FOXP3 over-expression inhibits melanoma tumorigenesis via effects on proliferation and apoptosis

Oncotarget

Volumn 5, Issue 1, 2014, Pages 264-276

  Tan, BeeShin ^a   Anaka, Matthew ^a   Deb, Siddhartha ^b   Freyer, Claudia ^a   Ebert, Lisa M ^c   Chueh, Anderly C ^a   Al Obaidi, Sheren ^a   Behren, Andreas ^a   Jayachandran, Aparna ^a   Cebon, Jonathan ^a   Chen, Weisan ^d   Mariadason, John M ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c CENTRE FOR CANCER BIOLOGY   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

Apoptosis; FOXP3; Melanoma; Proliferation

Indexed keywords

MELAN A; MESSENGER RNA; MONOPHENOL MONOOXYGENASE; TRANSCRIPTION FACTOR FOXP3; TYROSINASE RELATED PROTEIN 1; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER STAGING; CELL PROLIFERATION; CLONOGENESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MELANOMA; MELANOMA CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PIGMENTATION; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CARCINOGENESIS; CELL GROWTH; GENETIC TRANSFECTION; GENETICS; METABOLISM; METASTASIS; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CARCINOGENESIS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MELANOMA; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM METASTASIS; TRANSFECTION;

EID: 84893840464     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1600     Document Type: Article

References (47)

1. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG and Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 2005; 22(3):329-341.
2. Zuo T, Wang L, Morrison C, Chang X, Zhang H, Li W, Liu Y, Wang Y, Liu X, Chan MW, Liu JQ, Love R, Liu CG, Godfrey V, Shen R, Huang TH, et al. FOXP3 is an X-linked breast cancer suppressor gene and an important repressor of the HER-2/ErbB2 oncogene. Cell. 2007; 129(7):1275-1286.
3. Wang L, Liu R, Li W, Chen C, Katoh H, Chen GY, McNally B, Lin L, Zhou P, Zuo T, Cooney KA, Liu Y and Zheng P. Somatic single hits inactivate the X-linked tumor suppressor FOXP3 in the prostate. Cancer cell. 2009; 16(4):336-346.
4. Zhang HY and Sun H. Up-regulation of Foxp3 inhibits cell proliferation, migration and invasion in epithelial ovarian cancer. Cancer letters. 2010; 287(1):91-97.
5. Hinz S, Pagerols-Raluy L, Oberg HH, Ammerpohl O, Grussel S, Sipos B, Grutzmann R, Pilarsky C, Ungefroren H, Saeger HD, Kloppel G, Kabelitz D and Kalthoff H. Foxp3 expression in pancreatic carcinoma cells as a novel mechanism of immune evasion in cancer. Cancer research. 2007; 67(17):8344-8350.
6. Ebert LM, Tan BS, Browning J, Svobodova S, Russell SE, Kirkpatrick N, Gedye C, Moss D, Ng SP, MacGregor D, Davis ID, Cebon J and Chen W. The regulatory T cell-associated transcription factor FoxP3 is expressed by tumor cells. Cancer research. 2008; 68(8):3001-3009.
7. Quaglino P, Osella-Abate S, Marenco F, Nardo T, Gado C, Novelli M, Savoia P and Bernengo MG. FoxP3 expression on melanoma cells is related to early visceral spreading in melanoma patients treated by electrochemotherapy. Pigment Cell Melanoma Res. 2011; 24(4):734-736.
8. Niu J, Jiang C, Li C, Liu L, Li K, Jian Z and Gao T. Foxp3 expression in melanoma cells as a possible mechanism of resistance to immune destruction. Cancer Immunol Immunother. 2011; 60(8):1109-1118.
9. Wang WH, Jiang CL, Yan W, Zhang YH, Yang JT, Zhang C, Yan B, Zhang W, Han W, Wang JZ and Zhang YQ. FOXP3 expression and clinical characteristics of hepatocellular carcinoma. World J Gastroenterol. 2010; 16(43):5502-5509.
10. Kim MS, Chung NG, Yoo NJ and Lee SH. No mutation in the FOXP3 gene in acute leukemias. Leukemia research. 2011; 35(1):e10.
11. Winerdal ME, Marits P, Winerdal M, Hasan M, Rosenblatt R, Tolf A, Selling K, Sherif A and Winqvist O. FOXP3 and survival in urinary bladder cancer. BJU Int. 2011; 108(10):1672-1678.
12. Cunha LL, Morari EC, Nonogaki S, Soares FA, Vassallo J and Ward LS. Foxp3 expression is associated with aggressiveness in differentiated thyroid carcinomas. Clinics (Sao Paulo). 2012; 67(5):483-488.
13. Zeng C, Yao Y, Jie W, Zhang M, Hu X, Zhao Y, Wang S, Yin J and Song Y. Up-regulation of Foxp3 participates in progression of cervical cancer. Cancer Immunol Immunother. 2013; 62(3):481-487.
14. Zuo T, Liu R, Zhang H, Chang X, Liu Y, Wang L, Zheng P and Liu Y. FOXP3 is a novel transcriptional repressor for the breast cancer oncogene Skp2. The Journal of clinical investigation. 2007; 117(12):3765-3773.
15. McInnes N, Sadlon TJ, Brown CY, Pederson S, Beyer M, Schultze JL, McColl S, Goodall GJ and Barry SC. FOXP3 and FOXP3-regulated microRNAs suppress SATB1 in breast cancer cells. Oncogene. 2012; 31(8):1045-1054.
16. Liu R, Wang L, Chen G, Katoh H, Chen C, Liu Y and Zheng P. FOXP3 up-regulates p21 expression by site-specific inhibition of histone deacetylase 2/histone deacetylase 4 association to the locus. Cancer research. 2009; 69(6):2252-2259.
17. Li W, Wang L, Katoh H, Liu R, Zheng P and Liu Y. Identification of a tumor suppressor relay between the FOXP3 and the Hippo pathways in breast and prostate cancers. Cancer research. 2011; 71(6):2162-2171.
18. Li W, Katoh H, Wang L, Yu X, Du Z, Yan X, Zheng P and Liu Y. FOXP3 Regulates Sensitivity of Cancer Cells to Irradiation by Transcriptional Repression of BRCA1. Cancer research. 2013.
19. Frattini V, Pisati F, Speranza MC, Poliani PL, Frige G, Cantini G, Kapetis D, Cominelli M, Rossi A, Finocchiaro G and Pellegatta S. FOXP3, a novel glioblastoma oncosuppressor, affects proliferation and migration. Oncotarget. 2012; 3(10):1146-1157.
20. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C and Schultz N. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012; 2(5):401-404.
21. Tan B, Behren A, Anaka M, Vella L, Cebon J, Mariadason JM and Chen W. FOXP3 is not mutated in human melanoma. Pigment Cell Melanoma Res. 2012.
22. Merlo A, Casalini P, Carcangiu ML, Malventano C, Triulzi T, Menard S, Tagliabue E and Balsari A. FOXP3 expression and overall survival in breast cancer. J Clin Oncol. 2009; 27(11):1746-1752.
23. Kim M, Grimmig T, Grimm M, Lazariotou M, Meier E, Rosenwald A, Tsaur I, Blaheta R, Heemann U, Germer CT, Waaga-Gasser AM and Gasser M. Expression of Foxp3 in colorectal cancer but not in Treg cells correlates with disease progression in patients with colorectal cancer. PLoS One. 2013; 8(1):e53630.
24. Sato M and Kondoh M. Recent studies on metallothionein: protection against toxicity of heavy metals and oxygen free radicals. The Tohoku journal of experimental medicine. 2002; 196(1):9-22.
25. Hofmann O, Caballero OL, Stevenson BJ, Chen YT, Cohen T, Chua R, Maher CA, Panji S, Schaefer U, Kruger A, Lehvaslaiho M, Carninci P, Hayashizaki Y, Jongeneel CV, Simpson AJ, Old LJ, et al. Genome-wide analysis of cancer/testis gene expression. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(51):20422-20427.
26. Ladoire S, Arnould L, Mignot G, Coudert B, Rebe C, Chalmin F, Vincent J, Bruchard M, Chauffert B, Martin F, Fumoleau P and Ghiringhelli F. Presence of Foxp3 expression in tumor cells predicts better survival in HER2-overexpressing breast cancer patients treated with neoadjuvant chemotherapy. Breast Cancer Res Treat. 2011; 125(1):65-72.
27. Chen GY, Chen C, Wang L, Chang X, Zheng P and Liu Y. Cutting edge: Broad expression of the FoxP3 locus in epithelial cells: a caution against early interpretation of fatal inflammatory diseases following in vivo depletion of FoxP3-expressing cells. J Immunol. 2008; 180(8):5163-5166.
28. Yamamoto M, Tsuji-Takayama K, Suzuki M, Harashima A, Sugimoto A, Motoda R, Yamasaki F, Nakamura S and Kibata M. Comprehensive analysis of FOXP3 mRNA expression in leukemia and transformed cell lines. Leukemia research. 2008; 32(4):651-658.
29. Tran DQ, Ramsey H and Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood. 2007; 110(8):2983-2990.
30. Woo YL, Sterling J, Crawford R, van der Burg SH, Coleman N and Stanley M. FOXP3 immunohistochemistry on formalin-fixed paraffin-embedded tissue: poor correlation between different antibodies. J Clin Pathol. 2008; 61(8):969-971.
31. Liston A, Farr AG, Chen Z, Benoist C, Mathis D, Manley NR and Rudensky AY. Lack of Foxp3 function and expression in the thymic epithelium. The Journal of experimental medicine. 2007; 204(3):475-480.
32. Kim J, Lahl K, Hori S, Loddenkemper C, Chaudhry A, deRoos P, Rudensky A and Sparwasser T. Cutting edge: depletion of Foxp3+ cells leads to induction of autoimmunity by specific ablation of regulatory T cells in genetically targeted mice. J Immunol. 2009; 183(12):7631-7634.
33. Wolf D, Wolf AM and Tzankov A. Comment on "Cutting edge: depletion of Foxp3+ cells leads to induction of autoimmunity by specific ablation of regulatory T cells in genetically targeted mice". J Immunol. 2010; 184(8):4051.
34. Put S, Avau A, Humblet-Baron S, Schurgers E, Liston A and Matthys P. Macrophages have no lineage history of Foxp3 expression. Blood. 2012; 119(5):1316-1318.
35. Droeser RA, Obermann EC, Wolf AM, Wallner S, Wolf D and Tzankov A. Negligible Nuclear FOXP3 Expression in Breast Cancer Epithelial Cells Compared With FOXP3-Positive T Cells. Clin Breast Cancer. 2013; 13(4):264-270.
36. Hoek KS, Schlegel NC, Eichhoff OM, Widmer DS, Praetorius C, Einarsson SO, Valgeirsdottir S, Bergsteinsdottir K, Schepsky A, Dummer R and Steingrimsson E. Novel MITF targets identified using a two-step DNA microarray strategy. Pigment Cell Melanoma Res. 2008; 21(6):665-676.
37. Takeda K, Takemoto C, Kobayashi I, Watanabe A, Nobukuni Y, Fisher DE and Tachibana M. Ser298 of MITF, a mutation site in Waardenburg syndrome type 2, is a phosphorylation site with functional significance. Hum Mol Genet. 2000; 9(1):125-132.
38. Wu M, Hemesath TJ, Takemoto CM, Horstmann MA, Wells AG, Price ER, Fisher DZ and Fisher DE. c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev. 2000; 14(3):301-312.
39. Levy C, Sonnenblick A and Razin E. Role played by microphthalmia transcription factor phosphorylation and its Zip domain in its transcriptional inhibition by PIAS3. Molecular and cellular biology. 2003; 23(24):9073-9080.
40. Mann DL. Targeted cancer therapeutics: the heartbreak of success. Nature medicine. 2006; 12(8):881-882.
41. Behren A, Anaka M, Lo PH, Vella LJ, Davis ID, Catimel J, Cardwell T, Gedye C, Hudson C, Stan R and Cebon J. The Ludwig institute for cancer research Melbourne melanoma cell line panel. Pigment Cell Melanoma Res. 2013; 26(4):597-600.
42. Gibbs P, Hutchins AM, Dorian KT, Vaughan HA, Davis ID, Silvapulle M and Cebon JS. MAGE-12 and MAGE-6 are frequently expressed in malignant melanoma. Melanoma Res. 2000; 10(3):259-264.
43. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L and Rao A. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell. 2006; 126(2):375-387.
44. Jensen MM, Jorgensen JT, Binderup T and Kjaer A. Tumor volume in subcutaneous mouse xenografts measured by microCT is more accurate and reproducible than determined by 18F-FDG-microPET or external caliper. BMC Med Imaging. 2008; 8:16.
45. Smyth GK. (2005). Limma: linear models for microarray data. In: Gentleman R, Carey, V., Dudoit, S, Irizarry, R., Huber, W., ed. Bioinformatics and Computational Biology Solutions using R and Bioconductor. (New York: Springer), pp. 397-420.
46. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A and Smyth GK. A comparison of background correction methods for two-colour microarrays. Bioinformatics. 2007; 23(20):2700-2707.
47. Breitling R, Armengaud P, Amtmann A and Herzyk P. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 2004; 573(1-3):83-92.