SWI/SNF Chromatin-Remodeling Factor Smarcd3/Baf60c Controls Epithelial-Mesenchymal Transition by Inducing Wnt5a Signaling

Molecular and Cellular Biology

Volumn 33, Issue 15, 2013, Pages 3011-3025

  Jordan, Nicole Vincent ^a   Prat, Aleix ^a   Abell, Amy N ^a   Zawistowski, Jon S ^a   Sciaky, Noah ^a   Karginova, Olga A ^a   Zhou, Bingying ^a   Golitz, Brian T ^b   Perou, Charles M ^a   Johnson, Gary L ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b Department of Genetics and Lineberger Comprehensive Cancer Center ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAF 60C PROTEIN; BARRIER TO AUTOINTEGRATION FACTOR; BLOCKING ANTIBODY; CLAUDIN; EPITHELIAL CELL ADHESION MOLECULE; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION; WNT SIGNALING PATHWAY;

BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; EPIGENESIS, GENETIC; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; UP-REGULATION; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84880651479     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01443-12     Document Type: Article

References (47)

1. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial- mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7:131-142.
2. Yang J, Weinberg RA. 2008. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14:818-829.
3. Valastyan S, Weinberg RA. 2011. Tumor metastasis: molecular insights and evolving paradigms. Cell 147:275-292.
4. Thiery JP, Acloque H, Huang RYJ, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
5. Kalluri R, Weinberg RA. 2009. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119:1420-1428.
6. Nieto MA. 2011. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 27:347-376.
7. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128:693-705.
8. Nieto MA. 2002. The Snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3:155-166.
9. Abell AN, Jordan NV, Huang W, Prat A, Midland AA, Johnson NL, Granger DA, Mieczkowski PA, Perou CM, Gomez SM, Li L, Johnson GL. 2011. MAP3K4/CBP-regulated H2B acetylation controls epithelial-mesenchymal transition in trophoblast stem cells. Cell Stem Cell 8:525-537.
10. Fulford LG, Reis-Filho JS, Ryder K, Jones C, Gillett CE, Hanby A, Easton DF, Lakhani SR. 2007. Basal-like grade III invasive ductal carcinoma of the breast: patterns of metastasis and long term survival. Breast Cancer Res. 9:R4. doi:10.1186/bcr1636.
11. Gaedcke J, Traub F, Milde S, Wilkens L, Stan A, Ostertag H, Christgen M, von Wasielewski R, Kreipe HH. 2007. Predominance of the basal type and HER-2/neu type in brain metastasis from breast cancer. Mod. Pathol. 20:864-870.
12. Banerjee S. 2006. Basal-like breast carcinomas: clinical outcome and response to chemotherapy. J. Clin. Pathol. 59:729-735.
13. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, He X, Perou CM. 2010. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res. 12:R68. doi:10.1186/bcr2635.
14. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, Lander ES. 2011. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146:633-644.
15. Proia TA, Keller PJ, Gupta PB, Klebba I, Jones AD, Sedic M, Gilmore H, Tung N, Naber SP, Schnitt S, Lander ES, Kuperwasser C. 2011. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 8:149-163.
16. Troester MA. 2004. Cell-type-specific responses to chemotherapeutics in breast cancer. Cancer Res. 64:4218-4226.
17. Abell AN, Granger DA, Johnson NL, Vincent-Jordan N, Dibble CF, Johnson GL. 2009. Trophoblast stem cell maintenance by fibroblast growth factor 4 requires MEKK4 activation of Jun N-terminal kinase. Mol. Cell. Biol. 29:2748-2761.
18. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF, Livasy C, Carey LA, Reynolds E, Dressler L, Nobel A, Parker J, Ewend MG, Sawyer LR, Wu J, Liu Y, Nanda R, Tretiakova M, Orrico A, Dreher D, Palazzo JP, Perreard L, Nelson E, Mone M, Hansen H, Mullins M, Quackenbush JF, Ellis MJ, Olopade OI, Bernard PS, Perou CM. 2006. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 7:96-108. doi:10.1186/1471-2164-7-96.
19. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
20. Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463:474-484.
21. Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, Henkelman RM, Wrana JL, Rossant J, Bruneau BG. 2004. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432:107-112.
22. Takeuchi JK, Lickert H, Bisgrove BW, Sun X, Yamamoto M, Chawengsaksophak K, Hamada H, Yost HJ, Rossant J, Bruneau BG. 2007. Baf60c is a nuclear Notch signaling component required for the establishment of left-right asymmetry. Proc. Natl. Acad. Sci. U. S. A. 104:846-851.
23. Forcales SV, Albini S, Giordani L, Malecova B, Cignolo L, Chernov A, Coutinho P, Saccone V, Consalvi S, Williams R, Wang K, Wu Z, Baranovskaya S, Miller A, Dilworth FJ, Puri PL. 2011. Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J. 2:301-316.
24. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat M-L, Gyorki DE, Ward T, Partanen A, Feleppa F, Huschtscha LI, Thorne HJ, kConFab, Fox SB, Yan M, French JD, Brown MA, Smyth GK, Visvader JE, Lindeman GJ. 2009. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat. Med. 15:907-915.
25. Veeman MT, Axelrod JD, Moon RT. 2003. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5:367-377.
26. Zhu Y, Tian Y, Du J, Hu Z, Yang L, Liu J, Gu L. 2012. Dvl2-dependent activation of Daam1 and RhoA regulates Wnt5a-induced breast cancer cell migration. PLoS One 7:e37823. doi:10.1371/journal.pone.0037823.
27. Dissanayake SKS, Wade MM, Johnson CEC, O'Connell MPM, Leotlela PDP, French ADA, Shah KVK, Hewitt KJK, Rosenthal DTD, Indig FEF, Jiang YY, NickoloffBJB, Taub DDD, Trent JMJ, Moon RTR, Bittner MM, Weeraratna ATA. 2007. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J. Biol. Chem. 282:17259-17271.
28. Banine F. 2005. SWI/SNF chromatin-remodeling factors induce changes in DNA methylation to promote transcriptional activation. Cancer Res. 65:3542-3547.
29. Holder N, Klein R. 1999. Eph receptors and ephrins: effectors of morphogenesis. Development 126:2033-2044.
30. Pasquale EB. 2010. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat. Rev. Cancer 10:165-180.
31. Dominguez MG, Hughes VC, Pan L, Simmons M, Daly C, Anderson K, Noguera-Troise I, Murphy AJ, Valenzuela DM, Davis S, Thurston G, Yancopoulos GD, Gale NW. 2007. Vascular endothelial tyrosine phosphatase (VE-PTP)-null mice undergo vasculogenesis but die embryonically because of defects in angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 104:3243-3248.
32. Mori M, Murata Y, Kotani T, Kusakari S, Ohnishi H, Saito Y, Okazawa H, Ishizuka T, Mori M, Matozaki T. 2010. Promotion of cell spreading and migration by vascular endothelial-protein tyrosine phosphatase (VE-PTP) in cooperation with integrins. J. Cell. Physiol. 224:195-204.
33. Rafael MS, Laizé V, Florindo C, Ferraresso S, Bargelloni L, Cancela ML. 2012. Overexpression of four and a half LIM domains protein 2 promotes epithelial-mesenchymal transition-like phenotype in fish pre-osteoblasts. Biochimie 94:1128-1134.
34. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, Kieu C, Papior P, Baeuerle PA, Munz M, Gires O. 2009. Nuclear signalling by tumour-associated antigen EpCAM. Nat. Cell Biol. 11:162-171.
35. Ding L, Wang Z, Yan J, Yang X, Liu A, Qiu W, Zhu J, Han J, Zhang H, Lin J, Cheng L, Qin X, Niu C, Yuan B, Wang X, Zhu C, Zhou Y, Li J, Song H, Huang C, Ye Q. 2009. Human four-and-a-half LIM family members suppress tumor cell growth through a TGF-β -like signaling pathway. J. Clin. Invest. 119:349-361.
36. Sheikh F, Raskin A, Chu P-H, Lange S, Domenighetti AA, Zheng M, Liang X, Zhang T, Yajima T, Gu Y, Dalton ND, Mahata SK, Dorn GW, II, Heller-Brown J, Peterson KL, Omens JH, McCulloch AD, Chen J. 2008. An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice. J. Clin. Invest. 118:3870-3880.
37. Guais A, Siegrist S, Solhonne B, Jouault H, Guellaën G, Bulle F. 2006. h-Goliath, paralog of GRAIL, is a new E3 ligase protein, expressed in human leukocytes. Gene 374:112-120.
38. Sekiguchi T. 2001. Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B. J. Biol. Chem. 276:7246-7257.
39. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. 2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290-303.
40. Tcherkezian J, Lamarche-Vane N. 2007. Current knowledge of the large RhoGAP family of proteins. Biol. Cell 99:67-86.
41. Chuang TH, Xu X, Kaartinen V, Heisterkamp N, Groffen J, Bokoch GM. 1995. Abr and Bcr are multifunctional regulators of the Rho GTP-binding protein family. Proc. Natl. Acad. Sci. U. S. A. 92:10282-10286.
42. Singhal N, Graumann J, Wu G, Araúzo-Bravo MJ, Han DW, Greber B, Gentile L, Mann M, Schöler HR. 2010. Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141: 943-955.
43. Kidder BL, Palmer S, Knott JG. 2009. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 27:317-328.
44. Li R, Liang J, Ni S, Zhou T, Qing X, Li H, He W, Chen J, Li F, Zhuang Q, Qin B, Xu J, Li W, Yang J, Gan Y, Qin D, Feng S, Song H, Yang D, Zhang B, Zeng L, Lai L, Esteban MA, Pei D. 2010. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7:51-63.
45. Scheel C, Eaton EN, Li SH-J, Chaffer CL, Reinhardt F, Kah K-J, Bell G, Guo W, Rubin J, Richardson AL, Weinberg RA. 2011. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 145:926-940.
46. Yu M, Ting DT, Stott SL, Wittner BS, Ozsolak F, Paul S, Ciciliano JC, Smas ME, Winokur D, Gilman AJ, Ulman MJ, Xega K, Contino G, Alagesan B, Brannigan BW, Milos PM, Ryan DP, Sequist LV, Bardeesy N, Ramaswamy S, Toner M, Maheswaran S, Haber DA. 2012. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 487:510-513.
47. Dissanayake SK, Olkhanud PB, O'Connell MP, Carter A, French AD, Camilli TC, Emeche CD, Hewitt KJ, Rosenthal DT, Leotlela PD, Wade MS, Yang SW, Brant L, NickoloffBJ, Messina JL, Biragyn A, Hoek KS, Taub DD, Longo DL, Sondak VK, Hewitt SM, Weeraratna AT. 2008. Wnt5A regulates expression of tumor-associated antigens in melanoma via changes in signal transducers and activators of transcription 3 phosphorylation. Cancer Res. 68:10205-10214.