Pax6-dependent, but β-catenin-independent, function of Bcl9 proteins in mouse lens development

Genes and Development

Volumn 28, Issue 17, 2014, Pages 1879-1884

  Cantù, Claudio ^a   Zimmerli, Dario ^a   Hausmann, George ^a   Valenta, Tomas ^a   Moor, Andreas ^b   Aguet, Michel ^b   Basler, Konrad ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b EPFL   (Switzerland)

Author keywords

Bcl9; Lens induction; Mouse; Pax6; Pygopus; Wnt

Indexed keywords

BCL9; LENS INDUCTION; MOUSE; PAX6; PYGOPUS; WNT;

ANIMALS; BETA CATENIN; CELLS, CULTURED; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCK-IN TECHNIQUES; HOMEODOMAIN PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LENS, CRYSTALLINE; MICE; MICE, INBRED C57BL; NEOPLASM PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84906887964     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.246140.114     Document Type: Article

References (33)

1. Ashery-Padan R, Marquardt T, Zhou X, Gruss P. 2000. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev 14: 2701-2711.
2. Belenkaya TY, Han C, Standley HJ, Lin X, Houston DW, Heasman J, Lin X. 2002. pygopus encodes a nuclear protein essential for wingless/Wnt signaling. Development 129: 4089-4101.
3. Brack AS, Murphy-Seiler F, Hanifi J, Deka J, Eyckerman S, Keller C, Aguet M, Rando TA. 2009. BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev Biol 335: 93-105.
4. Brandman O, Ferrell JE, Li R, Meyer T. 2005. Interlinked fast and slow positive feedback loops drive reliable cell decisions. Science 310: 496-498.
5. Brembeck FH, Wiese M, Zatula N, Grigoryan T, Dai Y, Fritzmann J, BirchmeierW. 2011. BCL9-2 promotes early stages of intestinal tumor progression. Gastroenterology 141: 1359-1370.e3.
6. Callaerts P, Halder G, Gehring WJ. 1997. PAX-6 in development and evolution. Annu Rev Neurosci 20: 483-532.
7. Cantú C, Valenta T, Hausmann G, Vilain N, Aguet M, Basler K. 2013. The Pygo2-H3K4me2/3 interaction is dispensable formouse development and Wnt signaling-dependent transcription. Development 140: 2377-2386.
8. Deka J, Wiedemann N, Anderle P, Murphy-Seiler F, Bultinck J, Eyckerman S, Stehle J-C, André S, Vilain N, Zilian O, et al. 2010. Bcl9/Bcl9l are critical for Wnt-mediated regulation of stem cell traits in colon epithelium and adenocarcinomas. Cancer Res 70: 6619-6628.
9. de la Roche M, Rutherford TJ, Gupta D, Veprintsev DB, Saxty B, Freund SM, Bienz M. 2012. An intrinsically labile a-helix abutting the BCL9- binding site of b-catenin is required for its inhibition by carnosic acid. Nat Commun 3: 680.
10. Fiedler M, S-anchez-Barrena MJ, Nekrasov M, Mieszczanek J, Rybin V, Müller J, Evans P, Bienz M. 2008. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol Cell 30: 507-518.
11. Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND, van Heyningen V. 1991. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354: 522-525.
12. Hogan BL, Horsburgh G, Cohen J, Hetherington CM, Fisher G, Lyon MF. 1986. Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J Embryol Exp Morphol 97: 95-110.
13. Kawamoto SA, Coleska A, Ran X, Yi H, Yang C-Y, Wang S. 2012. Design of triazole-stapled BCL9 a-helical peptides to target the b-catenin/B-cell CLL/lymphoma 9 (BCL9) protein-protein interaction. J Med Chem55: 1137-1146.
14. Kramps T, Peter O, Brunner E, Nellen D, Froesch B, Chatterjee S, Murone M, Züllig S, Basler K. 2002. Wnt/wingless signaling requires BCL9/ legless-mediated recruitment of pygopus to the nuclear b-catenin- TCF complex. Cell 109: 47-60.
15. Lang RA. 2004. Pathways regulating lens induction in the mouse. Int J Dev Biol 48: 783-791.
16. Li B, Mackay DR, Ma J, Dai X. 2004. Cloning and developmental expression of mouse pygopus 2, a putative Wnt signaling component. Genomics 84: 398-405.
17. Li B, Rhe C, Teng A, Bilanchone V, Munguia JE, Hu M, Jessen S, Piccolo S, Waterman ML, Dai X. 2007. Developmental phenotypes and reduced Wnt signaling in mice deficient for pygopus 2. Genesis 45: 318-325.
18. Machon O, Kreslova J, Ruzickova J, Vacik T, Klimova L, Fujimura N, Lachova J, Kozmik Z. 2010. Lens morphogenesis is dependent on Pax6-mediated inhibition of the canonical Wnt/b-catenin signaling in the lens surface ectoderm. Genesis 48: 86-95.
19. Mani M, Carrasco DE, Zhang Y, Takada K, Gatt ME, Dutta-Simmons J, Ikeda H, Diaz-Griffero F, Pena-Cruz V, Bertagnolli M, et al. 2009. BCL9 promotes tumor progression by conferring enhanced proliferative, metastatic, and angiogenic properties to cancer cells. Cancer Res 69: 7577-7586.
20. Mosimann C, Hausmann G, Basler K. 2009. b-Catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 10: 276-286.
21. Nair M, Nagamori I, Sun P, Mishra DP, Rhéaume C, Li B, Sassone-Corsi P, Dai X. 2008. Nuclear regulator Pygo2 controls spermiogenesis and histone H3 acetylation. Dev Biol 320: 446-455.
22. Parker DS, Jemison J, Cadigan KM. 2002. Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129: 2565-2576.
23. Schwab KR, Patterson LT, Hartman HA, Song N, Lang RA, Lin X, Potter SS. 2007. Pygo1 and Pygo2 roles in Wnt signaling in mammalian kidney development. BMC Biol 5: 15.
24. Smith AN, Miller L-AD, Song N, Taketo MM, Lang RA. 2005. The duality of b-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev Biol 285: 477-489.
25. Song N, Schwab KR, Patterson LT, Yamaguchi T, Lin X, Potter SS, Lang RA. 2007. pygopus 2 has a crucial, Wnt pathway-independent function in lens induction. Development 134: 1873-1885.
26. Städeli R, Basler K. 2005. Dissecting nuclear Wingless signalling: recruitment of the transcriptional co-activator Pygopus by a chain of adaptor proteins. Mech Dev 122: 1171-1182.
27. Takada K, Zhu D, Bird GH, Sukhdeo K, Zhao J-J, Mani M, Lemieux M, Carrasco DE, Ryan J, Horst D, et al. 2012. Targeted disruption of the BCL9/b-catenin complex inhibits oncogenic Wnt signaling. Sci Transl Med 4: 148ra117.
28. Tang M, Yuan W, Fan X, Liu M, Bodmer R, Ocorr K, Wu X. 2013. Pygopus maintains heart function in aging Drosophila independently of canonical Wnt signaling. Circ Cardiovasc Genet 6: 472-480.
29. Tang M, Yuan W, Bodmer R, Wu X, Ocorr K. 2014. The role of pygopus in the differentiation of intracardiac valves in Drosophila. Genesis 52: 19-28.
30. Thompson B, Townsley F, Rosin-Arbesfeld R, Musisi H, Bienz M. 2002. A new nuclear component of the Wnt signalling pathway. Nat Cell Biol 4: 367-373.
31. Valenta T, Gay M, Steiner S, Draganova K, Zemke M, Hoffmans R, Cinelli P, Aguet M, Sommer L, Basler K. 2011. Probing transcriptionspecific outputs of b-catenin in vivo. Genes Dev 25: 2631-2643.
32. Xie Q, Yang Y, Huang J, Ninkovic J, Walcher T, Wolf L, Vitenzon A, Zheng D, Götz M, Beebe DC, et al. 2013. Pax6 interactions with chromatin and identification of its novel direct target genes in lens and forebrain. PLoS ONE 8: e54507.
33. Yang Y, Cvekl A. 2005. Tissue-specific regulation of the mouse aAcrystallin gene in lens via recruitment of Pax6 and c-Maf to its promoter. J Mol Biol 351: 453-469.