglossia and choanal atresia phenotypes. Hum. Mol. Genet. 18, 4171-4179.
37. Perez, C. A., Ott, J., Mays, D. J. and Pietenpol, J. A. (2007). p63 consensus DNA-binding site: identification, analysis and application into a p63MH algorithm. Oncogene 26, 7363-7370.
38. Richardson, R. J., Dixon, J., Malhotra, S., Hardman, M. J., Knowles, L., Boot- Handford, R. P., Shore, P., Whitmarsh, A. and Dixon, M. J. (2006). Irf6 is a key determinant of the keratinocyte proliferation-differentiation switch. Nat. Genet. 38, 1329-1334.
39. Richardson, R. J., Dixon, J., Jiang, R. and Dixon, M. J. (2009). Integration of IRF6 and Jagged2 signalling is essential for controlling palatal adhesion and fusion competence. Hum. Mol. Genet. 18, 2632-2642.
40. Ross, S. and Hill, C. S. (2008). How the Smads regulate transcription. Int. J. Biochem. Cell Biol. 40, 383-408.
41. Schmierer, B. and Hill, C. S. (2007). TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat. Rev. Mol. Cell Biol. 8, 970-982.
42. Shi, Y. and Massagué, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685-700.
43. 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-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase- independent manner. Nat. Cell Biol. 10, 1199-1207.
44. Srichomthong, C., Siriwan, P. and Shotelersuk, V. (2005). Significant association between IRF6 820G->A and non-syndromic cleft lip with or without cleft palate in the Thai population. J. Med. Genet. 42, e46.
45. Thomason, H. A., Zhou, H., Kouwenhoven, E. N., Dotto, G. P., Restivo, G., Nguyen, B. C., Little, H., Dixon, M. J., van Bokhoven, H. and Dixon, J. (2010). Cooperation between the transcription factors p63 and IRF6 is essential to prevent cleft palate in mice. J. Clin. Invest. 120, 1561-1569.
46. Toro, R., Saadi, I., Kuburas, A., Nemer, M. and Russo, A. F. (2004). Cell-specific activation of the atrial natriuretic factor promoter by PITX2 and MEF2A. J. Biol. Chem. 279, 52087-52094.
47. Welsh, I. C. and O'Brien, T. P. (2009). Signaling integration in the rugae growth zone directs sequential SHH signaling center formation during the rostral outgrowth of the palate. Dev. Biol. 336, 53-67.
48. Westfall, M. D., Mays, D. J., Sniezek, J. C. and Pietenpol, J. A. (2003). The Delta Np63 alpha phosphoprotein binds the p21 and 14-3-3 sigma promoters in vivo and has transcriptional repressor activity that is reduced by Hay-Wells syndrome-derived mutations. Mol. Cell. Biol. 23, 2264-2276.
49. Wong, F. K. and Hagg, U. (2004). An update on the aetiology of orofacial clefts. Hong Kong Med. J. 10, 331-336.
50. Xu, X., Han, J., Ito, Y., Bringas, P., Jr, Urata, M. M. and Chai, Y. (2006). Cell autonomous requirement for Tgfbr2 in the disappearance of medial edge epithelium during palatal fusion. Dev. Biol. 297, 238-248.
51. Xu, X., Han, J., Ito, Y., Bringas, P., Jr, Deng, C. and Chai, Y. (2008). Ectodermal Smad4 and p38 MAPK are functionally redundant in mediating TGF-beta/BMP signaling during tooth and palate development. Dev. Cell 15, 322-329.
52. 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-beta. Mol. Cell 31, 918-924.
53. Yang, L. T., Li, W. Y. and Kaartinen, V. (2008). Tissue-specific expression of Cre recombinase from the Tgfb3 locus. Genesis 46, 112-118.
54. Zawel, L., Dai, J. L., Buckhaults, P., Zhou, S., Kinzler, K. W., Vogelstein, B. and Kern, S. E. (1998). Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1, 611-617.
55. Zhang, Y. E. (2009). Non-Smad pathways in TGF-beta signaling. Cell Res. 19, 128-139.