Interactions between Twist and other core epithelial-mesenchymal transition factors are controlled by GSK3-mediated phosphorylation

Nature Communications

Volumn 4, Issue , 2013, Pages

  Lander, Rachel ^a   Nasr, Talia ^a   Ochoa, Stacy D ^a   Nordin, Kara ^a   Prasad, Maneeshi S ^a   Labonne, Carole ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SNAIL1; TRANSCRIPTION FACTOR SNAIL2; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CRANIUM; FROG; GENE EXPRESSION; GENOMICS; NEUROLOGY; PATHOLOGY; PHYSIOLOGY; TUMOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; NEURAL CREST; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; BODY PATTERNING; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOGEN SYNTHASE KINASE 3; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; MUTATION; NEURAL CREST; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS; TWIST TRANSCRIPTION FACTOR; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84874586520     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2543     Document Type: Article

References (57)

1. Le Douarin, N. & Kalcheim, C. The Neural Crest. 2nd edn (Cambridge University Press, 1999)
2. LaBonne, C. & Bronner-Fraser, M. Molecular mechanisms of neural crest formation. Annu. Rev. Cell Dev. Biol. 15, 81-112 (1999) (Pubitemid 32250372)
3. Duband, J. L. Neural crest delamination and migration: integrating regulations of cell interactions, locomotion, survival and fate. Adv. Exp. Med. Biol. 589, 45-77 (2006)
4. Thiery, J. P. & Sleeman, J. P. Complex networks orchestrate epithelialmesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142 (2006) (Pubitemid 43278296)
5. Yang, J. &Weinberg, R. A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829 (2008) (Pubitemid 351757205)
6. Bellmeyer, A., Krase, J., Lindgren, J. & LaBonne, C. The protooncogene c-Myc is an essential regulator of neural crest formation in Xenopus. Dev. Cell 4, 827-839 (2003) (Pubitemid 36676035)
7. Light, W., Vernon, A. E., Lasorella, A., Iavarone, A. & LaBonne, C. Xenopus Id3 is required downstream of Myc for the formation of multipotent neural crest progenitor cells. Development 132, 1831-1841 (2005) (Pubitemid 40691773)
8. Kelsh, R. N. Sorting out Sox10 functions in neural crest development. Bioessays 28, 788-798 (2006) (Pubitemid 44433741)
9. Spokony, R. F., Aoki, Y., Saint-Germain, N., Magner-Fink, E. & Saint-Jeannet, J. P. The transcription factor Sox9 is required for cranial neural crest development in Xenopus. Development 129, 421-432 (2002) (Pubitemid 34863808)
10. Aoki, Y. et al. Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev. Biol. 259, 19-33 (2003) (Pubitemid 36703141)
11. Kellerer, S. et al. Replacement of the Sox10 transcription factor by Sox8 reveals incomplete functional equivalence. Development 133, 2875-2886 (2006) (Pubitemid 44314265)
12. O'Donnell, M., Hong, C. S., Huang, X., Delnicki, R. J. & Saint-Jeannet, J. P. Functional analysis of Sox8 during neural crest development in Xenopus. Development 133, 3817-3826 (2006) (Pubitemid 44650960)
13. Lister, J. A. et al. Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Dev. Biol. 290, 92-104 (2006) (Pubitemid 43083606)
14. Teng, L., Mundell, N. A., Frist, A. Y., Wang, Q. & Labosky, P. A. Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 135, 1615-1624 (2008) (Pubitemid 351895491)
15. Hopwood, N. D., Pluck, A. & Gurdon, J. B. A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59, 893-903 (1989)
16. Soo, K. et al. Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev. Biol. 247, 251-270 (2002) (Pubitemid 34734863)
17. Sauka-Spengler, T. & Bronner-Fraser, M. A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9, 557-568 (2008) (Pubitemid 351881841)
18. Betancur, P., Bronner-Fraser, M. & Sauka-Spengler, T. Assembling neural crest regulatory circuits into a gene regulatory network. Annu. Rev. Cell Dev. Biol. 26, 581-603 (2010)
19. Prasad, M. S., Sauka-Spengler, T. & Labonne, C. Induction of the neural crest state: control of stem cell attributes by gene regulatory, post-transcriptional and epigenetic interactions. Dev. Biol. 366, 10-21 (2012)
20. Wu, Y. & Zhou, B. P. Snail: more than EMT. Cell Adh. Migr. 4, 199-203 (2010)
21. Taylor, K. M. & LaBonne, C. Modulating the activity of neural crest regulatory factors. Curr. Opin. Genet. Dev. 17, 326-331 (2007) (Pubitemid 47238612)
22. Hajra, K. M., Chen, D. Y. & Fearon, E. R. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 62, 1613-1618 (2002) (Pubitemid 34408479)
23. LaBonne, C. & Bronner-Fraser, M. Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration. Dev. Biol. 221, 195-205 (2000) (Pubitemid 30253584)
24. Nieto, M. A. The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166 (2002)
25. Cano, A. et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83 (2000)
26. Batlle, E. et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89 (2000)
27. Taneyhill, L. A., Coles, E. G. & Bronner-Fraser, M. Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development 134, 1481-1490 (2007) (Pubitemid 46746300)
28. Ikenouchi, J., Matsuda, M., Furuse, M. & Tsukita, S. Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J. Cell Sci. 116, 1959-1967 (2003) (Pubitemid 36622294)
29. Langeland, J. A., Tomsa, J. M., Jackman, Jr W. R. & Kimmel, C. B. An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev. Genes Evol. 208, 569-577 (1998) (Pubitemid 28542700)
30. Vernon, A. E. & LaBonne, C. Slug stability is dynamically regulated during neural crest development by the F-box protein Ppa. Development 133, 3359-3370 (2006) (Pubitemid 44501838)
31. Vernon, A. E. & LaBonne, C. Tumor metastasis: a new twist on epithelialmesenchymal transitions. Curr. Biol. 14, R719-R721 (2004) (Pubitemid 39290047)
32. Castanon, I. & Baylies, M. K. A Twist in fate: evolutionary comparison of Twist structure and function. Gene 287, 11-22 (2002) (Pubitemid 34460565)
33. Bialek, P. et al. A twist code determines the onset of osteoblast differentiation. Dev. Cell 6, 423-435 (2004) (Pubitemid 38364573)
34. Gu, S., Boyer, T. G. & Naski, M. C. Basic helix-loop-helix transcription factor Twist1 inhibits transactivator function of master chondrogenic regulator Sox9. J. Biol. Chem. 287, 21082-21092 (2012)
35. Laursen, K. B., Mielke, E., Iannaccone, P. & Fuchtbauer, E. M. Mechanism of transcriptional activation by the proto-oncogene Twist1. J. Biol. Chem. 282, 34623-34633 (2007) (Pubitemid 350232411)
36. Lander, R., Nordin, K. & LaBonne, C. The F-box protein Ppa is a common regulator of core EMT factors Twist, Snail, Slug, and Sip1. J. Cell Biol. 194, 17-25 (2011)
37. Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939 (2004) (Pubitemid 38798858)
38. Kwok, W. K. et al. Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res. 65, 5153-5162 (2005) (Pubitemid 40827324)
39. Zhang, Z. et al. Significance of TWIST expression and its association with E-cadherin in bladder cancer. Hum. Pathol. 38, 598-606 (2007) (Pubitemid 46399887)
40. Yang, M. H. et al. Comprehensive analysis of the independent effect of twist and snail in promoting metastasis of hepatocellular carcinoma. Hepatology 50, 1464-1474 (2009)
41. Feng, M. Y. et al. Metastasis-induction and apoptosis-protection by TWIST in gastric cancer cells. Clin. Exp. Metastasis 26, 1013-1023 (2009)
42. Puisieux, A., Valsesia-Wittmann, S. & Ansieau, S. A twist for survival and cancer progression. Br. J. Cancer 94, 13-17 (2006) (Pubitemid 43088534)
43. Maestro, R. et al. Twist is a potential oncogene that inhibits apoptosis. Genes Dev. 13, 2207-2217 (1999) (Pubitemid 29426726)
44. Valsesia-Wittmann, S. et al. Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell 6, 625-630 (2004) (Pubitemid 40017705)
45. Ansieau, S. et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 14, 79-89 (2008) (Pubitemid 351890463)
46. Mani, S. A. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008) (Pubitemid 351636299)
47. Battula, V. L. et al. Epithelial-mesenchymal transition-derived cells exhibit multilineage differentiation potential similar to mesenchymal stem cells. Stem Cells 28, 1435-1445 (2010)
48. Vesuna, F., Lisok, A., Kimble, B. & Raman, V. Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia 11, 1318-1328 (2009)
49. Ochoa, S. D., Salvador, S. & Labonne, C. The LIM adaptor protein LMO4 is an essential regulator of neural crest development. Dev. Biol. 361, 313-325 (2011)
50. Justice, M. J. Capitalizing on large-scale mouse mutagenesis screens. Nat. Rev. Genet. 1, 109-115 (2000)
51. Klein, P. S. & Melton, D. A. A molecular mechanism for the effect of lithium on development. Proc. Natl Acad. Sci. USA 93, 8455-8459 (1996) (Pubitemid 26269579)
52. Yeo, G. H., Cheah, F. S., Winkler, C., Jabs, E. W., Venkatesh, B. & Chong, S. S. Phylogenetic and evolutionary relationships and developmental expression patterns of the zebrafish twist gene family. Dev. Genes Evol. 219, 289-300 (2009)
53. Chen, Z. F. & Behringer, R. R. Twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev. 9, 686-699 (1995)
54. Yook, J. I., Li, X. Y., Ota, I., Fearon, E. R. & Weiss, S. J. Wnt-dependent regulation of the E-cadherin repressor snail. J. Biol. Chem. 280, 11740-11748 (2005) (Pubitemid 40418488)
55. Yook, J. I. et al. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat. Cell Biol. 8, 1398-1406 (2006) (Pubitemid 44835115)
56. Zhou, B. P. et al. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6, 931-940 (2004) (Pubitemid 39359846)
57. Kim, N. G., Xu, C. & Gumbiner, B. M. Identification of targets of the Wnt pathway destruction complex in addition to beta-catenin. Proc. Natl Acad. Sci. USA 106, 5165-5170 (2009).