Usp18 deficient mammary epithelial cells create an antitumour environment driven by hypersensitivity to IFN-λ and elevated secretion of Cxcl10

EMBO Molecular Medicine

Volumn 5, Issue 7, 2013, Pages 1035-1050

  Burkart, Christoph ^a   Arimoto, Kei ichiro ^a   Tang, Tingdong ^a   Cong, Xiuli ^a   Xiao, Nengming ^b   Liu, Yun Cai ^b   Kotenko, Sergei V ^c   Ellies, Lesley G ^d   Zhang, Dong Er ^a,d,e  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Breast cancer; Cxcl10; Interferon ; UBP43; Usp18

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST EPITHELIUM; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HYPERSENSITIVITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; TUMOR MICROENVIRONMENT; UPREGULATION;

EID: 84880018473     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201864     Document Type: Article

References (54)

1. Bidwell BN, Slaney CY, Withana NP, Forster S, Cao Y, Loi S, Andrews D, Mikeska T, Mangan NE, Samarajiwa SA, et al (2012) Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape. Nat Med 18: 1224-1231
2. Bonecchi R, Bianchi G, Bordignon PP, D'Ambrosio D, Lang R, Borsatti A, Sozzani S, Allavena P, Gray PA, Mantovani A, et al (1998) Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J Exp Med 187: 129-134
3. Burkart C, Fan JB, Zhang DE (2012) Two independent mechanisms promote expression of an N-terminal truncated USP18 isoform with higher DeISGylation activity in the nucleus. J Biol Chem 287: 4883-4893
4. Chiang JY, Jang IK, Hodes R, Gu H (2007) Ablation of Cbl-b provides protection against transplanted and spontaneous tumors. J Clin Invest 117: 1029-1036
5. Coccia EM, Severa M, Giacomini E, Monneron D, Remoli ME, Julkunen I, Cella M, Lande R, Uze G (2004) Viral infection and Toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur J Immunol 34: 796-805
6. Cong XL, Lo MC, Reuter BA, Yan M, Fan JB, Zhang DE (2012) Usp18 promotes conventional CD11b+ dendritic cell development. J Immunol 188: 4776-4781
7. Critchley-Thorne RJ, Simons DL, Yan N, Miyahira AK, Dirbas FM, Johnson DL, Swetter SM, Carlson RW, Fisher GA, Koong A, et al (2009) Impaired interferon signaling is a common immune defect in human cancer. Proc Natl Acad Sci USA 106: 9010-9015
8. Davie SA, Maglione JE, Manner CK, Young D, Cardiff RD, MacLeod CL, Ellies LG (2007) Effects of FVB/NJ and C57Bl/6J strain backgrounds on mammary tumor phenotype in inducible nitric oxide synthase deficient mice. Transgenic Res 16: 193-201
9. Doyle SE, Schreckhise H, Khuu-Duong K, Henderson K, Rosler R, Storey H, Yao L, Liu H, Barahmand-pour F, Sivakumar P, et al (2006) Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44: 896-906
10. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD (2002) IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168: 3195-3204
11. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3: 991-998
12. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R, Bui JD, Diamond MS, Koebel CM, Arthur C, White JM, et al (2005) A critical function for type I interferons in cancer immunoediting. Nat Immunol 6: 722-729
13. Dunn GP, Old LJ, Schreiber RD (2004) The three Es of cancer immunoediting. Annu Rev Immunol 22: 329-360
14. Egeter O, Mocikat R, Ghoreschi K, Dieckmann A, Rocken M (2000) Eradication of disseminated lymphomas with CpG-DNA activated T helper type 1 cells from nontransgenic mice. Cancer Res 60: 1515-1520
15. Francois-Newton V, Magno de Freitas Almeida G, Payelle-Brogard B, Monneron D, Pichard-Garcia L, Piehler J, Pellegrini S, Uze G (2011) USP18-based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon alpha response. PLoS ONE 6: e22200
16. Groom JR, Luster AD (2011) CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 89: 207-215
17. Guo Y, Dolinko AV, Chinyengetere F, Stanton B, Bomberger JM, Demidenko E, Zhou DC, Gallagher R, Ma T, Galimberti F, et al (2010) Blockade of the ubiquitin protease UBP43 destabilizes transcription factor PML/RARalpha and inhibits the growth of acute promyelocytic leukemia. Cancer Res 70: 9875-9885
18. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ (1992) Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci USA 89: 10578-10582
19. Haabeth OA, Lorvik KB, Hammarstrom C, Donaldson IM, Haraldsen G, Bogen B, Corthay A (2011) Inflammation driven by tumour-specific Th1 cells protects against B-cell cancer. Nat Commun 2: 240
20. Hsieh MF, Lai SL, Chen JP, Sung JM, Lin YL, Wu-Hsieh BA, Gerard C, Luster A, Liao F (2006) Both CXCR3 and CXCL10/IFN-inducible protein 10 are required for resistance to primary infection by dengue virus. J Immunol 177: 1855-1863
21. Jeon YJ, Jo MG, Yoo HM, Hong SH, Park JM, Ka SH, Oh KH, Seol JH, Jung YK, Chung CH (2012) Chemosensitivity is controlled by p63 modification with ubiquitin-like protein ISG15. J Clin Invest 122: 2622-2636
22. Jing W, Gershan JA, Johnson BD (2009) Depletion of CD4 T cells enhances immunotherapy for neuroblastoma after syngeneic HSCT but compromises development of antitumor immune memory. Blood 113: 4449-4457
23. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD (1998) Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 95: 7556-7561
24. Khan IA, MacLean JA, Lee FS, Casciotti L, DeHaan E, Schwartzman JD, Luster AD (2000) IP-10 is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity 12: 483-494
25. Kmieciak M, Worschech A, Nikizad H, Gowda M, Habibi M, Depcrynski A, Wang E, Godder K, Holt SE, Marincola FM, et al (2011) CD4+ T cells inhibit the neu-specific CD8+ T-cell exhaustion during the priming phase of immune responses against breast cancer. Breast Cancer Res Treat 126: 385-394
26. Koltsida O, Hausding M, Stavropoulos A, Koch S, Tzelepis G, Ubel C, Kotenko SV, Sideras P, Lehr HA, Tepe M, et al (2011) IL-28A (IFN-lambda2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol Med 3: 348-361
27. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP (2003) IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4: 69-77
28. Lasfar A, Lewis-Antes A, Smirnov SV, Anantha S, Abushahba W, Tian B, Reuhl K, Dickensheets H, Sheikh F, Donnelly RP, et al (2006) Characterization of the mouse IFN-lambda ligand-receptor system: IFN-lambdas exhibit antitumor activity against B16 melanoma. Cancer Res 66: 4468-4477
29. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, Pollard JW (2003) Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 163: 2113-2126
30. Loeser S, Loser K, Bijker MS, Rangachari M, van der Burg SH, Wada T, Beissert S, Melief CJ, Penninger JM (2007) Spontaneous tumor rejection by cbl-b-deficient CD8+ T cells. J Exp Med 204: 879-891
31. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, Baggiolini M, Moser B (1996) Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med 184: 963-969
32. Luster AD, Greenberg SM, Leder P (1995) The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J Exp Med 182: 219-231
33. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE (2002) UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem 277: 9976-9981
34. Malakhova OA, Kim KI, Luo JK, Zou W, Kumar KG, Fuchs SY, Shuai K, Zhang DE (2006) UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. EMBO J 25: 2358-2367
35. Matzinger P (1994) Tolerance, danger, and the extended family. Annu Rev Immunol 12: 991-1045
36. Miller DM, Klucher KM, Freeman JA, Hausman DF, Fontana D, Williams DE (2009) Interferon lambda as a potential new therapeutic for hepatitis C. Ann NY Acad Sci 1182: 80-87
37. Mohty AM, Grob JJ, Mohty M, Richard MA, Olive D, Gaugler B (2010) Induction of IP-10/CXCL10 secretion as an immunomodulatory effect of low-dose adjuvant interferon-alpha during treatment of melanoma. Immunobiology 215: 113-123
38. Muller-Hermelink N, Braumuller H, Pichler B, Wieder T, Mailhammer R, Schaak K, Ghoreschi K, Yazdi A, Haubner R, Sander CA, et al (2008) TNFR1 signaling and IFN-gamma signaling determine whether T cells induce tumor dormancy or promote multistage carcinogenesis. Cancer Cell 13: 507-518
39. Pertl U, Luster AD, Varki NM, Homann D, Gaedicke G, Reisfeld RA, Lode HN (2001) IFN-gamma-inducible protein-10 is essential for the generation of a protective tumor-specific CD8 T cell response induced by single-chain IL-12 gene therapy. J Immunol 166: 6944-6951
40. Potu H, Sgorbissa A, Brancolini C (2010) Identification of USP18 as an important regulator of the susceptibility to IFN-alpha and drug-induced apoptosis. Cancer Res 70: 655-665
41. Reid LM, Minato N, Gresser I, Holland J, Kadish A, Bloom BR (1981) Influence of anti-mouse interferon serum on the growth and metastasis of tumor cells persistently infected with virus and of human prostatic tumors in athymic nude mice. Proc Natl Acad Sci USA 78: 1171-1175
42. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD (2001) IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410: 1107-1111
43. Siren J, Pirhonen J, Julkunen I, Matikainen S (2005) IFN-alpha regulates TLR-dependent gene expression of IFN-alpha, IFN-beta, IL-28, and IL-29. J Immunol 174: 1932-1937
44. Sommereyns C, Paul S, Staeheli P, Michiels T (2008) IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4: e1000017
45. Street SE, Trapani JA, MacGregor D, Smyth MJ (2002) Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J Exp Med 196: 129-134
46. Thomas SY, Hou R, Boyson JE, Means TK, Hess C, Olson DP, Strominger JL, Brenner MB, Gumperz JE, Wilson SB, et al (2003) CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J Immunol 171: 2571-2580
47. Tissari J, Siren J, Meri S, Julkunen I, Matikainen S (2005) IFN-alpha enhances TLR3-mediated antiviral cytokine expression in human endothelial and epithelial cells by up-regulating TLR3 expression. J Immunol 174: 4289-4294
48. Tominaga M, Iwashita Y, Ohta M, Shibata K, Ishio T, Ohmori N, Goto T, Sato S, Kitano S (2007) Antitumor effects of the MIG and IP-10 genes transferred with poly [D, L-2, 4-diaminobutyric acid] on murine neuroblastoma. Cancer Gene Ther 14: 696-705
49. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ (2011) Natural innate and adaptive immunity to cancer. Annu Rev Immunol 29: 235-271
50. Wang P, Yang X, Xu W, Li K, Chu Y, Xiong S (2010) Integrating individual functional moieties of CXCL10 and CXCL11 into a novel chimeric chemokine leads to synergistic antitumor effects: a strategy for chemokine-based multi-target-directed cancer therapy. Cancer Immunol Immunother 59: 1715-1726
51. Xie JH, Nomura N, Lu M, Chen SL, Koch GE, Weng Y, Rosa R, Di Salvo J, Mudgett J, Peterson LB, et al (2003) Antibody-mediated blockade of the CXCR3 chemokine receptor results in diminished recruitment of T helper 1 cells into sites of inflammation. J Leukoc Biol 73: 771-780
52. Yamamoto J, Adachi Y, Onoue Y, Adachi YS, Okabe Y, Itazawa T, Toyoda M, Seki T, Morohashi M, Matsushima K, et al (2000) Differential expression of the chemokine receptors by the Th1- and Th2-type effector populations within circulating CD4+ T cells. J Leukoc Biol 68: 568-574
53. Yan M, Luo JK, Ritchie KJ, Sakai I, Takeuchi K, Ren R, Zhang DE (2007) Ubp43 regulates BCR-ABL leukemogenesis via the type 1 interferon receptor signaling. Blood 110: 305-312
54. Yu P, Lee Y, Liu W, Krausz T, Chong A, Schreiber H, Fu YX (2005) Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med 201: 779-791