USP18 is crucial for IFN-γ-mediated inhibition of B16 melanoma tumorigenesis and antitumor immunity

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Hong, Bangxing ^a   Li, Haiyan ^a   Lu, Yong ^a   Zhang, Mingjun ^a   Zheng, Yuhuan ^a   Qian, Jianfei ^a   Yi, Qing ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Immunosurveillance; Immunotherapy; USP18

Indexed keywords

DEUBIQUITINASE; GAMMA INTERFERON; UBIQUITIN SPECIFIC PROTEASE 18; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; PDCD1 PROTEIN, MOUSE; PROGRAMMED DEATH 1 RECEPTOR; UBIQUITIN THIOLESTERASE; USP18 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CARCINOGENESIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MELANOMA B16; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR CELL; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; CELL PROLIFERATION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; EXPERIMENTAL MELANOMA; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; PATHOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; SKIN TUMOR; TRANSPLANTATION;

MURINAE; MUS;

ANIMALS; CARCINOGENESIS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNITY, INNATE; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, SCID; NEOPLASM TRANSPLANTATION; PROGRAMMED CELL DEATH 1 RECEPTOR; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT; UBIQUITIN THIOLESTERASE;

EID: 84902544657     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-132     Document Type: Article

References (39)

1. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002, 3:991-998. 10.1038/ni1102-991, 12407406.
2. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol 2004, 22:329-360. 10.1146/annurev.immunol.22.012703.104803, 15032581.
3. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A 1998, 95:7556-7561. 10.1073/pnas.95.13.7556, 22681, 9636188.
4. van Hall T, Wolpert EZ, van Veelen P, Laban S, van der Veer M, Roseboom M, Bres S, Grufman P, de Ru A, Meiring H, de Jong A, Franken K, Teixeira A, Valentijn R, Drijfhout JW, Koning F, Camps M, Ossendorp F, Karre K, Ljunggren HG, Melief CJ, Offringa R. Selective cytotoxic T-lymphocyte targeting of tumor immune escape variants. Nat Med 2006, 12:417-424. 10.1038/nm1381, 16550190.
5. Dighe AS, Richards E, Old LJ, Schreiber RD. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1994, 1:447-456. 10.1016/1074-7613(94)90087-6, 7895156.
6. Smyth MJ. Type I interferon and cancer immunoediting. Nat Immunol 2005, 6:646-648.
7. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005, 5:375-386. 10.1038/nri1604, 15864272.
8. Liu SY, Sanchez DJ, Aliyari R, Lu S, Cheng G. Systematic identification of type I and type II interferon-induced antiviral factors. Proc Natl Acad Sci U S A 2012, 109:4239-4244. 10.1073/pnas.1114981109, 3306696, 22371602.
9. Hong B, Ren W, Song XT, Evel-Kabler K, Chen SY, Huang XF. Human suppressor of cytokine signaling 1 controls immunostimulatory activity of monocyte-derived dendritic cells. Cancer Res 2009, 69:8076-8084. 10.1158/0008-5472.CAN-09-1507, 2763040, 19789342.
10. Hong B, Song XT, Rollins L, Berry L, Huang XF, Chen SY. Mucosal and systemic anti-HIV immunity controlled by A20 in mouse dendritic cells. J Clin Invest 2011, 121:739-751. 10.1172/JCI42656, 3026719, 21206085.
11. Honke N, Shaabani N, Cadeddu G, Sorg UR, Zhang DE, Trilling M, Klingel K, Sauter M, Kandolf R, Gailus N, van Rooijen N, Burkart C, Baldus SE, Grusdat M, Lohning M, Hengel H, Pfeffer K, Tanaka M, Haussinger D, Recher M, Lang PA, Lang KS. Enforced viral replication activates adaptive immunity and is essential for the control of a cytopathic virus. Nat Immunol 2011, 13:51-57. 10.1038/ni.2169, 22101728.
12. Ritchie KJ, Hahn CS, Kim KI, Yan M, Rosario D, Li L, de la Torre JC, Zhang DE. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat Med 2004, 10:1374-1378. 10.1038/nm1133, 15531891.
13. Lu Y, Hong S, Li H, Park J, Hong B, Wang L, Zheng Y, Liu Z, Xu J, He J, Yang J, Qian J, Yi Q. Th9 cells promote antitumor immune responses in vivo. J Clin Invest 2012, 122:4160-4171. 10.1172/JCI65459, 3484462, 23064366.
14. Propper DJ, Chao D, Braybrooke JP, Bahl P, Thavasu P, Balkwill F, Turley H, Dobbs N, Gatter K, Talbot DC, Harris AL, Ganesan TS. Low-dose IFN-gamma induces tumor MHC expression in metastatic malignant melanoma. Clin Cancer Res 2003, 9:84-92.
15. Raulet DH, Guerra N. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 2009, 9:568-580. 10.1038/nri2604, 3017432, 19629084.
16. Vicari AP, Trinchieri G. Interleukin-10 in viral diseases and cancer: exiting the labyrinth?. Immunol Rev 2004, 202:223-236. 10.1111/j.0105-2896.2004.00216.x, 15546396.
17. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004, 4:540-550. 10.1038/nrc1388, 15229479.
18. Klebanoff CA, Gattinoni L, Restifo NP. CD8+ T-cell memory in tumor immunology and immunotherapy. Immunol Rev 2006, 211:214-224. 10.1111/j.0105-2896.2006.00391.x, 1501075, 16824130.
19. Anichini A, Molla A, Vegetti C, Bersani I, Zappasodi R, Arienti F, Ravagnani F, Maurichi A, Patuzzo R, Santinami M, Pircher H, Di Nicola M, Mortarini R. Tumor-reactive CD8+ early effector T cells identified at tumor site in primary and metastatic melanoma. Cancer Research 2010, 70:8378-8387. 10.1158/0008-5472.CAN-10-2028, 20861189.
20. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012, 12:252-264. 10.1038/nrc3239, 22437870.
21. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem 2002, 277:9976-9981. 10.1074/jbc.M109078200, 11788588.
22. Chen L, Sun J, Meng L, Heathcote J, Edwards AM, McGilvray ID. ISG15, a ubiquitin-like interferon-stimulated gene, promotes hepatitis C virus production in vitro: implications for chronic infection and response to treatment. J Gen Virol 2010, 91:382-388. 10.1099/vir.0.015388-0, 19846672.
23. D'Cunha J, Knight E, Haas AL, Truitt RL, Borden EC. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc Natl Acad Sci U S A 1996, 93:211-215. 10.1073/pnas.93.1.211, 40208, 8552607.
24. Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, Salem S, Radovanovic I, Grant AV, Adimi P, Mansouri N, Okada S, Bryant VL, Kong XF, Velez MM, Boisson B, Khalilzadeh S, Ozcelik U, Darazam IA, Schoggins JW, Rice CM, Al-Muhsen S, Behr M, Vogt G, Puel A, Bustamante J, Gros P, Huibregtse JM, Abel L, Boisson-Dupuis S, et al. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 2012, 337:1684-1688. 10.1126/science.1224026, 3507439, 22859821.
25. Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012, 12:265-277. 10.1038/nrc3258, 3433802, 22437871.
26. Hutchinson E. Tolerance: PD1-a multitasking receptor. Nat Rev Immunol 2012, 12:553. 10.1038/nri3266, 22828908.
27. Kurts C, Robinson BW, Knolle PA. Cross-priming in health and disease. Nat Rev Immunol 2010, 10:403-414. 10.1038/nri2780, 20498667.
28. Finkelstein SE, Carey T, Fricke I, Yu D, Goetz D, Gratz M, Dunn M, Urbas P, Daud A, DeConti R, Antonia S, Gabrilovich D, Fishman M. Changes in dendritic cell phenotype after a new high-dose weekly schedule of interleukin-2 therapy for kidney cancer and melanoma. J Immunother 2010, 33:817-827. 10.1097/CJI.0b013e3181ecccad, 20842055.
29. Bidwell BN, Slaney CY, Withana NP, Forster S, Cao Y, Loi S, Andrews D, Mikeska T, Mangan NE, Samarajiwa SA, de Weerd NA, Gould J, Argani P, Moller A, Smyth MJ, Anderson RL, Hertzog PJ, Parker BS. Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape. Nat Med 2012, 18:1224-1231. 10.1038/nm.2830, 22820642.
30. Li XL, Blackford JA, Judge CS, Liu M, Xiao W, Kalvakolanu DV, Hassel BA. RNase-L-dependent destabilization of interferon-induced mRNAs. A role for the 2-5A system in attenuation of the interferon response. J Biol Chem 2000, 275:8880-8888. 10.1074/jbc.275.12.8880, 10722734.
31. Kitareewan S, Pitha-Rowe I, Sekula D, Lowrey CH, Nemeth MJ, Golub TR, Freemantle SJ, Dmitrovsky E. UBE1L is a retinoid target that triggers PML/RARalpha degradation and apoptosis in acute promyelocytic leukemia. Proc Natl Acad Sci U S A 2002, 99:3806-3811. 10.1073/pnas.052011299, 122605, 11891284.
32. Shahidul Makki M, Cristy Ruteshouser E, Huff V. Ubiquitin specific protease 18 (Usp18) is a WT1 transcriptional target. Exp Cell Res 2013, 319:612-622. 10.1016/j.yexcr.2012.12.021, 3791519, 23291318.
33. Kim YH, Kim WT, Jeong P, Ha YS, Kang HW, Yun SJ, Moon SK, Choi YH, Kim IY, Kim WJ. Novel combination markers for predicting survival in patients with muscle invasive bladder cancer: USP18 and DGCR2. J Korean Med Sci 2014, 29:351-356. 10.3346/jkms.2014.29.3.351, 3945129, 24616583.
34. Guo Y, Dolinko AV, Chinyengetere F, Stanton B, Bomberger JM, Demidenko E, Zhou DC, Gallagher R, Ma T, Galimberti F, Liu X, Sekula D, Freemantle S, Dmitrovsky E. Blockade of the ubiquitin protease UBP43 destabilizes transcription factor PML/RARalpha and inhibits the growth of acute promyelocytic leukemia. Cancer Res 2010, 70:9875-9885. 10.1158/0008-5472.CAN-10-1100, 2999664, 20935222.
35. Guo Y, Chinyengetere F, Dolinko AV, Lopez-Aguiar A, Lu Y, Galimberti F, Ma T, Feng Q, Sekula D, Freemantle SJ, Andrew AS, Memoli V, Dmitrovsky E. Evidence for the ubiquitin protease UBP43 as an antineoplastic target. Mol Cancer Ther 2012, 11:1968-1977. 10.1158/1535-7163.MCT-12-0248, 3438286, 22752428.
36. Gabrilovich DI. Combination of chemotherapy and immunotherapy for cancer: a paradigm revisited. Lancet Oncol 2007, 8:2-3. 10.1016/S1470-2045(06)70985-8, 17196504.
37. Jett JR, Maksymiuk AW, Su JQ, Mailliard JA, Krook JE, Tschetter LK, Kardinal CG, Twito DI, Levitt R, Gerstner JB. Phase III trial of recombinant interferon gamma in complete responders with small-cell lung cancer. J Clin Oncol 1994, 12:2321-2326.
38. Shen L, Evel-Kabler K, Strube R, Chen SY. Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nat Biotechnol 2004, 22:1546-1553. 10.1038/nbt1035, 15558048.
39. Kuball J, Wen SF, Leissner J, Atkins D, Meinhardt P, Quijano E, Engler H, Hutchins B, Maneval DC, Grace MJ, Fritz MA, Storkel S, Thuroff JW, Huber C, Schuler M. Successful adenovirus-mediated wild-type p53 gene transfer in patients with bladder cancer by intravesical vector instillation. J Clin Oncol 2002, 20:957-965. 10.1200/JCO.20.4.957, 11844817.