High motility of triple-negative breast cancer cells is due to repression of plakoglobin gene by metastasis modulator protein SLUG

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19472-19486

  Bailey, Charvann K ^a   Mittal, Mukul K ^a   Misras, Smita ^a   Chaudhuris, Gautam ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENT; BREAST CANCER; BREAST CANCER CELLS; CANCER CELLS; CELL MOTILITY; DOUBLE STRANDED DNA; OVER-EXPRESSION; PLAKOGLOBIN; PROMOTER ACTIVITIES; REVERSE EFFECTS; TRANSCRIPTIONAL REPRESSORS; TRIPLE NEGATIVE;

CYTOLOGY; GENES; NUCLEIC ACIDS; PATHOLOGY; PROTEINS; TRANSCRIPTION;

CELLS;

DOUBLE STRANDED DNA; MESSENGER RNA; PLAKOGLOBIN; TRANSCRIPTION FACTOR SLUG;

ACTIN FILAMENT; ARTICLE; BINDING COMPETITION; BREAST METASTASIS; CANCER CELL; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PLAKOGLOBIN GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SLUG GENE; TRANSCRIPTION REGULATION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION;

ACTIN CYTOSKELETON; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; DESMOPLAKINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, NEOPLASM; TRANSCRIPTION FACTORS;

EID: 84861755376     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.345728     Document Type: Article

References (49)

1. Lehmann, B. D., Bauer, J. A., Chen, X., Sanders, M. E., Chakravarthy, A. B., Shyr, Y., and Pietenpol, J. A. (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 121, 2750-2767
2. Huo, D., Ikpatt, F., Khramtsov, A., Dangou, J. M., Nanda, R., Dignam, J., Zhang, B., Grushko, T., Zhang, C., Oluwasola, O., Malaka, D., Malami, S., Odetunde, A., Adeoye, A. O., Iyare, F., Falusi, A., Perou, C. M., and Olopade, O. I. (2009) Population differences in breast cancer. Survey in indigenous African women reveals over-representation of triple-negative breast cancer. J. Clin. Oncol. 27, 4515-4521
3. Anders, C. K., and Carey, L. A. (2009) Biology, metastatic patterns, and treatment of patients with triple-negative breast cancer. Clin. Breast Cancer. 9, S73-S81
4. O'Brien, K. M., Cole, S. R., Tse, C. K., Perou, C. M., Carey, L. A., Foulkes, W. D., Dressler, L. G., Geradts, J., and Millikan, R. C. (2010) Intrinsic breast tumor subtypes, race, and long term survival in the Carolina Breast Cancer Study. Clin. Cancer Res. 16, 6100-6110
5. Amirikia, K. C., Mills, P., Bush, J., and Newman, L. A. (2011) Higher population- based incidence rates of triple-negative breast cancer among young African-American women. Implications for breast cancer screening recommendations. Cancer 117, 2747-2753
6. Tawfik, O., Davis, K., Kimler, B. F., Davis, M. K., Hull, S., Fan, F., Khan, Q. J., O'Dea, A. P., and Thomas, P. (2010) Clinicopathological characteristics of triple-negative invasive mammary carcinomas in African-Amer- ican versus Caucasian women. Ann. Clin. Lab. Sci. 40, 315-323
7. Shirley, S. H., Hudson, L. G., He, J., and Kusewitt, D. F. (2010) The skinny on Slug. Mol. Carcinog. 49, 851-861
8. Alves, C. C., Carneiro, F., Hoefler, H., and Becker, K. F. (2009) Role of the epithelial-mesenchymal transition regulator Slug in primary human cancers. Front. Biosci. 14, 3035-3050
9. Nieto, M. A. (2002) The snail superfamily of zinc finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166
10. Storci, G., Sansone, P., Trere, D., Tavolari, S., Taffurelli, M., Ceccarelli, C., Guarnieri, T., Paterini, P., Pariali, M., Montanaro, L., Santini, D., Chieco, P., and Bonafé, M. (2008) The basal-like breast carcinoma phenotype is regulated by SLUG gene expression. J. Pathol. 214, 25-37
11. Hajra, K. M., Chen, D. Y., and Fearon, E. R. (2002) The SLUG zinc finger protein represses E-cadherin in breast cancer. Cancer Res. 62, 1613-1618 (Pubitemid 34408479)
12. Mittal, M. K., Singh, K., Misra, S., and Chaudhuri, G. (2011) SLUG-induced elevation of D1 cyclin in breast cancer cells through the inhibition of its ubiquitination. J. Biol. Chem. 286, 469-479
13. Mittal, M. K., Myers, J. N., Misra, S., Bailey, C. K., and Chaudhuri, G. (2008) In vivo binding to and functional repression of the VDR gene promoter by SLUG in human breast cells. Biochem. Biophys. Res. Commun. 372, 30-34
14. Tripathi, M. K., Misra, S., and Chaudhuri, G. (2005) Negative regulation of the expressions of cytokeratins 8 and 19 by SLUG repressor protein in human breast cells. Biochem. Biophys. Res. Commun. 329, 508-515 (Pubitemid 40311774)
15. Tripathi, M. K., Misra, S., Khedkar, S. V., Hamilton, N., Irvin-Wilson, C., Sharan, C., Sealy, L., and Chaudhuri, G. (2005) Regulation of BRCA2 gene expression by the SLUG repressor protein in human breast cells. J. Biol. Chem. 280, 17163-17171 (Pubitemid 41389182)
16. Guo, W., Keckesova, Z., Donaher, J. L., Shibue, T., Tischler, V., Reinhardt, F., Itzkovitz, S., Noske, A., Zürrer-Härdi, U., Bell, G., Tam, W. L., Mani, S. A., van Oudenaarden, A., and Weinberg, R. A. (2012) Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148, 1015-1028
17. Todorovi, V., Desai, B. V., Patterson, M. J., Amargo, E. V., Dubash, A. D., Yin, T., Jones, J. C., and Green, K. J. (2010) Plakoglobin regulates cell motility through Rho- and fibronectin-dependent Src signaling. J. Cell Sci. 123, 3576-3586
18. Huang, H., Asimaki, A., Lo, D., McKenna, W., and Saffitz, J. (2008) Disparate effects of different mutations in plakoglobin on cell mechanical behavior. Cell. Motil. Cytoskeleton 65, 964-978
19. Shair, K. H., Schnegg, C. I., and Raab-Traub, N. (2008) EBV latent membrane protein 1 effects on plakoglobin, cell growth, and migration. Cancer Res. 68, 6997-7005
20. Pan, H., Gao, F., Papageorgis, P., Abdolmaleky, H. M., Faller, D. V., and Thiagalingam, S. (2007) Aberrant activation of γ-catenin promotes genomic instability and oncogenic effects during tumor progression. Cancer Biol. Ther. 6, 1638-1643 (Pubitemid 351590337)
21. Shafiei, F., Rahnama, F., Pawella, L., Mitchell, M. D., Gluckman, P. D., and Lobie, P. E. (2008) DNMT3A and DNMT3B mediate autocrine hGH repression of plakoglobin gene transcription and consequent phenotypic conversion of mammary carcinoma cells. Oncogene 27, 2602-2612 (Pubitemid 351550882)
22. Rieger-Christ, K. M., Ng, L., Hanley, R. S., Durrani, O., Ma, H., Yee, A. S., Libertino, J. A., and Summerhayes, I. C. (2005) Restoration of plakoglobin expression in bladder carcinoma cell lines suppresses cell migration and tumorigenic potential. Br. J. Cancer. 92, 2153-2159 (Pubitemid 40966250)
23. Yin, T., Getsios, S., Caldelari, R., Kowalczyk, A. P., Müller, E. J., Jones, J. C., and Green, K. J. (2005) Plakoglobin suppresses keratinocyte motility through both cell-cell adhesion-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. U.S.A. 102, 5420-5425 (Pubitemid 40530273)
24. Coates, J. C. (2003) Armadillo repeat proteins. Beyond the animal kingdom. Trends Cell Biol. 13, 463-471
25. Ridley, A. J. (2011) Life at the leading edge. Cell 145, 1012-1022
26. Murphy, D. A., and Courtneidge, S. A. (2011) The "ins" and "outs" of podosomes and invadopodia. Characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426
27. Destaing, O., Block, M. R., Planus, E., and Albiges-Rizo, C. (2011) Invadosome regulation by adhesion signaling. Curr. Opin. Cell Biol. 23, 597-606
28. Caca, K., Kolligs, F. T., Ji, X., Hayes, M., Qian, J., Yahanda, A., Rimm, D. L., Costa, J., and Fearon, E. R. (1999) β- and γ-catenin mutations, but not E-cadherin inactivation, underlie T-cell factor/lymphoid enhancer factor transcriptional deregulation in gastric and pancreatic cancer. Cell Growth Differ. 10, 369-376
29. Misra, S., Sharma, S., Agarwal, A., Khedkar, S. V., Tripathi, M. K., Mittal, M. K., and Chaudhuri, G. (2010) Cell cycle-dependent regulation of the bidirectional overlapping promoter of human BRCA2/ZAR2 genes in breast cancer cells. Mol. Cancer 9, 50
30. Wei, S., Gao, X., Du, J., Su, J., and Xu, Z. (2011) Angiogenin enhances cell migration by regulating stress fiber assembly and focal adhesion dynamics. PLoS One 6, e28797
31. Wu, W. S., Heinrichs, S., Xu, D., Garrison, S. P., Zambetti, G. P., Adams, J. M., and Look, A. T. (2005) Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123, 641-653 (Pubitemid 41613746)
32. Zilfou, J. T., Spector, M. S., and Lowe, S. W. (2005) Slugging it out. Fine tuning the p53-PUMA death connection. Cell 123, 545-548 (Pubitemid 41608457)
33. Leong, K. G., Niessen, K., Kulic, I., Raouf, A., Eaves, C., Pollet, I., and Karsan, A. (2007) Jagged1-mediated Notch activation induces epithelial-to- mesenchymal transition through Slug-induced repression of E-cadherin. J. Exp. Med. 204, 2935-2948 (Pubitemid 350179562)
34. Chen, H., Zhu, G., Li, Y., Padia, R. N., Dong, Z., Pan, Z. K., Liu, K., and Huang, S. (2009) Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res. 69, 9228-9235
35. McConkey, D. J., Choi, W., Marquis, L., Martin, F., Williams, M. B., Shah, J., Svatek, R., Das, A., Adam, L., Kamat, A., Siefker-Radtke, A., and Dinney, C. (2009) Role of epithelial-to-mesenchymal transition (EMT) in drug sensitivity and metastasis in bladder cancer. Cancer Metastasis Rev. 28, 335-344
36. Anastassiou, D., Rumjantseva, V., Cheng, W., Huang, J., Canoll, P. D., Yamashiro, D. J., and Kandel, J. J. (2011) Human cancer cells express Slug-based epithelial-mesenchymal transition gene expression signature obtained in vivo. BMC Cancer 11, 529
37. Katafiasz, D., Smith, L. M., and Wahl, J. K., 3rd. (2011) Slug (SNAI2) expression in oral SCC cells results in altered cell-cell adhesion and increased motility. Cell Adh. Migr. 5, 315-322
38. Wels, C., Joshi, S., Koefinger, P., Bergler, H., and Schaider, H. (2011) Transcriptional activation of ZEB1 by Slug leads to cooperative regulation of the epithelial-mesenchymal transition-like phenotype in melanoma. J. Invest. Dermatol. 131, 1877-1885
39. Yang, A. D., Camp, E. R., Fan, F., Shen, L., Gray, M. J., Liu, W., Somcio, R., Bauer, T. W., Wu, Y., Hicklin, D. J., and Ellis, L. M. (2006) Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells. Cancer Res. 66, 46-51 (Pubitemid 43166007)
40. Li, Y., Zhu, X., Zeng, Y., Wang, J., Zhang, X., Ding, Y. Q., and Liang, L. (2010) FMNL2 enhances invasion of colorectal carcinoma by inducing epithelial-mesenchymal transition. Mol. Cancer Res. 8, 1579-1590
41. Chinnadurai, G. (2009) The transcriptional corepressor CtBP: a foe of multiple tumor suppressors. Cancer Res. 69, 731-734
42. Chinnadurai, G. (2007) Transcriptional regulation by C-terminal binding proteins. Int. J. Biochem. Cell Biol. 39, 1593-1607
43. Bailey, C. K., Misra, S., Mittal, M. K., and Chaudhuri, G. (2007) Human SLUG does not directly bind to CtBP1. Biochem. Biophys. Res. Commun. 353, 661-664 (Pubitemid 46048720)
44. Cabrini, G., Bezzerri, V., Mancini, I., Nicolis, E., Dechecchi, M. C., Tamanini, A., Lampronti, I., Piccagli, L., Bianchi, N., Borgatti, M., and Gambari, R. (2010) Targeting transcription factor activity as a strategy to inhibit pro-inflammatory genes involved in cystic fibrosis. Decoy oligonucleotides and low molecular weight compounds. Curr. Med. Chem. 17, 4392-4404
45. Gambari, R., Borgatti, M., Bezzerri, V., Nicolis, E., Lampronti, I., Dechecchi, M. C., Mancini, I., Tamanini, A., and Cabrini, G. (2010) Decoy oligodeoxyribonucleotides and peptide nucleic acid-DNA chimeras targeting nuclear factor κB. Inhibition of IL-8 gene expression in cystic fibrosis cells infected with Pseudomonas aeruginosa. Biochem. Pharmacol. 80, 1887-1894
46. De Stefano, D., De Rosa, G., and Carnuccio, R. (2010) NFκB decoy oligo- nucleotides. Curr. Opin. Mol. Ther. 12, 203-213
47. Piva, R., and Gambari, R. (2002) Transcription factor decoy (TFD) in breast cancer research and treatment. Technol. Cancer Res. Treat. 1, 405-416 (Pubitemid 36554400)
48. Piva, R., Penolazzi, L., Zennaro, M., Bianchini, E., Magri, E., Borgatti, M., Lampronti, I., Lambertini, E., Tavanti, E., and Gambari, R. (2006) Induction of apoptosis of osteoclasts by targeting transcription factors with decoy molecules. Ann. N.Y. Acad. Sci. 1091, 509-516 (Pubitemid 47092262)
49. Penolazzi, L., Zennaro, M., Lambertini, E., Tavanti, E., Torreggiani, E., Gambari, R., and Piva, R. (2007) Induction of estrogen receptor α expression with decoy oligonucleotide targeted to NFATc1 binding sites in osteoblasts. Mol. Pharmacol. 71, 1457-1462 (Pubitemid 47010898)