BRMS1L suppresses breast cancer metastasis by inducing epigenetic silence of FZD10

Nature Communications

Volumn 5, Issue , 2014, Pages

  Gong, Chang ^a,b   Qu, Shaohua ^a,b   Lv, Xiao Bin ^a,b   Liu, Bodu ^a,b   Tan, Weige ^a,b   Nie, Yan ^a,b   Su, Fengxi ^a,b   Liu, Qiang ^a,b   Yao, Herui ^a,b   Song, Erwei ^a,b  

^a Medical Research Center   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BREAST CANCER METASTASIS SUPPRESSOR 1 LIKE; CELL SURFACE RECEPTOR; FZD10 PROTEIN; HISTONE; HISTONE DEACETYLASE 1; MICRORNA; MICRORNA 106B; PROTEIN; UNCLASSIFIED DRUG; WNT3 PROTEIN; BRMS1 PROTEIN, HUMAN; FRIZZLED PROTEIN; FZD10 PROTEIN, HUMAN; HDAC1 PROTEIN, HUMAN; MIRN106 MICRORNA, HUMAN; REPRESSOR PROTEIN; WNT3 PROTEIN, HUMAN;

CANCER; GENE EXPRESSION; INHIBITION; RNA; RODENT;

ADULT; ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER INCIDENCE; CANCER TISSUE; CELL INVASION; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEACETYLATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MIDDLE AGED; POINT MUTATION; PROMOTER REGION; PROTEIN EXPRESSION; RNA INTERFERENCE; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; TRANSIENT TRANSFECTION; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; CELL MOTION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; MCF 7 CELL LINE; METABOLISM; METASTASIS; MOUSE; PAGET NIPPLE DISEASE; PATHOLOGY; TUMOR CELL LINE; TUMOR INVASION;

MUS;

ADULT; ANIMALS; BETA CATENIN; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; CELL MOVEMENT; EPIGENESIS, GENETIC; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FRIZZLED RECEPTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HISTONE DEACETYLASE 1; HUMANS; MCF-7 CELLS; MICE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; REPRESSOR PROTEINS; WNT SIGNALING PATHWAY; WNT3 PROTEIN;

EID: 84923239528     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6406     Document Type: Article

References (53)

1. Weigelt, B., Peterse, J. L. & van 't Veer, L. J. Breast cancer metastasis: markers and models. Nat. Rev. Cancer 5, 591-602 (2005).
2. Aghdassi, A. et al. Recruitment of histone deacetylases HDAC1 and HDAC2 by the transcriptional repressor ZEB1 downregulates E-cadherin expression in pancreatic cancer. Gut 61, 439-448 (2012).
3. Castro-Castro, A., Janke, C., Montagnac, G., Paul-Gilloteaux, P. & Chavrier, P. ATAT1/MEC-17 acetyltransferase and HDAC6 deacetylase control a balance of acetylation of alpha-tubulin and cortactin and regulate MT1-MMP trafficking and breast tumor cell invasion. Eur. J. Cell Biol. 91, 950-960 (2012).
4. Thurn, K. T., Thomas, S., Raha, P., Qureshi, I. & Munster, P. N. Histone deacetylase regulation of ATM-mediated DNA damage signaling. Mol. Cancer Ther. 12, 2078-2087 (2013).
5. De Amicis, F. et al. Resveratrol, through NF-Y/p53/Sin3/HDAC1 complex phosphorylation, inhibits estrogen receptor alpha gene expression via p38MAPK/CK2 signaling in human breast cancer cells. FASEB J. 25, 3695-3707 (2011).
6. Xiong, Y. et al. Differential coupling of KLF10 to Sin3-HDAC and PCAF regulates the inducibility of the FOXP3 gene. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R608-R620 (2014).
7. Alland, L. et al. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature 387, 49-55 (1997).
8. Heideman, M. R. et al. Sin3a associated Hdac1 and Hdac2 are essential for hematopoietic stem cell homeostasis and contribute differentially to hematopoiesis. Haematologica 9, 1292-1303 (2014).
9. Dannenberg, J. H. et al. mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survival. Genes Dev. 19, 1581-1595 (2005).
10. Icardi, L. et al. The Sin3a repressor complex is a master regulator of STAT transcriptional activity. Proc. Natl Acad. Sci. USA 109, 12058-12063 (2012).
11. Balgkouranidou, I. et al. Breast cancer metastasis suppressor-1 promoter methylation in cell-free DNA provides prognostic information in non-small cell lung cancer. Br. J. Cancer 110, 2054-2062 (2014).
12. Liu, Y. et al. BRMS1 suppresses lung cancer metastases through an E3 ligase function on histone acetyltransferase p300. Cancer Res. 73, 1308-1317 (2013).
13. Li, J. et al. Prognostic significance of BRMS1 expression in human melanoma and its role in tumor angiogenesis. Oncogene 30, 896-906 (2011).
14. Cui, R. X. et al. Low BRMS1 expression promotes nasopharyngeal carcinoma metastasis in vitro and in vivo and is associated with poor patient survival. BMC Cancer 12, 376 (2012).
15. Phadke, P. A., Vaidya, K. S., Nash, K. T., Hurst, D. R. & Welch, D. R. BRMS1 suppresses breast cancer experimental metastasis to multiple organs by inhibiting several steps of the metastatic process. Am. J. Pathol. 172, 809-817 (2008).
16. Seraj, M. J., Samant, R. S., Verderame, M. F. & Welch, D. R. Functional evidence for a novel human breast carcinoma metastasis suppressor, BRMS1, encoded at chromosome 11q13. Cancer Res. 60, 2764-2769 (2000).
17. Hedley, B. D. et al. BRMS1 suppresses breast cancer metastasis in multiple experimental models of metastasis by reducing solitary cell survival and inhibiting growth initiation. Clin. Exp. Metastasis 25, 727-740 (2008).
18. Zhang, Y. et al. Effect of BRMS1 on Tumorigenicity and Metastasis of Human Rectal Cancer. Cell Biochem. Biophys. 70, 505-509 (2014).
19. Samant, R. S. et al. Breast cancer metastasis suppressor 1 (BRMS1) inhibits osteopontin transcription by abrogating NF-kappaB activation. Mol. Cancer 6, 6 (2007).
20. Hedley, B. D. et al. Downregulation of osteopontin contributes to metastasis suppression by breast cancer metastasis suppressor 1. Int. J. Cancer 123, 526-534 (2008).
21. Cicek, M. et al. BRMS1 contributes to the negative regulation of uPA gene expression through recruitment of HDAC1 to the NF-kappaB binding site of the uPA promoter. Clin. Exp. Metastasis 26, 229-237 (2009).
22. Vaidya, K. S. et al. Breast cancer metastasis suppressor-1 differentially modulates growth factor signaling. J. Biol. Chem. 283, 28354-28360 (2008).
23. Yang, J. et al. Breast cancer metastasis suppressor 1 inhibits SDF-1alpha-induced migration of non-small cell lung cancer by decreasing CXCR4 expression. Cancer Lett. 269, 46-56 (2008).
24. Hurst, D. R. et al. Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res. 69, 1279-1283 (2009).
25. Edmonds, M. D. et al. Breast cancer metastasis suppressor 1 coordinately regulates metastasis-associated microRNA expression. Int. J. Cancer 125, 1778-1785 (2009).
26. Hurst, D. R. & Welch, D. R. Unraveling the enigmatic complexities of BRMS1-mediated metastasis suppression. FEBS Lett. 585, 3185-3190 (2011).
27. Nikolaev, A. Y., Papanikolaou, N. A., Li, M., Qin, J. & Gu, W. Identification of a novel BRMS1-homologue protein p40 as a component of the mSin3A/p33(ING1b)/HDAC1 deacetylase complex. Biochem. Biophys. Res. Commun. 323, 1216-1222 (2004).
28. Silveira, A. C., Hurst, D. R., Vaidya, K. S., Ayer, D. E. & Welch, D. R. Over-expression of the BRMS1 family member SUDS3 does not suppress metastasis of human cancer cells. Cancer Lett. 276, 32-37 (2009).
29. Wend, P., Holland, J. D., Ziebold, U. & Birchmeier, W. Wnt signaling in stem and cancer stem cells. Semin. Cell Dev. Biol. 21, 855-863 (2010).
30. DiMeo, T. A. et al. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 69, 5364-5373 (2009).
31. Nguyen, D. X. et al. WNT/TCF signaling through LEF1 and HOXB9 mediates lung adenocarcinoma metastasis. Cell 138, 51-62 (2009).
32. Clevers, H. & Nusse, R. Wnt/beta-catenin signaling and disease. Cell 149, 1192-1205 (2012).
33. Nagayama, S. et al. Inverse correlation of the up-regulation of FZD10 expression and the activation of beta-catenin in synchronous colorectal tumors. Cancer Sci. 100, 405-412 (2009).
34. Fukukawa, C. et al. Activation of the non-canonical Dvl-Rac1-JNK pathway by Frizzled homologue 10 in human synovial sarcoma. Oncogene 28, 1110-1120 (2009).
35. Koike, J. et al. Molecular cloning of Frizzled-10, a novel member of the Frizzled gene family. Biochem. Biophys. Res. Commun. 262, 39-43 (1999).
36. Jeong, H., Ryu, Y. J., An, J., Lee, Y. & Kim, A. Epithelial-mesenchymal transition in breast cancer correlates with high histological grade and triple-negative phenotype. Histopathology 60, E87-E95 (2012).
37. Geyer, F. C. et al. beta-Catenin pathway activation in breast cancer is associated with triple-negative phenotype but not with CTNNB1 mutation. Mod. Pathol. 24, 209-231 (2011).
38. Gong, C. et al. MiR-106b expression determines the proliferation paradox of TGF-beta in breast cancer cells. Oncogene. doi: 10.1038/onc.2013.525 (2013).
39. Dawson, M. A. & Kouzarides, T. Cancer epigenetics: from mechanism to therapy. Cell 150, 12-27 (2012).
40. Baer, C., Claus, R. & Plass, C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res. 73, 473-477 (2013).
41. Cai, J. et al. MicroRNA-374a activates Wnt/beta-catenin signaling to promote breast cancer metastasis. J. Clin. Invest. 123, 566-579 (2013).
42. Zhang, Q. et al. Wnt/beta-catenin signaling enhances hypoxia-induced epithelial-mesenchymal transition in hepatocellular carcinoma via crosstalk with hif-1alpha signaling. Carcinogenesis 34, 962-973 (2013).
43. Kirikoshi, H., Sekihara, H. & Katoh, M. Expression profiles of 10 members of Frizzled gene family in human gastric cancer. Int. J. Oncol. 19, 767-771 (2001).
44. Terasaki, H., Saitoh, T., Shiokawa, K. & Katoh, M. Frizzled-10, up-regulated in primary colorectal cancer, is a positive regulator of the WNT - beta-catenin - TCF signaling pathway. Int. J. Mol. Med. 9, 107-112 (2002).
45. Das, T. K., Sangodkar, J., Negre, N., Narla, G. & Cagan, R. L. Sin3a acts through a multi-gene module to regulate invasion in Drosophila and human tumors. Oncogene 32, 3184-3197 (2013).
46. Nagayama, S. et al. Therapeutic potential of antibodies against FZD 10, a cell-surface protein, for synovial sarcomas. Oncogene 24, 6201-6212 (2005).
47. Hunter, K. W. et al. Predisposition to efficient mammary tumor metastatic progression is linked to the breast cancer metastasis suppressor gene Brms1. Cancer Res. 61, 8866-8872 (2001).
48. Smith, A. L. et al. The miR-106b-25 cluster targets Smad7, activates TGF-beta signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 31, 5162-5171 (2012).
49. Cai, K., Wang, Y. & Bao, X. MiR-106b promotes cell proliferation via targeting RB in laryngeal carcinoma. J. Exp. Clin. Cancer. Res. 30, 73 (2011).
50. Poliseno, L. et al. Identification of the miR-106b∼25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci. Signal. 3, ra29 (2010).
51. Smith, A. L. et al. The miR-106b-25 cluster targets Smad7, activates TGF-beta signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 31, 5162-5171.
52. Friedrichs, K., Gluba, S., Eidtmann, H. & Jonat, W. Overexpression of p53 and prognosis in breast cancer. Cancer 72, 3641-3647 (1993).
53. Chui, X. et al. Immunohistochemical expression of the c-kit proto-oncogene product in human malignant and non-malignant breast tissues. Br. J. Cancer 73, 1233-1236 (1996).