Intranodal vaccination with mRNA-optimized dendritic cells in metastatic melanoma patients

OncoImmunology

Volumn 4, Issue 8, 2015, Pages

  Bol, Kalijn F ^a,b   Figdor, Carl G ^a   Aarntzen, Erik H J G ^a,b   Welzen, Marieke E B ^b   van Rossum, Michelle M ^b   Blokx, Willeke A M ^b   van de Rakt, Mandy W M M ^a   Scharenborg, Nicole M ^a   de Boer, Annemiek J ^a   Pots, Jeanette M ^a   olde Nordkamp, Michel A M ^a   van Oorschot, Tom G M ^a   Mus, Roel D M ^b   Croockewit, Sandra A J ^b   Jacobs, Joannes F M ^b   Schuler, Gerold ^c   Neyns, Bart ^d   Austyn, Jonathan M ^e   Punt, Cornelis J A ^f   Schreibelt, Gerty ^a   de Vries, I Jolanda M ^a,b   more..

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

DC vaccines; dendritic cell; immunotherapy; melanoma; mRNA electroporation

Indexed keywords

B7 ANTIGEN; CD40 LIGAND; CD70 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; DENDRITIC CELL VACCINE; GAMMA INTERFERON; GLYCOPROTEIN GP 100; HLA DP ANTIGEN; HLA DQ ANTIGEN; HLA DR ANTIGEN; INTERLEUKIN 12P70; KEYHOLE LIMPET HEMOCYANIN; LACTATE DEHYDROGENASE; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MONOPHENOL MONOOXYGENASE; SECONDARY LYMPHOID TISSUE CHEMOKINE; TOLL LIKE RECEPTOR 4; TUMOR ANTIGEN;

ADULT; AGED; ANTIGEN RECOGNITION; ARTICLE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; DELAYED HYPERSENSITIVITY; DISTANT METASTASIS; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLU LIKE SYNDROME; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INJECTION SITE REACTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MALE; METASTATIC MELANOMA; MIDDLE AGED; OVERALL SURVIVAL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PLASMID; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; SKIN REDNESS; SWELLING; TOXICITY; TREATMENT OUTCOME; TUMOR BIOPSY;

EID: 84940486922     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1019197     Document Type: Article

References (42)

1. R.M.Steinman, J.Banchereau. Taking dendritic cells into medicine. Nature 2007; 449:419-26; PMID:17898760; http://dx.doi.org/10.1038/nature06175
2. C.G.Figdor, I.J.de Vries, W.J.Lesterhuis, C.J.Melief. Dendritic cell immunotherapy: mapping the way. Nat Med 2004; 10:475-80; PMID:15122249; http://dx.doi.org/10.1038/nm1039
3. G.J.Adema, F.Hartgers, R.Verstraten, E.de Vries, G.Marland, S.Menon, J.Foster, Y.Xu, P.Nooyen, T.McClanahan et al. A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells. Nature 1997; 387:713-7; PMID:9192897; http://dx.doi.org/10.1038/42716
4. J.Banchereau, R.M.Steinman. Dendritic cells and the control of immunity. Nature 1998; 392:245-52; PMID:9521319; http://dx.doi.org/10.1038/32588
5. N.C.Fernandez, A.Lozier, C.Flament, P.Ricciardi-Castagnoli, D.Bellet, M.Suter, M.Perricaudet, T.Tursz, E.Maraskovsky, L.Zitvogel. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 1999; 5:405-11; PMID:10202929; http://dx.doi.org/10.1038/7403
6. W.J.Lesterhuis, E.H.Aarntzen, I.J.De Vries, D.H.Schuurhuis, C.G.Figdor, G.J.Adema, C.J.Punt. Dendritic cell vaccines in melanoma: from promise to proof? Crit Rev Oncol Hematol 2008; 66:118-34; PMID:18262431; http://dx.doi.org/10.1016/j.critrevonc.2007.12.007
7. I.J.de Vries, M.R.Bernsen, W.J.Lesterhuis, N.M.Scharenborg, S.P.Strijk, M.J.Gerritsen, D.J.Ruiter, C.G.Figdor, C.J.Punt, G.J.Adema. 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; PMID:16110035; http://dx.doi.org/10.1200/JCO.2005.06.478
8. E.H.Aarntzen, K.Bol, G.Schreibelt, J.F.Jacobs, W.J.Lesterhuis, M.M.van Rossum, G.J.Adema, C.G.Figdor, C.J.Punt, I.J.de Vries. Skin-test infiltrating lymphocytes early predict clinical outcome of dendritic cell based vaccination in metastatic melanoma. Cancer Res 2012:72:6102-10; PMID:23010076; http://dx.doi.org/10.1158/0008-5472.CAN-12-2479
9. E.S.Schultz, B.Schuler-Thurner, V.Stroobant, L.Jenne, T.G.Berger, K.Thielemanns, P.van der Bruggen, G.Schuler. Functional analysis of tumor-specific Th cell responses detected in melanoma patients after dendritic cell-based immunotherapy. J Immunol 2004; 172:1304-10; PMID:14707109; http://dx.doi.org/10.4049/jimmunol.172.2.1304
10. S.Wilgenhof, A.M.Van Nuffel, J.Corthals, C.Heirman, S.Tuyaerts, D.Benteyn, A.De Coninck, I.Van Riet, G.Verfaillie, J.Vandeloo et al. Therapeutic vaccination with an autologous mRNA electroporated dendritic cell vaccine in patients with advanced melanoma. J Immunother 2011; 34:448-56; PMID:21577140; http://dx.doi.org/10.1097/CJI.0b013e31821dcb31
11. I.J.de Vries, W.J.Lesterhuis, N.M.Scharenborg, L.P.Engelen, D.J.Ruiter, M.J.Gerritsen, S.Croockewit, C.M.Britten, R.Torensma, G.J.Adema et al. Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin Cancer Res 2003; 9:5091-100; PMID:14613986
12. H.Jonuleit, A.Giesecke-Tuettenberg, T.Tuting, B.Thurner-Schuler, T.B.Stuge, L.Paragnik, A.Kandemir, P.P.Lee, G.Schuler, J.Knop et al. A comparison of two types of dendritic cell as adjuvants for the induction of melanoma-specific T-cell responses in humans following intranodal injection. Int J Cancer 2001; 93:243-51; PMID:11410873; http://dx.doi.org/10.1002/ijc.1323
13. D.McIlroy, M.Gregoire. Optimizing dendritic cell-based anticancer immunotherapy: maturation state does have clinical impact. Cancer Immunol Immunother 2003; 52:583-91; PMID:12827310; http://dx.doi.org/10.1007/s00262-003-0414-7
14. G.Trinchieri. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003; 3:133-46; PMID:12563297; http://dx.doi.org/10.1038/nri1001
15. A.Bonehill, S.Tuyaerts, A.M.Van Nuffel, C.Heirman, T.J.Bos, K.Fostier, B.Neyns, K.Thielemans. Enhancing the T-cell stimulatory capacity of human dendritic cells by co-electroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA. Mol Ther 2008; 16:1170-80; PMID:18431362; http://dx.doi.org/10.1038/mt.2008.77
16. A.Bonehill, A.M.Van Nuffel, J.Corthals, S.Tuyaerts, C.Heirman, V.Francois, D.Colau, P.van der Bruggen, B.Neyns, K.Thielemans. Single-step antigen loading and activation of dendritic cells by mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients. Clin Cancer Res 2009; 15:3366-75; PMID:19417017; http://dx.doi.org/10.1158/1078-0432.CCR-08-2982
17. T.Kikuchi, M.A.Moore, R.G.Crystal. Dendritic cells modified to express CD40 ligand elicit therapeutic immunity against preexisting murine tumors. Blood 2000; 96:91-9; PMID:10891436
18. R.M.Cisco, Z.Abdel-Wahab, J.Dannull, S.Nair, D.S.Tyler, E.Gilboa, J.Vieweg, Y.Daaka, S.K.Pruitt. Induction of human dendritic cell maturation using transfection with RNA encoding a dominant positive toll-like receptor 4. J Immunol 2004; 172:7162-8; PMID:15153540; http://dx.doi.org/10.4049/jimmunol.172.11.7162
19. J.Borst, J.Hendriks, Y.Xiao. CD27 and CD70 in T cell and B cell activation. Curr Opin Immunol 2005; 17:275-81; PMID:15886117
20. A.M.Van Nuffel, D.Benteyn, S.Wilgenhof, L.Pierret, J.Corthals, C.Heirman, P.van der Bruggen, P.G.Coulie, B.Neyns, K.Thielemans et al. Dendritic cells loaded with mRNA encoding full-length tumor antigens prime CD4+ and CD8+ T cells in melanoma patients. Mol Ther 2012; 20:1063-74; PMID:22371843; http://dx.doi.org/10.1038/mt.2012.11
21. S.Wilgenhof, A.M.Van Nuffel, D.Benteyn, J.Corthals, C.Aerts, C.Heirman, I.Van Riet, A.Bonehill, K.Thielemans, B.Neyns. A phase IB study on intravenous synthetic mRNA electroporated dendritic cell immunotherapy in pretreated advanced melanoma patients. Ann Oncol 2013; 24:2686-93; PMID:23904461; http://dx.doi.org/10.1093/annonc/mdt245
22. P.Laverman, I.J.de Vries, N.M.Scharenborg, A.de Boer, M.Broekema, W.J.Oyen, C.G.Figdor, G.J.Adema, O.C.Boerman. Development of 111In-labeled tumor-associated antigen peptides for monitoring dendritic-cell-based vaccination. Nucl Med Biol 2006; 33:453-8; PMID:16720236; http://dx.doi.org/10.1016/j.nucmedbio.2006.02.005
23. D.A.Mitchell, S.K.Nair. RNA-transfected dendritic cells in cancer immunotherapy. J Clin Invest 2000; 106:1065-9; PMID:11067858; http://dx.doi.org/10.1172/JCI11405
24. J.C.Skipper, R.C.Hendrickson, P.H.Gulden, V.Brichard, A.Van Pel, Y.Chen, J.Shabanowitz, T.Wolfel, C.L.SlingluffJr, T.Boon et al. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J Exp Med 1996; 183:527-34; PMID:8627164; http://dx.doi.org/10.1084/jem.183.2.527
25. A.L.Zarling, S.B.Ficarro, F.M.White, J.Shabanowitz, D.F.Hunt, V.H.Engelhard. Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. J Exp Med 2000; 192:1755-62; PMID:11120772; http://dx.doi.org/10.1084/jem.192.12.1755
26. E.H.Aarntzen, I.J.De Vries, W.J.Lesterhuis, D.Schuurhuis, J.F.Jacobs, K.Bol, G.Schreibelt, R.Mus, J.H.De Wilt, J.B.Haanen et al. Targeting CD4(+) T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res 2013; 73:19-29; PMID:23087058; http://dx.doi.org/10.1158/0008-5472.CAN-12-1127
27. A.M.Van Nuffel, S.Wilgenhof, K.Thielemans, A.Bonehill. Overcoming HLA restriction in clinical trials: Immune monitoring of mRNA-loaded DC therapy. Oncoimmunology 2012; 1:1392-s4; PMID:23243604; http://dx.doi.org/10.4161/onci.20926
28. D.H.Schuurhuis, P.Verdijk, G.Schreibelt, E.H.Aarntzen, N.Scharenborg, A.de Boer, M.W.van de Rakt, M.Kerkhoff, M.J.Gerritsen, F.Eijckeler et al. In situ expression of tumor antigens by messenger RNA-electroporated dendritic cells in lymph nodes of melanoma patients. Cancer Res 2009; 69:2927-34; PMID:19318559; http://dx.doi.org/10.1158/0008-5472.CAN-08-3920
29. V.F.Van Tendeloo, P.Ponsaerts, F.Lardon, G.Nijs, M.Lenjou, C.Van Broeckhoven, D.R.Van Bockstaele, Z.N.Berneman. Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood 2001; 98:49-56; PMID:11418462; http://dx.doi.org/10.1182/blood.V98.1.49
30. D.H.Schuurhuis, W.J.Lesterhuis, M.Kramer, M.G.Looman, M.van Hout-Kuijer, G.Schreibelt, A.C.Boullart, E.H.Aarntzen, D.Benitez-Ribas, C.G.Figdor et al. Polyinosinic polycytidylic acid prevents efficient antigen expression after mRNA electroporation of clinical grade dendritic cells. Cancer Immunol Immunother 2009; 58:1109-15; PMID:19018531; http://dx.doi.org/10.1007/s00262-008-0626-y
31. N.Sanchez-Sanchez, L.Riol-Blanco, J.L.Rodriguez-Fernandez. The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J Immunol 2006; 176:5153-9; PMID:16621978; http://dx.doi.org/10.4049/jimmunol.176.9.5153
32. E.H.Aarntzen, G.Schreibelt, K.Bol, W.J.Lesterhuis, A.J.Croockewit, J.H.de Wilt, M.M.van Rossum, W.A.Blokx, J.F.Jacobs, T.Duiveman-de Boer et al. Vaccination with mRNA-electroporated dendritic cells induces robust tumor antigen-specific CD4+ and CD8+ T cells responses in stage III and IV melanoma patients. Clin Cancer Res 2012; 18:5460-70; PMID:22896657; http://dx.doi.org/10.1158/1078-0432.CCR-11-3368
33. A.M.Van Nuffel, S.Tuyaerts, D.Benteyn, S.Wilgenhof, J.Corthals, C.Heirman, B.Neyns, K.Thielemans, A.Bonehill. Epitope and HLA-type independent monitoring of antigen-specific T-cells after treatment with dendritic cells presenting full-length tumor antigens. J Immunol Methods 2012; 377:23-36; PMID:22269772; http://dx.doi.org/10.1016/j.jim.2011.12.010
34. K.Bol, E.Aarntzen, F.Hout, G.Schreibelt, J.Creemers, W.Lesterhuis, W.Gerritsen, D.Grunhagen, C.Verhoef, C.Punt et al. Favorable overall survival in stage III melanoma patients after adjuvant dendritic cell vaccination. Oncoimmunology 2015; in press.
35. W.J.Lesterhuis, G.Schreibelt, N.M.Scharenborg, H.M.Brouwer, M.J.Gerritsen, S.Croockewit, P.G.Coulie, R.Torensma, G.J.Adema, C.G.Figdor 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; PMID:21069321; http://dx.doi.org/10.1007/s00262-010-0942-x
36. W.J.Lesterhuis, I.J.de Vries, G.Schreibelt, A.J.Lambeck, E.H.Aarntzen, J.F.Jacobs, N.M.Scharenborg, M.W.van de Rakt, A.J.de Boer, S.Croockewit et al. Route of administration modulates the induction of dendritic cell vaccine-induced antigen-specific T cells in advanced melanoma patients. Clin Cancer Res 2011; 17:5725-35; PMID:21771874; http://dx.doi.org/10.1158/1078-0432.CCR-11-1261
37. S.Nair, C.McLaughlin, A.Weizer, Z.Su, D.Boczkowski, J.Dannull, J.Vieweg, E.Gilboa. Injection of immature dendritic cells into adjuvant-treated skin obviates the need for ex vivo maturation. J Immunol 2003; 171:6275-82; PMID:14634145; http://dx.doi.org/10.4049/jimmunol.171.11.6275
38. C.Linnemann, M.M.van Buuren, L.Bies, E.M.Verdegaal, R.Schotte, J.J.Calis, S.Behjati, A.Velds, H.Hilkmann, D.E.Atmioui et al. High-throughput epitope discovery reveals frequent recognition of neo-antigens by CD4+ T cells in human melanoma. Nat Med 2015; 21:81-5; PMID:25531942; http://dx.doi.org/10.1038/nm.3773
39. J.Tel, E.H.Aarntzen, T.Baba, G.Schreibelt, B.M.Schulte, D.Benitez-Ribas, O.C.Boerman, S.Croockewit, W.J.Oyen, M.van Rossum et al. Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients. Cancer Res 2013; 73:1063-75; PMID:23345163; http://dx.doi.org/10.1158/0008-5472.CAN-12-2583
40. K.F.Bol, J.Tel, I.J.de Vries, C.G.Figdor. Naturally circulating dendritic cells to vaccinate cancer patients. Oncoimmunology 2013; 2:e23431; PMID:23802086; http://dx.doi.org/10.4161/onci.23431
41. B.W.S.Neyns, J.Corthals, C.Heirman, K.Thielemans. Phase II study of autologous mRNA electroporated dendritic cells (TriMixDC-MEL) in combination with ipilimumab in patients with pretreated advanced melanoma. ASCO Meeting Abstracts 32(15_suppl): 3014.
42. E.H.Aarntzen, I.J.de Vries, J.H.Goertz, M.Beldhuis-Valkis, H.M.Brouwers, M.W.van de Rakt, R.G.van der Molen, C.J.Punt, G.J.Adema, P.J.Tacken, et al. Humoral anti-KLH responses in cancer patients treated with dendritic cell-based immunotherapy are dictated by different vaccination parameters. Cancer Immunol Immunother 2012; 61:2003-11; PMID:22527252; http://dx.doi.org/10.1007/s00262-012-1263-z