Lymphoid enhancer factor-1 mediates loading of Pax3 to a promoter harbouring lymphoid enhancer factor-1 binding sites resulting in enhancement of transcription

International Journal of Biochemistry and Cell Biology

Volumn 42, Issue 5, 2010, Pages 630-640

  Christova, Tania ^a   Mojtahedi, Golnessa ^a   Hamel, Paul A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Catenin; Cooperative interaction; Lef1; Pax3; Transcription; Wnt signalling

Indexed keywords

BETA CATENIN; LUCIFERASE; LYMPHOID ENHANCER FACTOR 1; TRANSCRIPTION FACTOR PAX3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; DELETION MUTANT; DNA SEQUENCE; EMBRYO; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNOPRECIPITATION; NONHUMAN; PROMOTER REGION; PROTEIN DNA BINDING; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION;

ANIMALS; BETA CATENIN; BINDING SITES; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LYMPHOID ENHANCER-BINDING FACTOR 1; MESODERM; MICE; NEURAL TUBE; ORGAN SPECIFICITY; PAIRED BOX TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; SOMITES; TRANSCRIPTIONAL ACTIVATION;

EID: 77649189284     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.12.006     Document Type: Article

References (98)

1. Abu-Elmagd M., Robson L., Sweetman D., Hadley J., Francis-West P., and Munsterberg A. Wnt/Lef1 signaling acts via Pitx2 to regulate somite myogenesis. Dev Biol (2009)
2. Amen M., Liu X., Vadlamudi U., Elizondo G., Diamond E., Engelhardt J.F., et al. PITX2 and beta-catenin interactions regulate Lef-1 isoform expression. Mol Cell Biol 27 (2007) 7560-7573
3. Apuzzo S., Abdelhakim A., Fortin A.S., and Gros P. Cross-talk between the paired domain and the homeodomain of Pax3: DNA binding by each domain causes a structural change in the other domain, supporting interdependence for DNA Binding. J Biol Chem 279 (2004) 33601-33612
4. Baldwin C.T., Hoth C.F., Amos J.A., da-Silva E.O., and Milunsky A. An exonic mutation in the HuP2 paired domain gene causes Waardenburg's syndrome. Nature 355 (1992) 637-638
5. Baldwin C.T., Lipsky N.R., Hoth C.F., Cohen T., Mamuya W., and Milunsky A. Mutations in PAX3 associated with Waardenburg syndrome type I. Hum Mutat 3 (1994) 205-211
6. Barr F.G., Galili N., Holick J., Biegel J.A., Rovera G., and Emanuel B.S. Rearrangement of the PAX3 paired box gene in the paediatric solid tumour alveolar rhabdomyosarcoma. Nat Genet 3 (1993) 113-117
7. Begum S., Emani N., Cheung A., Wilkins O., Der S., and Hamel P.A. Cell-type-specific regulation of distinct sets of gene targets by Pax3 and Pax3/FKHR. Oncogene (2005)
8. Behrens J., von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., et al. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382 (1996) 638-642
9. Beland M., Pilon N., Houle M., Oh K., Sylvestre J.R., Prinos P., et al. Cdx1 autoregulation is governed by a novel Cdx1-LEF1 transcription complex. Mol Cell Biol 24 (2004) 5028-5038
10. Bennicelli J.L., Fredericks W.J., Wilson R.B., Rauscher III F.J., and Barr F.G. Wild type PAX3 protein and the PAX3-FKHR fusion protein of alveolar rhabdomyosarcoma contain potent, structurally distinct transcriptional activation domains. Oncogene 11 (1995) 119-130
11. Bhanot P., Brink M., Samos C.H., Hsieh J.C., Wang Y., Macke J.P., et al. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 382 (1996) 225-230
12. Blake J., and Ziman M.R. Aberrant PAX3 and PAX7 expression. A link to the metastatic potential of embryonal rhabdomyosarcoma and cutaneous malignant melanoma?. Histol Histopathol 18 (2003) 529-539
13. Bober E., Franz T., Arnold H.H., Gruss P., and Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120 (1994) 603-612
14. Bondurand N., Pingault V., Goerich D.E., Lemort N., Sock E., Le Caignec C., et al. Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet 9 (2000) 1907-1917
15. Boras K., and Hamel P.A. Alx4 binding to LEF-1 regulates N-CAM promoter activity. J Biol Chem 277 (2002) 1120-1127
16. Boras-Granic K., Grosschedl R., and Hamel P.A. Genetic interaction between Lef1 and Alx4 is required for early embryonic development. Int J Dev Biol 50 (2006) 601-610
17. Brannon M., Brown J.D., Bates R., Kimelman D., and Moon R.T. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 126 (1999) 3159-3170
18. Briata P., Ilengo C., Corte G., Moroni C., Rosenfeld M.G., Chen C.Y., et al. The Wnt/beta-catenin-->Pitx2 pathway controls the turnover of Pitx2 and other unstable mRNAs. Mol Cell 12 (2003) 1201-1211
19. Bruhn L., Munnerlyn A., and Grosschedl R. ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRalpha enhancer function. Genes Dev 11 (1997) 640-653
20. Cao Y., and Wang C. The COOH-terminal transactivation domain plays a key role in regulating the in vitro and in vivo function of Pax3 homeodomain. J Biol Chem 275 (2000) 9854-9862
21. Cavallo R.A., Cox R.T., Moline M.M., Roose J., Polevoy G.A., Clevers H., et al. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395 (1998) 604-608
22. Chalepakis G., Goulding M., Read A., Strachan T., and Gruss P. Molecular basis of splotch and Waardenburg Pax-3 mutations. Proc Natl Acad Sci USA 91 (1994) 3685-3689
23. Chalepakis G., and Gruss P. Identification of DNA recognition sequences for the Pax3 paired domain. Gene 162 (1995) 267-270
24. Chalepakis G., Wijnholds J., and Gruss P. Pax-3-DNA interaction: flexibility in the DNA binding and induction of DNA conformational changes by paired domains. Nucleic Acids Res 22 (1994) 3131-3137
25. Chan W.Y., Cheung C.S., Yung K.M., and Copp A.J. Cardiac neural crest of the mouse embryo: axial level of origin, migratory pathway and cell autonomy of the splotch (Sp2H) mutant effect. Development 131 (2004) 3367-3379
26. Conway S.J., Henderson D.J., and Copp A.J. Pax3 is required for cardiac neural crest migration in the mouse: evidence from the splotch (Sp2H) mutant. Development 124 (1997) 505-514
27. Conway S.J., Henderson D.J., Kirby M.L., Anderson R.H., and Copp A.J. Development of a lethal congenital heart defect in the splotch (Pax3) mutant mouse. Cardiovasc Res 36 (1997) 163-173
28. Daniels D.L., and Weis W.I. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol 12 (2005) 364-371
29. De Pitta C., Tombolan L., Albiero G., Sartori F., Romualdi C., Jurman G., et al. Gene expression profiling identifies potential relevant genes in alveolar rhabdomyosarcoma pathogenesis and discriminates PAX3-FKHR positive and negative tumors. Int J Cancer 118 (2006) 2772-2781
30. Diamond E., Amen M., Hu Q., Espinoza H.M., and Amendt B.A. Functional interactions between Dlx2 and lymphoid enhancer factor regulate Msx2. Nucleic Acids Res 34 (2006) 5951-5965
31. Epstein J.A., Li J., Lang D., Chen F., Brown C.B., Jin F., et al. Migration of cardiac neural crest cells in Splotch embryos. Development 127 (2000) 1869-1878
32. Epstein J.A., Shapiro D.N., Cheng J., Lam P.Y., and Maas R.L. Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc Natl Acad Sci USA 93 (1996) 4213-4218
33. Epstein J.A., Song B., Lakkis M., and Wang C. Tumor-specific PAX3-FKHR transcription factor, but not PAX3, activates the platelet-derived growth factor alpha receptor. Mol Cell Biol 18 (1998) 4118-4130
34. Fortin A.S., Underhill D.A., and Gros P. Reciprocal effect of Waardenburg syndrome mutations on DNA binding by the Pax-3 paired domain and homeodomain. Hum Mol Genet 6 (1997) 1781-1790
35. Fortin A.S., Underhill D.A., and Gros P. Helix 2 of the paired domain plays a key role in the regulation of DNA-binding by the Pax-3 homeodomain. Nucleic Acids Res 26 (1998) 4574-4581
36. Franz T., and Kothary R. Characterization of the neural crest defect in Splotch (Sp1H) mutant mice using a lacZ transgene. Brain Res Dev Brain Res 72 (1993) 99-105
37. Fredericks W.J., Galili N., Mukhopadhyay S., Rovera G., Bennicelli J., Barr F.G., et al. The PAX3-FKHR fusion protein created by the t(2;13) translocation in alveolar rhabdomyosarcomas is a more potent transcriptional activator than PAX3. Mol Cell Biol 15 (1995) 1522-1535
38. Galceran J., Farinas I., Depew M.J., Clevers H., and Grosschedl R. Wnt3a-/--like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev 13 (1999) 709-717
39. Galceran J., Sustmann C., Hsu S.C., Folberth S., and Grosschedl R. LEF1-mediated regulation of Delta-like1 links Wnt and Notch signaling in somitogenesis. Genes Dev 18 (2004) 2718-2723
40. Galili N., Davis R.J., Fredericks W.J., Mukhopadhyay S., Rauscher III F.J., Emanuel B.S., et al. Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat Genet 5 (1993) 230-235
41. Giese K., Cox J., and Grosschedl R. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69 (1992) 185-195
42. Glaser T., Walton D.S., and Maas R.L. Genomic structure, evolutionary conservation and aniridia mutations in the human PAX6 gene. Nat Genet 2 (1992) 232-239
43. Goulding M.D., Chalepakis G., Deutsch U., Erselius J.R., and Gruss P. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10 (1991) 1135-1147
44. Graham T.A., Weaver C., Mao F., Kimelman D., and Xu W. Crystal structure of a beta-catenin/Tcf complex. Cell 103 (2000) 885-896
45. Hamblet N.S., Lijam N., Ruiz-Lozano P., Wang J., Yang Y., Luo Z., et al. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129 (2002) 5827-5838
46. Hart M.J., de los Santos R., Albert I.N., Rubinfeld B., and Polakis P. Downregulation of beta-catenin by human Axin and its association with the APC tumor suppressor, beta-catenin and GSK3 beta. Curr Biol 8 (1998) 573-581
47. Hollenbach A.D., Sublett J.E., McPherson C.J., and Grosveld G. The Pax3-FKHR oncoprotein is unresponsive to the Pax3-associated repressor hDaxx. EMBO J 18 (1999) 3702-3711
48. Hoth C.F., Milunsky A., Lipsky N., Sheffer R., Clarren S.K., and Baldwin C.T. Mutations in the paired domain of the human PAX3 gene cause Klein-Waardenburg syndrome (WS-III) as well as Waardenburg syndrome type I (WS-I). Am J Hum Genet 52 (1993) 455-462
49. Hsieh M.J., Yao Y.L., Lai I.L., and Yang W.M. Transcriptional repression activity of PAX3 is modulated by competition between corepressor KAP1 and heterochromatin protein 1. Biochem Biophys Res Commun 349 (2006) 573-581
50. Hsu S.C., Galceran J., and Grosschedl R. Modulation of transcriptional regulation by LEF-1 in response to Wnt-1 signaling and association with beta-catenin. Mol Cell Biol 18 (1998) 4807-4818
51. Hussein S.M., Duff E.K., and Sirard C. Smad4 and beta-catenin co-activators functionally interact with lymphoid-enhancing factor to regulate graded expression of Msx2. J Biol Chem 278 (2003) 48805-48814
52. Jin Z.X., Kishi H., Wei X.C., Matsuda T., Saito S., and Muraguchi A. Lymphoid enhancer-binding factor-1 binds and activates the recombination-activating gene-2 promoter together with c-Myb and Pax-5 in immature B cells. J Immunol 169 (2002) 3783-3792
53. Khan J., Bittner M.L., Saal L.H., Teichmann U., Azorsa D.O., Gooden G.C., et al. cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. Proc Natl Acad Sci USA 96 (1999) 13264-13269
54. Kwang S.J., Brugger S.M., Lazik A., Merrill A.E., Wu L.Y., Liu Y.H., et al. Msx2 is an immediate downstream effector of Pax3 in the development of the murine cardiac neural crest. Development 129 (2002) 527-538
55. Labbe E., Letamendia A., and Attisano L. Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways. Proc Natl Acad Sci USA 97 (2000) 8358-8363
56. Lalwani A.K., Brister J.R., Fex J., Grundfast K.M., Ploplis B., San Agustin T.B., et al. Further elucidation of the genomic structure of PAX3, and identification of two different point mutations within the PAX3 homeobox that cause Waardenburg syndrome type 1 in two families. Am J Hum Genet 56 (1995) 75-83
57. Lam P.Y., Sublett J.E., Hollenbach A.D., and Roussel M.F. The oncogenic potential of the Pax3-FKHR fusion protein requires the Pax3 homeodomain recognition helix but not the Pax3 paired-box DNA binding domain. Mol Cell Biol 19 (1999) 594-601
58. Lang D., Chen F., Milewski R., Li J., Lu M.M., and Epstein J.A. Pax3 is required for enteric ganglia formation and functions with Sox10 to modulate expression of c-ret. J Clin Invest 106 (2000) 963-971
59. Lang D., and Epstein J.A. Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum Mol Genet 12 (2003) 937-945
60. Lang D., Lu M.M., Huang L., Engleka K.A., Zhang M., Chu E.Y., et al. Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature 433 (2005) 884-887
61. Levanon D., Goldstein R.E., Bernstein Y., Tang H., Goldenberg D., Stifani S., et al. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc Natl Acad Sci USA 95 (1998) 11590-11595
62. Love J.J., Li X., Case D.A., Giese K., Grosschedl R., and Wright P.E. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 376 (1995) 791-795
63. Mansouri A., Hallonet M., and Gruss P. Pax genes and their roles in cell differentiation and development. Curr Opin Cell Biol 8 (1996) 851-857
64. Mansouri A., Pla P., Larue L., and Gruss P. Pax3 acts cell autonomously in the neural tube and somites by controlling cell surface properties. Development 128 (2001) 1995-2005
65. Murakami M., Tominaga J., Makita R., Uchijima Y., Kurihara Y., Nakagawa O., et al. Transcriptional activity of Pax3 is co-activated by TAZ. Biochem Biophys Res Commun 339 (2006) 533-539
66. Nishita M., Hashimoto M.K., Ogata S., Laurent M.N., Ueno N., Shibuya H., et al. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403 (2000) 781-785
67. Noll M. Evolution and role of Pax genes. Curr Opin Genet Dev 3 (1993) 595-605
68. Petropoulos H., and Skerjanc I.S. Beta-catenin is essential and sufficient for skeletal myogenesis in P19 cells. J Biol Chem 277 (2002) 15393-15399
69. Porfiri E., Rubinfeld B., Albert I., Hovanes K., Waterman M., and Polakis P. Induction of a beta-catenin-LEF-1 complex by wnt-1 and transforming mutants of beta-catenin. Oncogene 15 (1997) 2833-2839
70. Poser I., and Bosserhoff A.K. Transcription factors involved in development and progression of malignant melanoma. Histol Histopathol 19 (2004) 173-188
71. Potterf S.B., Furumura M., Dunn K.J., Arnheiter H., and Pavan W.J. Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 107 (2000) 1-6
72. Ridgeway A.G., Petropoulos H., Wilton S., and Skerjanc I.S. Wnt signaling regulates the function of MyoD and myogenin. J Biol Chem 275 (2000) 32398-32405
73. Ridgeway A.G., and Skerjanc I.S. Pax3 is essential for skeletal myogenesis and the expression of Six1 and Eya2. J Biol Chem 276 (2001) 19033-19039
74. Riese J., Yu X., Munnerlyn A., Eresh S., Hsu S.C., Grosschedl R., et al. LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88 (1997) 777-787
75. Roose J., Molenaar M., Peterson J., Hurenkamp J., Brantjes H., Moerer P., et al. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395 (1998) 608-612
76. Ross D.A., and Kadesch T. The notch intracellular domain can function as a coactivator for LEF-1. Mol Cell Biol 21 (2001) 7537-7544
77. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S., and Polakis P. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272 (1996) 1023-1026
78. Schleiffarth J.R., Person A.D., Martinsen B.J., Sukovich D.J., Neumann A., Baker C.V., et al. Wnt5a is required for cardiac outflow tract septation in mice. Pediatr Res 61 (2007) 386-391
79. Scholl F.A., Kamarashev J., Murmann O.V., Geertsen R., Dummer R., and Schafer B.W. PAX3 is expressed in human melanomas and contributes to tumor cell survival. Cancer Res 61 (2001) 823-826
80. Shapiro D.N., Sublett J.E., Li B., Downing J.R., and Naeve C.W. Fusion of PAX3 to a member of the forkhead family of transcription factors in human alveolar rhabdomyosarcoma. Cancer Res 53 (1993) 5108-5112
81. Song L., Li Y., Wang K., and Zhou C.J. Cardiac neural crest and outflow tract defects in Lrp6 mutant mice. Dev Dyn (2009)
82. Sporle R., Gunther T., Struwe M., and Schughart K. Severe defects in the formation of epaxial musculature in open brain (opb) mutant mouse embryos. Development 122 (1996) 79-86
83. Stoller J.Z., Degenhardt K.R., Huang L., Zhou D.D., Lu M.M., and Epstein J.A. Cre reporter mouse expressing a nuclear localized fusion of GFP and beta-galactosidase reveals new derivatives of Pax3-expressing precursors. Genesis 46 (2008) 200-204
84. Sun X., Zhang R., Lin X., and Xu X. Wnt3a regulates the development of cardiac neural crest cells by modulating expression of cysteine-rich intestinal protein 2 in rhombomere 6. Circ Res 102 (2008) 831-839
85. Takeda K., Yasumoto K., Takada R., Takada S., Watanabe K., Udono T., et al. Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a. J Biol Chem 275 (2000) 14013-14016
86. Tassabehji M., Newton V.E., Leverton K., Turnbull K., Seemanova E., Kunze J., et al. PAX3 gene structure and mutations: close analogies between Waardenburg syndrome and the Splotch mouse. Hum Mol Genet 3 (1994) 1069-1074
87. Terzic J., and Saraga-Babic M. Expression pattern of PAX3 and PAX6 genes during human embryogenesis. Int J Dev Biol 43 (1999) 501-508
88. Travis A., Amsterdam A., Belanger C., and Grosschedl R. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function [corrected]. Genes Dev 5 (1991) 880-894
89. Tremblay P., Kessel M., and Gruss P. A transgenic neuroanatomical marker identifies cranial neural crest deficiencies associated with the Pax3 mutant Splotch. Dev Biol 171 (1995) 317-329
90. Underhill D.A., Vogan K.J., and Gros P. Analysis of the mouse Splotch-delayed mutation indicates that the Pax-3 paired domain can influence homeodomain DNA-binding activity. Proc Natl Acad Sci USA 92 (1995) 3692-3696
91. Vogan K.J., Epstein D.J., Trasler D.G., and Gros P. The splotch-delayed (Spd) mouse mutant carries a point mutation within the paired box of the Pax-3 gene. Genomics 17 (1993) 364-369
92. Wiggan O., Fadel M.P., and Hamel P.A. Pax3 induces cell aggregation and regulates phenotypic mesenchymal-epithelial interconversion. J Cell Sci 115 (2002) 517-529
93. Wiggan O., and Hamel P.A. Pax3 regulates morphogenetic cell behavior in vitro coincident with activation of a PCP/non-canonical Wnt-signaling cascade. J Cell Sci 115 (2002) 531-541
94. Wiggan O., Taniguchi-Sidle A., and Hamel P.A. Interaction of the pRB-family proteins with factors containing paired-like homeodomains. Oncogene 16 (1998) 227-236
95. Xia S.J., and Barr F.G. Analysis of the transforming and growth suppressive activities of the PAX3-FKHR oncoprotein. Oncogene 23 (2004) 6864-6871
96. Yang-Snyder J., Miller J.R., Brown J.D., Lai C.J., and Moon R.T. A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr Biol 6 (1996) 1302-1306
97. Zhou P., Byrne C., Jacobs J., and Fuchs E. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 9 (1995) 700-713
98. Zirn B., Samans B., Wittmann S., Pietsch T., Leuschner I., Graf N., et al. Target genes of the WNT/beta-catenin pathway in Wilms tumors. Genes Chromosomes Cancer 45 (2006) 565-574