Virus-induced tumor inflammation facilitates effective DC cancer immunotherapy in a Treg-dependent manner in mice

Journal of Clinical Investigation

Volumn 121, Issue 7, 2011, Pages 2570-2582

  Woller, Norman ^a   Knocke, Sarah ^a   Mundt, Bettina ^a   Gürlevik, Engin ^a   Strüver, Nina ^a   Kloos, Arnold ^a   Boozari, Bita ^a   Schache, Peter ^a   Manns, Michael P ^a   Malek, Nisar P ^a   Sparwasser, Tim ^b   Zender, Lars ^a,c   Wirth, Thomas C ^a   Kubicka, Stefan ^a,d   Kühnel, Florian ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d Kreiskliniken Reutlingen   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; DENDRITIC CELL VACCINE; ONCOLYTIC ADENOVIRUS; TOLL LIKE RECEPTOR; VIRUS DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; DRUG TARGETING; HUMORAL IMMUNITY; INFLAMMATION; METASTASIS; MOUSE; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; T CELL DEPLETION; TUMOR CELL DESTRUCTION; TUMOR IMMUNITY; TUMOR REGRESSION; VIRUS REPLICATION;

ANIMALS; CANCER VACCINES; CELL LINE; DENDRITIC CELLS; HUMANS; IMMUNOTHERAPY; MICE; MICE, INBRED STRAINS; NEOPLASMS; NEOPLASMS, EXPERIMENTAL; T-LYMPHOCYTES, REGULATORY; VIRUSES;

EID: 79959956606     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45585     Document Type: Article

References (49)

1. Gilboa E. DC-based cancer vaccines. J Clin Invest. 2007;117(5):1195-1203. (Pubitemid 46718404)
2. Melief CJ. Cancer immunotherapy by dendritic cells. Immunity. 2008;29(3):372-383.
3. Ilett EJ, Prestwich RJ, Melcher AA. The evolving role of dendritic cells in cancer therapy. Expert Opin Biol Ther. 2010;10(3):369-379.
4. Kawai T, Akira S. Innate immune recognition of viral infection. Nat Immunol. 2006;7(2):131-137. (Pubitemid 43135878)
5. Chen M, Barnfield C, Naslund TI, Fleeton MN, Liljestrom P. MyD88 expression is required for efficient cross-presentation of viral antigens from infected cells. J Virol. 2005;79(5):2964-2972. (Pubitemid 40270575)
6. Schulz O, et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature. 2005;433(7028):887-892. (Pubitemid 40314900)
7. Sfriso P, et al. Infections and autoimmunity: the multifaceted relationship. J Leukoc Biol. 2010;87(3):385-395.
8. Rouse BT, Sehrawat S. Immunity and immunopathology to viruses: what decides the outcome? Nat Rev Immunol. 2010;10(7):514-526.
9. Robertson SJ, Hasenkrug KJ. The role of virus-induced regulatory T cells in immunopathology. Springer Semin Immunopathol. 2006;28(1):51-62. (Pubitemid 44267959)
10. Joosten SA, Ottenhoff TH. Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination. Hum Immunol. 2008;69(11):760-770.
11. Lanteri MC, et al. Tregs control the development of symptomatic West Nile virus infection in humans and mice. J Clin Invest. 2009;119(11):3266-3277.
12. Lee DC, et al. CD25+ natural regulatory T cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J Virol. 2010;84(17):8790-8798.
13. Filippi CM, Estes EA, Oldham JE, von Herrath MG. Immunoregulatory mechanisms triggered by viral infections protect from type 1 diabetes in mice. J Clin Invest. 2009;119(6):1515-1523.
14. Dittmer U, et al. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity. 2004;20(3):293-303. (Pubitemid 38388231)
15. Myers L, Messer RJ, Carmody AB, Hasenkrug KJ. Tissue-specific abundance of regulatory T cells correlates with CD8+ T cell dysfunction and chronic retrovirus loads. J Immunol. 2009;183(3):1636-1643.
16. Beilharz MW, et al. Timed ablation of regulatory CD4+ T cells can prevent murine AIDS progression. J Immunol. 2004;172(8):4917-4925. (Pubitemid 38456416)
17. Lund JM, Hsing L, Pham TT, Rudensky AY. Coordination of early protective immunity to viral infection by regulatory T cells. Science. 2008;320(5880):1220- 1224. (Pubitemid 351929511)
18. Wirth T, et al. A telomerase-dependent conditionally replicating adenovirus for selective treatment of cancer. Cancer Res. 2003;63(12):3181-3188. (Pubitemid 36735870)
19. Younghusband HB, Tyndall C, Bellett AJ. Replication and interaction of virus DNA and cellular DNA in mouse cells infected by a human adenovirus. J Gen Virol. 1979;45(2):455-467. (Pubitemid 10211263)
20. Jogler C, Hoffmann D, Theegarten D, Grunwald T, Uberla K, Wildner O. Replication properties of human adenovirus in vivo and in cultures of primary cells from different animal species. J Virol. 2006;80(7):3549-3558.
21. Hallden G, et al. Novel immunocompetent murine tumor models for the assessment of replication-competent oncolytic adenovirus efficacy. Mol Ther. 2003;8(3):412-424. (Pubitemid 37161463)
22. Ramakrishna E, et al. Antitumoral immune response by recruitment and expansion of dendritic cells in tumors infected with telomerase-dependent oncolytic viruses. Cancer Res. 2009;69(4):1448-1458.
23. Wang Y, et al. E3 gene manipulations affect oncolytic adenovirus activity in immunocompetent tumor models. Nat Biotechnol. 2003;21(11):1328-1335. (Pubitemid 37356618)
24. Snapper CM, Paul WE. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 1987;236(4804):944-947. (Pubitemid 17107942)
25. Maloy KJ, et al. CD4(+) T cell subsets during virus infection. Protective capacity depends on effector cytokine secretion and on migratory capability. J Exp Med. 2000;191(12):2159-2170. (Pubitemid 30416362)
26. Zhu J, Huang X, Yang Y. Type I IFN signaling on both B and CD4 T cells is required for protective antibody response to adenovirus. J Immunol. 2007;178(6):3505-3510. (Pubitemid 46417615)
27. Gurlevik E, et al. Selectivity of oncolytic viral replication prevents antiviral immune response and toxicity, but does not improve antitumoral immunity. Mol Ther. 2010;18(11):1972-1982.
28. Yu P, et al. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med. 2005;201(5):779-791. (Pubitemid 40395122)
29. Diaz RM, et al. Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res. 2007;67(6):2840-2848. (Pubitemid 46548974)
30. Lahl K, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med. 2007;204(1):57-63. (Pubitemid 46148756)
31. Bromley SK, Mempel TR, Luster AD. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat Immunol. 2008;9(9):970-980.
32. Zhang Y, McCluskey K, Fujii K, Wahl LM. Differential regulation of monocyte matrix metalloproteinase and TIMP-1 production by TNF-alpha, granulocyte-macrophage CSF, and IL-1 beta through prostaglandin-dependent and -independent mechanisms. J Immunol. 1998;161(6):3071-3076. (Pubitemid 28425734)
33. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9(3):162-174.
34. Van Tendeloo VF, et al. Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci U S A. 2010;107(31):13824-13829.
35. Ledford H. A shot in the arm for cancer vaccines? Nature. 2010;464(7292):1110-1111.
36. Gross S, Walden P. Immunosuppressive mechanisms in human tumors: why we still cannot cure cancer. Immunol Lett. 2008;116(1):7-14.
37. Kurooka M, Kaneda Y. Inactivated Sendai virus particles eradicate tumors by inducing immune responses through blocking regulatory T cells. Cancer Res. 2007;67(1):227-236. (Pubitemid 46142779)
38. Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature. 2006;440(7085):808-812.
39. Badovinac VP, Messingham KA, Jabbari A, Haring JS, Harty JT. Accelerated CD8+ T-cell memory and prime-boost response after dendritic-cell vaccination. Nat Med. 2005;11(7):748-756. (Pubitemid 41021207)
40. Bridle BW, et al. Potentiating cancer immunotherapy using an oncolytic virus. Mol Ther. 2010;18(8):1430-1439.
41. Robertson SJ, et al. Suppression of acute anti-friend virus CD8+ T-cell responses by coinfection with lactate dehydrogenase-elevating virus. J Virol. 2008;82(1):408-418. (Pubitemid 350309155)
42. Schneider-Schaulies S, Dittmer U. Silencing T cells or T-cell silencing: concepts in virus-induced immunosuppression. J Gen Virol. 2006;87(pt 6):1423-1438. (Pubitemid 43827197)
43. Zelinskyy G, Dietze K, Sparwasser T, Dittmer U. Regulatory T cells suppress antiviral immune responses and increase viral loads during acute infection with a lymphotropic retrovirus. PLoS Pathog. 2009;5(8):e1000406.
44. Zelinskyy G, et al. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood. 2009;114(15):3199-3207.
45. Vahlenkamp TW, Tompkins MB, Tompkins WA. The role of CD4+CD25+ regulatory T cells in viral infections. Vet Immunol Immunopathol. 2005;108(1-2):219-225. (Pubitemid 41317084)
46. Sharma MD, et al. Reprogrammed foxp3(+) regulatory T cells provide essential help to support cross-presentation and CD8(+) T cell priming in naive mice. Immunity. 2010;33(6):942-954.
47. McKelvey T, Tang A, Bett AJ, Casimiro DR, Chastain M. T-cell response to adenovirus hexon and DNA-binding protein in mice. Gene Ther. 2004;11(9):791-796. (Pubitemid 38659758)
48. Mennuni C, et al. Preventive vaccination with telomerase controls tumor growth in genetically engineered and carcinogen-induced mouse models of cancer. Cancer Res. 2008;68(23):9865-9874.
49. Mueller SN, Jones CM, Smith CM, Heath WR, Carbone FR. Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J Exp Med. 2002;195(5):651-656. (Pubitemid 34461510)