Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients

Cancer Research

Volumn 73, Issue 3, 2013, Pages 1063-1075

  Tel, Jurjen ^a   Erik H J G Aarntzen, ^a   Baba, Tetsuro ^d   Schreibelt, Gerty ^a   Schulte, Barbara M ^a   Benitez Ribas, Daniel ^a,f   Boerman, Otto C ^b   Croockewit, Sandra ^c   Wim J G Oyen, ^b   Van Rossum, Michelle ^a   Winkels, Gregor ^e   Coulie, Pierre G ^d   Cornelis J A Punt, ^a,g   Figdor, Carl G ^a   De Vries, I Jolanda M ^a,h  

^a Department of Tumor Immunology ^*  (Netherlands)

^b Nuclear Medicine   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d DE DUVE INSTITUTE   (Belgium)

^e MILTENYI BIOTEC GMBH   (Germany)

^f HOSPITAL CLÍNIC   (Spain)

^g ACADEMIC MEDICAL CENTER   (Netherlands)

^h RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; DENDRITIC CELL VACCINE; GAMMA INTERFERON;

ADULT; AGED; ALPHA INTERFERON GENE; ANTIGEN SPECIFICITY; ARTICLE; CANCER IMMUNIZATION; CANCER PREVENTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DRUG EFFECT; DRUG SAFETY; EX VIVO STUDY; FEMALE; FLU LIKE SYNDROME; GAMMA INTERFERON GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOLOGICAL MONITORING; IMMUNOREACTIVITY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MALE; METASTATIC MELANOMA; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; TREATMENT DURATION; TREATMENT OUTCOME;

ADULT; AGED; ANTIBODY FORMATION; CELL MOVEMENT; DENDRITIC CELLS; FEMALE; HUMANS; INTERFERONS; LYMPHOCYTE ACTIVATION; MALE; MELANOMA; MIDDLE AGED; T-LYMPHOCYTES; VACCINATION;

EID: 84873460701     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2583     Document Type: Article

References (52)

1. Banchereau J, Palucka AK. Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol 2005;5:296-306.
2. denBrok MH, Nierkens S, Figdor CG, Ruers TJM, Adema GJ. Dendritic cells: tools and targets for antitumor vaccination. Expert Rev Vaccines 2005;4:699-710.
3. Nestle FO, Farkas A, Conrad C. Dendritic-cell-based therapeutic vaccination against cancer. Curr Opin Immunol 2005;17: 163-9.
4. Bakker AB, Schreurs MW, Tafazzul G, de Boer AJ, Kawakami Y, Adema GJ, et al. Identification of a novel peptide derived from the melanocyte-specific gp100 antigen as the dominant epitope recognized by an HLA-A2.1-restricted anti-melanoma CTL line. Int J Cancer 1995;62:97-102.
5. Brichard V, Van Pel A, Wolfel T, Wolfel C, De Plaen E, Lethe B, et al. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med 1993; 178:489-95.
6. Figdor CG, de Vries IJ, Lesterhuis WJ, Melief CJ. Dendritic cell immunotherapy: mapping the way. Nat Med 2004;10:475-80.
7. Schreibelt G, Benitez-Ribas D, Schuurhuis D, Lambeck AJ, van Hout-Kuijer M, Schaft N, et al. Commonly used prophylactic vaccines as an alternative for synthetically produced TLR ligands to mature monocyte-derived dendritic cells. Blood 2010;116:564-74.
8. Kadowaki N, Antonenko S, Lau JY, Liu YJ. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J Exp Med 2000;192:219-26.
9. Farkas L, Kvale EO, Johansen FE, Jahnsen FL, Lund-Johansen F. Plasmacytoid dendritic cells activate allergen-specific TH2 memory cells: modulation by CpG oligodeoxynucleotides. J Allergy Clin Immunol 2004;114:436-43.
10. Ito T, Liu YJ, Kadowaki N. Functional diversity and plasticity of human dendritic cell subsets. Int J Hematol 2005;81:188-96.
11. Cella M, Facchetti F, Lanzavecchia A, Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat Immunol 2000;1:305-10.
12. + T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood 2003;101:3520-6.
13. Salio M, Cella M, Vermi W, Facchetti F, Palmowski MJ, Smith CL, et al. Plasmacytoid dendritic cells prime IFN-gamma-secreting melanomaspecific CD8 lymphocytes and are found in primary melanoma lesions. Eur J Immunol 2003;33:1052-62.
14. Remer KA, Apetrei C, Schwarz T, Linden C, Moll H. Vaccination with plasmacytoid dendritic cells induces protection against infection with Leishmania major in mice. Eur J Immunol 2007;37:2463-73.
15. + T cell responses in vivo after viral stimulation. Blood 2004;104:1808-15.
16. Salio M, Palmowski MJ, Atzberger A, Hermans IF, Cerundolo V. CpGmatured murine plasmacytoid dendritic cells are capable of in vivo priming of functional CD8 T cell responses to endogenous but not exogenous antigens. J Exp Med 2004;199:567-79.
17. Takagi H, Fukaya T, Eizumi K, Sato Y, Sato K, Shibazaki A, et al. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 2011;35:958-71.
18. Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 2001;19:3635-48.
19. de Vries IJ, Lesterhuis WJ, Scharenborg NM, Engelen LP, Ruiter DJ, Gerritsen MJ, et al. Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin Cancer Res 2003;9:5091-100.
20. de Vries IJM, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC, et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 2005;23:1407-13.
21. de Vries IJ, Eggert AA, Scharenborg NM, Vissers JL, Lesterhuis WJ, Boerman OC, et al. Phenotypical and functional characterization of clinical grade dendritic cells. J Immunother 2002;25:429-38.
22. Eggert AAO, Schreurs MWJ, Boerman OC, Oyen WJC, de Boer AJ, Punt CJA, et al. Biodistribution and vaccine efficiency of murine dendritic cells are dependent on the route of administration. Cancer Res 1999;59:3340-5.
23. de Vries IJM, Bernsen MR, Lesterhuis WJ, Scharenborg NM, Strijk SP, Gerritsen M-JP, et al. Immunomonitoring tumor-specific T cells in delayed-type hypersensitivity skin biopsies after dendritic cell vaccination correlates with clinical outcome. J Clin Oncol 2005;23: 5779-87.
24. Labtube.tv [Internet]. Sudbury, United Kingdom: Technology Networks Ltd.; 2011 [cited 2011 Oct 11]. Available from: http://www.labtube.tv/playvideo.aspx? vid=131825.
25. Karanikas V, Lurquin C, Colau D, van Baren N, De Smet C, Lethe B, et al. Monoclonal anti-MAGE-3 CTL responses in melanoma patients displaying tumor regression after vaccination with a recombinant canarypox virus. J Immunol 2003;171:4898-904.
26. Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003;31:e154.
27. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199-206.
28. de Vries IJ, Tel J, Benitez-Ribas D, Torensma R, Figdor CG. Prophylactic vaccines mimic synthetic CpG oligonucleotides in their ability to modulate immune responses. Mol Immunol 2011;48:810-7.
29. De Vries IJ, Krooshoop DJ, Scharenborg NM, Lesterhuis WJ, Diepstra JH, Van Muijen GN, et al. Effective migration of antigen-pulsed dendritic cells to lymph nodes in melanoma patients is determined by their maturation state. Cancer Res 2003;63:12-7.
30. Conrad C, Meller S, Gilliet M. Plasmacytoid dendritic cells in the skin: to sense or not to sense nucleic acids. Semin Immunol 2009;21:101-9.
31. Treilleux I, Blay JY, Bendriss-Vermare N, Ray-Coquard I, Bachelot T, Guastalla JP, et al. Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res 2004;10:7466-74.
32. Labidi-Galy SI, Sisirak V, Meeus P, Gobert M, Treilleux I, Bajard A, et al. Quantitative and functional alterations of plasmacytoid dendritic cells contribute to immune tolerance in ovarian cancer. Cancer Res 2011;71:5423-34.
33. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011; 208:1989-2003.
34. + T cell responses through CD8{alpha}+ dendritic cells. J Exp Med 2011; 208:2005-16.
35. Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, et al. Subsets of human dendritic cell precursors express different tolllike receptors and respond to different microbial antigens. J Exp Med 2001;194:863-9.
36. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999;284:1835-7.
37. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999;5:919-23.
38. Penna G, Vulcano M, Sozzani S, Adorini L. Differential migration behavior and chemokine production by myeloid and plasmacytoid dendritic cells. Hum Immunol 2002;63:1164-71.
39. Yoneyama H, Matsuno K, Zhang Y, Nishiwaki T, Kitabatake M, Ueha S, et al. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int Immunol 2004;16:915-28.
40. Morse MA, Coleman RE, Akabani G, Niehaus N, Coleman D, Lyerly HK. Migration of human dendritic cells after injection in patients with metastatic malignancies. Cancer Res 1999;59:56-8.
41. + hematopoietic progenitor cells. Cancer Immunol Immunother 1999;48:118-22.
42. Gunzer M, Friedl P, Niggemann B, Brocker EB, Kampgen E, Zanker KS. Migration of dendritic cells within 3-D collagen lattices is dependent on tissue origin, state of maturation, and matrix structure and is maintained by proinflammatory cytokines. J Leukoc Biol 2000;67:622-9.
43. Lopez MN, Pereda C, Segal G, Munoz L, Aguilera R, Gonzalez FE, et al. Prolonged survival of dendritic cell-vaccinated melanoma patients correlates with tumor-specific delayed type IV hypersensitivity response and reduction of tumor growth factor {beta}-expressing T cells. J Clin Oncol 2009;27:945-52.
44. Brossart P, Wirths S, Stuhler G, Reichardt VL, Kanz L, Brugger W. Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood 2000;96:3102-8.
45. Lau R, Wang F, Jeffery G, Marty V, Kuniyoshi J, Bade E, et al. Phase I trial of intravenous peptide-pulsed dendritic cells in patients with metastatic melanoma. J Immunotherapy 2001;24:66-78.
46. + T cells by endogenous tumor antigen and peptide vaccines. A comparison to virusspecific T cells. Eur J Immunol 2002;32:731-41.
47. Valmori D, Dutoit V, Schnuriger V, Quiquerez A-L, Pittet MJ, Guillaume P, et al. Vaccination with a melan-Apeptide selects an oligoclonal T cell population with increased functional avidity and tumor reactivity. J Immunol 2002;168:4231-40.
48. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517-26.
49. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
50. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011;364:2507-16.
51. Lonchay C, van der Bruggen P, Connerotte T, Hanagiri T, Coulie P, Colau D, et al. Correlation between tumor regression and T cell responses in melanoma patients vaccinated with a MAGE antigen. Proc Natl Acad Sci U S A 2004;101(Suppl 2):14631-8.
52. Lesterhuis WJ, Schreibelt G, Scharenborg NM, Brouwer HM, Gerritsen MJ, Croockewit S, et al. Wild-type and modified gp100 peptide-pulsed dendritic cell vaccination of advanced melanoma patients can lead to long-term clinical responses independent of the peptide used. Cancer Immunol Immunother 2011;60:249-60.