Presentation of tumour antigens by dendritic cells and challenges faced

Current Opinion in Immunology

Volumn 22, Issue 1, 2010, Pages 137-144

  Robson, Neil C ^c   Hoves, Sabine ^b   Maraskovsky, Eugene ^a   Schnurr, Max ^b  

^a CSL LIMITED   (Australia)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE PROSTATE ISOENZYME; AUTOANTIGEN; BCR ABL PROTEIN; CARCINOEMBRYONIC ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPSTEIN BARR VIRUS ANTIGEN; FREUND ADJUVANT; GLYCOPROTEIN GP 100; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 2; LATENT MEMBRANE PROTEIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MELAN A; MELANOMA ANTIGEN 3; MONOCLONAL ANTIBODY PR1; MONOPHENOL MONOOXYGENASE; MUCIN 1; NY ESO 1 ANTIGEN; PROSTATE SPECIFIC ANTIGEN; PROSTATE SPECIFIC MEMBRANE ANTIGEN; PROTEIN P53; RAS PROTEIN; RUBELLA VACCINE; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TUMOR ANTIGEN; UNINDEXED DRUG; WT1 PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; BREAST CANCER; CANCER ADJUVANT THERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL MATURATION; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL; COLORECTAL CANCER; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENDOPLASMIC RETICULUM; EX VIVO GENE TRANSFER; GLIOBLASTOMA; HEAD AND NECK CANCER; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOTHERAPY; IN VIVO GENE TRANSFER; KIDNEY CARCINOMA; LUNG NON SMALL CELL CANCER; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MULTIPLE MYELOMA; OVARY CANCER; OVERALL SURVIVAL; PANCREAS CANCER; PERITONEUM CANCER; PROSTATE CANCER; REVIEW; SOLID TUMOR; UPREGULATION; UTERINE CERVIX CANCER;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CLINICAL TRIALS AS TOPIC; DENDRITIC CELLS; HUMANS; NEOPLASMS; TUMOR ESCAPE;

EID: 77249118696     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2010.01.002     Document Type: Review

References (59)

1. Savina A., and Amigorena S. Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 219 (2007) 143-156
2. Melief C.J. Cancer immunotherapy by dendritic cells. Immunity 29 (2008) 372-383
3. Wilson N.S., and Villadangos J.A. Regulation of antigen presentation and cross-presentation in the dendritic cell network: facts, hypothesis, and immunological implications. Adv Immunol 86 (2005) 241-305
4. + T cells in anti-tumor immune responses. Immunol Rev 222 (2008) 129-144
5. Rock K.L., York I.A., and Goldberg A.L. Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat Immunol 5 (2004) 670-677
6. Degli-Esposti M.A., and Smyth M.J. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol 5 (2005) 112-124
7. Kloetzel P.M. Generation of major histocompatibility complex class I antigens: functional interplay between proteasomes and TPPII. Nat Immunol 5 (2004) 661-669
8. Gaczynska M., Rock K.L., and Goldberg A.L. Gamma-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 365 (1993) 264-267
9. Momburg F., Roelse J., Howard J.C., Butcher G.W., Hammerling G.J., and Neefjes J.J. Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367 (1994) 648-651
10. Chapatte L., Ayyoub M., Morel S., Peitrequin A.-L., Levy N., Servis C., Van den Eynde B.J., Valmori D., and Levy F. Processing of tumor-associated antigen by the proteasomes of dendritic cells controls in vivo T cell responses. Cancer Res 66 (2006) 5461-5468
11. Chapiro J., Claverol S., Piette F., Ma W., Stroobant V., Guillaume B., Gairin J.E., Morel S., Burlet-Schiltz O., Monsarrat B., et al. Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 176 (2006) 1053-1061
12. Dissemond J., Goette P., Moers J., Lindeke A., Goos M., Ferrone S., and Wagner S.N. Immunoproteasome subunits LMP2 and LMP7 downregulation in primary malignant melanoma lesions: association with lack of spontaneous regression. Melanoma Res 13 (2003) 371-377
13. Hoves S., Aigner M., Pfeiffer C., Laumer M., Obermann E.C., and Mackensen A. In situ analysis of the antigen-processing machinery in acute myeloid leukaemic blasts by tissue microarray. Leukemia 23 (2009) 877-885. This paper shows for the first time, that APM components in AML blasts are downregulated from initial diagnosis to relapse in individual patients.
14. Seliger B., Atkins D., Bock M., Ritz U., Ferrone S., Huber C., and Storkel S. Characterization of human lymphocyte antigen class I antigen-processing machinery defects in renal cell carcinoma lesions with special emphasis on transporter-associated with antigen-processing down-regulation. Clin Cancer Res 9 (2003) 1721-1727
15. Meidenbauer N., Zippelius A., Pittet M.J., Laumer M., Vogl S., Heymann J., Rehli M., Seliger B., Schwarz S., Le Gal F.A., et al. High frequency of functionally active Melan-A-specific T cells in a patient with progressive immunoproteasome-deficient melanoma. Cancer Res 64 (2004) 6319-6326
16. Khan A.N., Gregorie C.J., and Tomasi T.B. Histone deacetylase inhibitors induce TAP, LMP, Tapasin genes and MHC class I antigen presentation by melanoma cells. Cancer Immunol Immunother 57 (2008) 647-654
17. Cheever M.A., Allison J.P., Ferris A.S., Finn O.J., Hastings B.M., Hecht T.T., Mellman I., Prindiville S.A., Viner J.L., Weiner L.M., et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res 15 (2009) 5323-5337. This work represents a substantial undertaking that has pooled the opinions of numerous world-class scientists and clinicians for the purpose of prioritising tumour antigens with the goal of identifying those most likely to prove effective clinically.
18. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6 (2006) 295-307
19. Zarling A.L., Polefrone J.M., Evans A.M., Mikesh L.M., Shabanowitz J., Lewis S.T., Engelhard V.H., and Hunt D.F. Identification of class I MHC-associated phosphopeptides as targets for cancer immunotherapy. Proc Natl Acad Sci U S A 103 (2006) 14889-14894
20. Ochi T., Fujiwara H., Suemori K., Azuma T., Yakushijin Y., Hato T., Kuzushima K., and Yasukawa M. Aurora-A kinase: a novel target of cellular immunotherapy for leukemia. Blood 113 (2009) 66-74
21. Holler C., Pinon J.D., Denk U., Heyder C., Hofbauer S., Greil R., and Egle A. PKCbeta is essential for the development of chronic lymphocytic leukemia in the TCL1 transgenic mouse model: validation of PKCbeta as a therapeutic target in chronic lymphocytic leukemia. Blood 113 (2009) 2791-2794
22. Takahashi Y., Harashima N., Kajigaya S., Yokoyama H., Cherkasova E., McCoy J.P., Hanada K., Mena O., Kurlander R., Tawab A., et al. Regression of human kidney cancer following allogeneic stem cell transplantation is associated with recognition of an HERV-E antigen by T cells. J Clin Invest 118 (2008) 1099-1109
23. Hambach L., Vermeij M., Buser A., Aghai Z., van der Kwast T., and Goulmy E. Targeting a single mismatched minor histocompatibility antigen with tumor-restricted expression eradicates human solid tumors. Blood 112 (2008) 1844-1852
24. Qing J., Du X., Chen Y., Chan P., Li H., Wu P., Marsters S., Stawicki S., Tien J., Totpal K., et al. Antibody-based targeting of FGFR3 in bladder carcinoma and t(4;14)-positive multiple myeloma in mice. J Clin Invest 119 (2009) 1216-1229
25. Wray J., Williamson E.A., Sheema S., Lee S.H., Libby E., Willman C.L., Nickoloff J.A., and Hromas R. Metnase mediates chromosome decatenation in acute leukemia cells. Blood 114 (2009) 1852-1858
26. Young R.M., Hardy I.R., Clarke R.L., Lundy N., Pine P., Turner B.C., Potter T.A., and Refaeli Y. Mouse models of non-Hodgkin lymphoma reveal Syk as an important therapeutic target. Blood 113 (2009) 2508-2516
27. Besch R., Poeck H., Hohenauer T., Senft D., Häcker G., Berking C., Hornung V., Endres S., Ruzicka T., Rothenfusser S., and Hartmann G. Proapoptotic signaling induced by RIG-I and MDA-5 results in type I interferon-independent apoptosis in human melanoma cells. J Clin Invest 119 (2009) 2399-2411. This work identifies cytosolic helicases, such as the viral sensors MDA-5 and RIG-I, as targets for the induction of tumour-specific apoptosis via transfected RNA molecules.
28. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., Vermaelen K., Panaretakis T., Mignot G., Ullrich E., et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1[beta]-dependent adaptive immunity against tumors. Nat Med 15 (2009) 1170-1178. Identifies that conventional chemotherapy regimens are not all equal and that specific classes can induce immunogenic cell death and improved patient outcome via an inflammasome-dependent pathway.
29. Green D.R., Ferguson T., Zitvogel L., and Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 9 (2009) 353-363
30. Saric T., Graef C.I., and Goldberg A.L. Pathway for degradation of peptides generated by proteasomes: a key role for thimet oligopeptidase and other metallopeptidases. J Biol Chem 279 (2004) 46723-46732
31. Towne C.F., York I.A., Neijssen J., Karow M.L., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Neefjes J.J., and Rock K.L. Leucine aminopeptidase is not essential for trimming peptides in the cytosol or generating epitopes for MHC class I antigen presentation. J Immunol 175 (2005) 6605-6614
32. Towne C.F., York I.A., Watkin L.B., Lazo J.S., and Rock K.L. Analysis of the role of bleomycin hydrolase in antigen presentation and the generation of CD8 T cell responses. J Immunol 178 (2007) 6923-6930
33. Geier E., Pfeifer G., Wilm M., Lucchiari-Hartz M., Baumeister W., Eichmann K., and Niedermann G. A giant protease with potential to substitute for some functions of the proteasome. Science 283 (1999) 978-981
34. Schnurr M., Orban M., Robson N.C., Shin A., Braley H., Airey D., Cebon J., Maraskovsky E., and Endres S. ISCOMATRIX adjuvant induces efficient cross-presentation of tumor antigen by dendritic cells via rapid cytosolic antigen delivery and processing via Tripeptidyl Peptidase II. J Immunol 182 (2009) 1253-1259. Demonstrated that the formulation of the T-Ag was critical to which intracellular protease complex was recruited for processing class I MHC cross-presentation.
35. Seifert U., Maranon C., Shmueli A., Desoutter J.-F., Wesoloski L., Janek K., Henklein P., Diescher S., Andrieu M., de la Salle H., et al. An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 4 (2003) 375-379. Demonstrated that the cytosolic aminopeptidase, TPPII, could generate certain MHC class I epitopes independently of the proteasome.
36. Reits E., Neijssen J., Herberts C., Benckhuijsen W., Janssen L., Drijfhout J.W., and Neefjes J. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 20 (2004) 495-506
37. Marcilla M., Villasevil E.M., and de Castro J.A. Tripeptidyl peptidase II is dispensable for the generation of both proteasome-dependent and proteasome-independent ligands of HLA-B27 and other class I molecules. Eur J Immunol 38 (2008) 631-639
38. + T cells.
39. Kyte J.A., Mu L., Aamdal S., Kvalheim G., Dueland S., Hauser M., Gullestad H.P., Ryder T., Lislerud K., Hammerstad H., et al. Phase I/II trial of melanoma therapy with dendritic cells transfected with autologous tumor-mRNA. Cancer Gene Ther 13 (2006) 905-918
40. Engell-Noerregaard L., Hansen T.H., Andersen M.H., Thor Straten P., and Svane I.M. Review of clinical studies on dendritic cell-based vaccination of patients with malignant melanoma: assessment of correlation between clinical response and vaccine parameters. Cancer Immunol Immunother 58 (2009) 1-14
41. Higano C.S., Schellhammer P.F., Small E.J., Burch P.A., Nemunaitis J., Yuh L., Provost N., and Frohlich M.W. Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer. Cancer 115 (2009) 3670-3679
42. Didierlaurent A.M., Morel S., Lockman L., Giannini S.L., Bisteau M., Carlsen H., Kielland A., Vosters O., Vanderheyde N., Schiavetti F., et al. AS04, an aluminum salt- and TLR-4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. J Immunol 183 (2009) 6186-6197
43. Lambrecht B.N., Kool M., Willart M.A., and Hammad H. Mechanism of action of clinically approved adjuvants. Curr Opin Immunol 21 (2009) 23-29
44. O'Hagan D.T. MF59 is a safe and potent vaccine adjuvant that enhances protection against influenza virus infection. Expert Rev Vac 6 (2007) 699-710
45. Peek L.J., Middaugh C.R., and Berkland C. Nanotechnology in vaccine delivery. Adv Drug Deliv Rev 60 (2008) 915-928
46. Baldridge J.R., McGowan P., Evans J.T., Cluff C., Mossman S., Johnson D., and Persing D. Taking a Toll on human disease: Toll-like receptor 4 agonists as vaccine adjuvants and monotherapeutic agents. Expert Opin Biol Ther 4 (2004) 1129-1138
47. Tomai M.A., Miller R.L., Lipson K.E., Kieper W.C., Zarraga I.E., and Vasilakos J.P. Resiquimod and other immune response modifiers as vaccine adjuvants. Expert Rev Vac 6 (2007) 835-847
48. Wagner H. The immunogenicity of CpG-antigen conjugates. Adv Drug Deliv Rev 61 (2009) 243-247
49. Maraskovsky E., Schnurr M., Wilson N.S., Robson N.C., Boyle J., and Drane D. Development of prophylactic and therapeutic vaccines using the ISCOMATRIX adjuvant. Immunol Cell Biol 87 (2009) 371-376
50. Testori A., Richards J., Whitman E., Mann G.B., Lutzky J., Camacho L., Parmiani G., Tosti G., Kirkwood J.M., Hoos A., et al. Phase III comparison of vitespen, an autologous tumor-derived heat shock protein gp96 peptide complex vaccine, with physician's choice of treatment for stage IV melanoma: the C-100-21 Study Group. J Clin Oncol 26 (2008) 955-962
51. Liu T.C., and Kirn D. Systemic efficacy with oncolytic virus therapeutics: clinical proof-of-concept and future directions. Cancer Res 67 (2007) 429-432
52. Marshall J.L., Gulley J.L., Arlen P.M., Beetham P.K., Tsang K.Y., Slack R., Hodge J.W., Doren S., Grosenbach D.W., Hwang J., et al. Phase I study of sequential vaccinations with fowlpox-CEA(6D)-TRICOM alone and sequentially with vaccinia-CEA(6D)-TRICOM, with and without granulocyte-macrophage colony-stimulating factor, in patients with carcinoembryonic antigen-expressing carcinomas. J Clin Oncol 23 (2005) 720-731
53. Garcon N., Chomez P., and Van Mechelen M. GlaxoSmithKline adjuvant systems in vaccines: concepts, achievements and perspectives. Expert Rev Vac 6 (2007) 723-739
54. Skoberne M., Yewdall A., Bahjat K.S., Godefroy E., Lauer P., Lemmens E., Liu W., Luckett W., Leong M., Dubensky T.W., et al. KBMA Listeria monocytogenes is an effective vector for DC-mediated induction of antitumor immunity. J Clin Invest 118 (2008) 3990-4001. An earlier report by these researchers introduced Listeria monocytogenes as a potential vaccine platform (Nat Med 2005). This study now demonstrates that Listeria monocytogenes, engineered to express Melan-A or NY-ESO-1, activates human DCs and facilitates presentation and cross-presentation of the tumour Ags. Harnessing the inherent 'danger' provoking properties of bacteria (or viruses) is particularly attractive.
55. Shortman K., Lahoud M.H., and Caminschi I. Improving vaccines by targeting antigens to dendritic cells. Exp Mol Med 41 (2009) 61-66. An excellent review on the development of new strategies for DC in vivo targeting for enhancing vaccine efficacy.
56. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5 (2005) 263-274
57. Brode S., and Cooke A. Immune-potentiating effects of the chemotherapeutic drug cyclophosphamide. Crit Rev Immunol 28 (2008) 109-126
58. Dannull J., Su Z., Rizzieri D., Yang B.K., Coleman D., Yancey D., Zhang A., Dahm P., Chao N., Gilboa E., et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 115 (2005) 3623-3633
59. Ribas A. Anti-CTLA4 antibody clinical trials in melanoma. Update Cancer Ther 2 (2007) 133-139