FOXP3-MIR-146-NF-κB axis and therapy for precancerous lesions in prostate

Cancer Research

Volumn 75, Issue 8, 2015, Pages 1714-1724

  Liu, Runhua ^a,b   Yi, Bin ^a,c   Wei, Shi ^d   Yang, Wei Hsiung ^e   Hart, Karen M ^a   Chauhan, Priyanka ^a   Zhang, Wei ^a,f   Mao, Xicheng ^a   Liu, Xiuping ^g   Liu, Chang Gong ^g   Wang, Lizhong ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d University of Alabama at Birmingham   (United States)

^e MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f HARBIN MEDICAL UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

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

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; DRUG EFFECT; ENZYME INHIBITION; FOXP3 GENE; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULARLY TARGETED THERAPY; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROSTATE EPITHELIUM; PROSTATIC INTRAEPITHELIAL NEOPLASIA; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; PRECANCEROUS CONDITIONS; PROSTATE; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; BORONIC ACIDS; BORTEZOMIB; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, TRANSGENIC; MICRORNAS; PRECANCEROUS CONDITIONS; PROSTATE; PROSTATIC NEOPLASMS; PYRAZINES; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942919053     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2109     Document Type: Article

References (47)

1. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-61.
2. 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.
3. 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.
4. 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.
5. 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.
6. Zhang HY, Sun H. Up-regulation of Foxp3 inhibits cell proliferation, migration and invasion in epithelial ovarian cancer. Cancer Lett 2010; 287:91-7.
7. Tan B, Anaka M, Deb S, Freyer C, Ebert LM, Chueh AC, et al. FOXP3 overexpression inhibits melanoma tumorigenesis via effects on proliferation and apoptosis. Oncotarget 2014;5:264-76.
8. Frattini V, Pisati F, Speranza MC, Poliani PL, Frige G, Cantini G, et al. FOXP3, a novel glioblastoma oncosuppressor, affects proliferation and migration. Oncotarget 2012;3:1146-57.
9. Heinze E, Baldwin S, ChanG, Hansen J, Song J, Clements D, et al. Antibodymediated FOXP3 protein therapy induces apoptosis in cancer cells in vitro and inhibits metastasis in vivo. Int J Oncol 2009;35:167-73.
10. Liu R, Kain M, Wang L. Inactivation of X-linked tumor suppressor genes in human cancer. Future Oncol 2012;8:463-81.
11. Wang L, Liu R, Ribick M, Zheng P, Liu Y. FOXP3 as an X-linked tumor suppressor. Discov Med 2010;10:322-8.
12. 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.
13. Li W, Wang L, Katoh H, Liu R, Zheng P, Liu Y. Identification of a tumor suppressor relay between theFOXP3 and the Hippo pathways in breast and prostate cancers. Cancer Res 2011;71:2162-71.
14. Held-Feindt J, Hattermann K, Sebens S, Krautwald S, Mehdorn HM, Mentlein R. The transcription factor Forkhead box P3 (FoxP3) is expressed in glioma cells and associated with increased apoptosis. Exp Cell Res 2013;319:731-9.
15. Liu Y, Wang Y, Li W, Zheng P, Liu Y. Activating transcription factor 2 and c- Jun-mediated induction of FoxP3 for experimental therapy of mammary tumor in the mouse. Cancer Res 2009;69:5954-60.
16. Ma GF, Chen SY, Sun ZR, Miao Q, Liu YM, Zeng XQ, et al. FoxP3 inhibits proliferation and induces apoptosis of gastric cancer cells by activating the apoptotic signaling pathway. Biochem Biophys Res Commun 2013;430: 804-9.
17. 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.
18. 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.
19. 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.
20. 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.
21. Lin SL, Chiang A, Chang D, Ying SY. Loss of mir-146a function in hormonerefractory prostate cancer. Rna 2008;14:417-24.
22. Leite KR, Tomiyama A, Reis ST, Sousa-Canavez JM, Sanudo A, Camara- Lopes LH, et al. MicroRNAexpression profiles in the progression of prostate cancer-from high-grade prostate intraepithelial neoplasia to metastasis. Urol Oncol 2013;31:796-801.
23. Ma XP, Zhang T, Peng B, Yu L, Jiang de K. Association between microRNA polymorphisms and cancer risk based on the findings of 66 case-control studies. PLoS One 2013;8:e79584.
24. Lian H, Wang L, Zhang J. Increased risk of breast cancer associated with CC genotype of Has-miR-146a Rs2910164 polymorphism in Europeans. PLoS One 2012;7:e31615.
25. 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.
26. 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.
27. 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.
28. Wang X, Gao H, Ren L, Gu J, Zhang Y, Zhang Y. Demethylation of the miR- 146a promoter by 5-Aza-20-deoxycytidine correlates with delayed progression of castration-resistant prostate cancer. BMC Cancer 2014;14:308.
29. 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.
30. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res 2004;64:2270-305.
31. Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev 2007;8:49-62.
32. 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.
33. Dahlman JM, Guttridge DC. Detection of NF-kappaB activity in skeletal muscle cells by electrophoretic mobility shift analysis. Methods Mol Biol 2012;798:505-16.
34. Christian PA, Thorpe JA, Schwarze SR. Velcade sensitizes prostate cancer cells to TRAIL induced apoptosis and suppresses tumor growth in vivo. Cancer Biol Ther 2009;8:73-80.
35. 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.
36. WuX, WuJ, Huang J, Powell WC, Zhang J, Matusik RJ, et al. Generation of a prostate epithelial cell-specific Cre transgenic mouse model for tissuespecific gene ablation. Mech Dev 2001;101:61-9.
37. Chen D, Frezza M, Schmitt S, Kanwar J, Dou QP. Bortezomib as the first proteasome inhibitor anticancer drug: current status and future perspectives. Curr Cancer Drug Targets 2011;11:239-53.
38. Hideshima T, Richardson P, ChauhanD, Palombella VJ, Elliott PJ, Adams J, et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 2001;61:3071-6.
39. Chauhan D, Singh A, Brahmandam M, Podar K, Hideshima T, Richardson P, et al. Combination of proteasome inhibitors bortezomib and NPI-0052 trigger in vivo synergistic cytotoxicity in multiple myeloma. Blood 2008; 111:1654-64.
40. Ma MH, Yang HH, Parker K, Manyak S, Friedman JM, Altamirano C, et al. The proteasome inhibitor PS-341 markedly enhances sensitivity of multiple myeloma tumor cells to chemotherapeutic agents. Clin Cancer Res 2003;9:1136-44.
41. Naugler WE, Karin M. NF-kappaB and cancer-identifying targets and mechanisms. Curr Opin Genet Dev 2008;18:19-26.
42. Yip KW, Reed JC. Bcl-2 family proteins and cancer. Oncogene 2008;27: 6398-406.
43. 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.
44. 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.
45. 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.
46. 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.
47. Pacifico F, Crescenzi E, Mellone S, Iannetti A, Porrino N, Liguoro D, et al. Nuclear factor-{kappa}B contributes to anaplastic thyroid carcinomas through up-regulation of miR-146a. J Clin Endocrinol Metab 2010;95: 1421-30.