FOXP3 controls an MIR-146/NF-κB negative feedback loop that inhibits apoptosis in breast cancer cells

Cancer Research

Volumn 75, Issue 8, 2015, Pages 1703-1713

  Liu, Runhua ^a,b   Liu, Cong ^a,c   Chen, Dongquan ^d   Yang, Wei Hsiung ^e   Liu, Xiuping ^f   Liu, Chang Gong ^f   Dugas, Courtney M ^a   Tang, Fei ^g   Zheng, Pan ^g   Liu, Yang ^g   Wang, Lizhong ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c CHINA MEDICAL UNIVERSITY   (China)

^d University of Alabama at Birmingham   (United States)

^e MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^g CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MICRORNA; MICRORNA 146A; MICRORNA 146B; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; MIRN146 MICRORNA, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; BREAST EPITHELIUM CELL; CANCER INHIBITION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; IRAK1 GENE; MALE; METASTASIS INHIBITION; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; TRAF6 GENE; ANIMAL; BREAST TUMOR; DOWN REGULATION; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; MCF 7 CELL LINE; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; TUMOR CELL CULTURE;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; DOWN-REGULATION; FEEDBACK, PHYSIOLOGICAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; MICE; MICE, INBRED NOD; MICE, TRANSGENIC; MICRORNAS; NF-KAPPA B; TUMOR CELLS, CULTURED;

EID: 84927941644     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2108     Document Type: Article

References (47)

1. Lu LF, Boldin MP, Chaudhry A, Lin LL, Taganov KD, Hanada T, et al. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 2010;142: 914-29.
2. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 2006;103: 12481-6.
3. Bhaumik D, Scott GK, Schokrpur S, Patil CK, Campisi J, Benz CC. Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene 2008;27: 5643-7.
4. Hurst DR, Edmonds MD, Scott GK, Benz CC, Vaidya KS, Welch DR. Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res 2009;69: 1279-83.
5. Luo D, Wilson JM, Harvel N, Liu J, Pei L, Huang S, et al. A systematic evaluation of miRNA: MRNA interactions involved in the migration and invasion of breast cancer cells. J Transl Med 2013;11: 57.
6. Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, et al. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 2011;208: 1189-201.
7. Zhao JL, Rao DS, Boldin MP, Taganov KD, O'Connell RM, Baltimore D. NFkappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc Natl Acad Sci U S A 2011;108: 9184-9.
8. Starczynowski DT, Morin R, McPherson A, Lam J, Chari R, Wegrzyn J, et al. Genome-wide identification of human microRNAs located in leukemiaassociated genomic alterations. Blood 2011;117: 595-607.
9. Li Y, Vandenboom TG II, Wang Z, Kong D, Ali S, Philip PA, et al. miR-146a suppresses invasion of pancreatic cancer cells. Cancer Res 2010;70: 1486-95.
10. Xu B, Wang N, Wang X, Tong N, Shao N, Tao J, et al. MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERKdependent manner in castration-resistant prostate cancer. Prostate 2012; 72: 1171-8.
11. Wang D, Liu D, Gao J, Liu M, Liu S, Jiang M, et al. TRAIL-induced miR-146a expression suppresses CXCR4-mediated human breast cancer migration. FEBS J 2013;280: 3340-53.
12. Mei J, Bachoo R, Zhang CL. MicroRNA-146a inhibits glioma development by targeting Notch1. Mol Cell Biol 2011;31: 3584-92.
13. Lin SL, Chiang A, Chang D, Ying SY. Loss of mir-146a function in hormonerefractory prostate cancer. RNA 2008;14: 417-24.
14. Zhang X, Li D, Li M, Ye M, Ding L, Cai H, et al. MicroRNA-146a targets PRKCE to modulate papillary thyroid tumor development. Int J Cancer 2014;134: 257-67.
15. Li X, Xu B, Moran MS, Zhao Y, Su P, Haffty BG, et al. 53BP1 functions as a tumor suppressor in breast cancer via the inhibition ofNF-kappaB through miR-146a. Carcinogenesis 2012;33: 2593-600.
16. Liu R, Wang L, Chen G, Katoh H, Chen C, Liu Y, et al. FOXP3 up-regulates p21 expression by site-specific inhibition of histone deacetylase 2/histone deacetylase 4 association to the locus. Cancer Res 2009;69: 2252-9.
17. Zuo T, Liu R, Zhang H, Chang X, Liu Y, Wang L, et al. FOXP3 is a novel transcriptional repressor for the breast cancer oncogene SKP2. J Clin Invest 2007;117: 3765-73.
18. Zuo T, Wang L, Morrison C, Chang X, Zhang H, Li W, et al. FOXP3 is an Xlinked breast cancer suppressor gene and an important repressor of the HER-2/ErbB2 oncogene. Cell 2007;129: 1275-86.
19. Katoh H, Qin ZS, Liu R, Wang L, Li W, Li X, et al. FOXP3 orchestrates H4K16 acetylation and H3K4 trimethylation for activation of multiple genes by recruiting MOF and causing displacement of PLU-1. Mol Cell 2011;44: 770-84.
20. Wang L, Liu R, Li W, Chen C, Katoh H, Chen GY, et al. Somatic single hits inactivate the X-linked tumor suppressor FOXP3 in the prostate. Cancer Cell 2009;16: 336-46.
21. Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev 2007;8: 49-62.
22. Magness ST, Jijon H, Van Houten Fisher N, Sharpless NE, Brenner DA, Jobin C. In vivo pattern of lipopolysaccharide and anti-CD3-induced NF-kappa B activation using a novel gene-targeted enhanced GFP reporter gene mouse. J Immunol 2004;173: 1561-70.
23. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005;22: 329-41.
24. Wang CY, Cusack JC Jr, Liu R, Baldwin AS Jr. Control of inducible chemoresistance: Enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat Med 1999;5: 412-7.
25. Liang CC, Park AY, Guan JL. In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2007;2: 329-33.
26. McSherry EA, Brennan K, Hudson L, Hill AD, Hopkins AM. Breast cancer cell migration is regulated through junctional adhesion molecule-A-mediated activation of Rap1 GTPase. Breast Cancer Res 2011;13: R31.
27. Schramek D, Kotsinas A, Meixner A, Wada T, Elling U, Pospisilik JA, et al. The stress kinase MKK7 couples oncogenic stress to p53 stability and tumor suppression. Nat Genet 2011;43: 212-9.
28. Corcoran DL, Pandit KV, Gordon B, Bhattacharjee A, Kaminski N, Benos PV. Features of mammalian microRNA promoters emerge from polymerase II chromatin immunoprecipitation data. PLoS ONE 2009;4: E5279.
29. Baer C, Claus R, Plass C. Genome-wide epigenetic regulation ofmiRNAs in cancer. Cancer Res 2013;73: 473-7.
30. Ozsolak F, Poling LL, Wang Z, Liu H, Liu XS, Roeder RG, et al. Chromatin structure analyses identify miRNA promoters. Genes Dev 2008;22: 3172-83.
31. Wang X, Lu H, Li T, Yu L, Liu G, Peng X, et al. Kruppel-like factor 8 promotes tumorigenic mammary stem cell induction by targeting miR-146a. Am J Cancer Res 2013;3: 356-73.
32. Wang L, Liu R, Ribick M, Zheng P, Liu Y. FOXP3 as an X-linked tumor suppressor. Discov Med 2010;10: 322-8.
33. McInnes N, Sadlon TJ, Brown CY, Pederson S, Beyer M, Schultze JL, et al. FOXP3 and FOXP3-regulated microRNAs suppress SATB1 in breast cancer cells. Oncogene 2012;31: 1045-54.
34. Zheng Y, Josefowicz SZ, Kas A, Chu TT, GavinMA, Rudensky AY. Genomewide analysis of Foxp3 target genes in developing andmature regulatory T cells. Nature 2007;445: 936-40.
35. Liu WH, Chang LS. Suppression of Akt/Foxp3-mediated miR-183 expression blocks Sp1-mediated ADAM17 expression and TNFalpha-mediated NFkappaB activation in piceatannol-treated human leukemia U937 cells. Biochem Pharmacol 2012;84: 670-80.
36. Hao Q, Li W, Zhang C, Qin X, Xue X, Li M, et al. TNFalpha induced FOXP3-NFkappaB interaction dampens the tumor suppressor role of FOXP3 in gastric cancer cells. Biochem Biophys Res Commun 2013;430: 436-41.
37. Hao Q, Zhang C, Gao Y, Wang S, Li J, LiM, et al. FOXP3 inhibits NF-kappaB activity and hence COX2 expression in gastric cancer cells. Cell Signal 2014;26: 564-9.
38. Xiang M, Birkbak NJ, Vafaizadeh V, Walker SR, Yeh JE, Liu S, et al. STAT3 induction of miR-146b formsa feedback loopto inhibit theNF-kappaB to IL-6 signaling axis and STAT3-driven cancer phenotypes. Sci Signal 2014;7: Ra11.
39. Hossain DM, Panda AK, Manna A, Mohanty S, Bhattacharjee P, Bhattacharyya S, et al. FoxP3 acts as a cotranscription factor with STAT3 in tumorinduced regulatory T cells. Immunity 2013;39: 1057-69.
40. Douglass S, Meeson AP, Overbeck-Zubrzycka D, Brain JG, Bennett MR, Lamb CA, et al. Breast cancer metastasis: Demonstration that FOXP3 regulates CXCR4 expression and the response to CXCL12. J Pathol 2014; 234: 74-85.
41. Nakahira K, Morita A, Kim NS, Yanagihara I. Phosphorylation of FOXP3 by LCK downregulates MMP9 expression and represses cell invasion. PLoS ONE 2013;8: E77099.
42. Dong QG, Sclabas GM, Fujioka S, Schmidt C, Peng B, Wu T, et al. The function of multiple IkappaB: NF-kappaB complexes in the resistance of cancer cells to Taxol-induced apoptosis. Oncogene 2002;21: 6510-9.
43. Wang CY, MayoMW, Korneluk RG, Goeddel DV, Baldwin AS Jr. NF-kappaB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998;281: 1680-3.
44. Weintraub SJ, Manson SR, Deverman BE. Resistance to antineoplastic therapy. The oncogenic tyrosine kinase-Bcl-x(L) axis. Cancer Cell 2004; 5: 3-4.
45. Yip KW, Reed JC. Bcl-2 family proteins and cancer. Oncogene 2008; 27: 6398-406.
46. Zhou F, Yang Y, Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J 2011;278: 403-13.
47. Chen C, Edelstein LC, Gelinas C. The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol Cell Biol 2000;20: 2687-95.