Intravenous and intradermal TriMix-dendritic cell therapy results in a broad T-cell response and durable tumor response in a chemorefractory stage IV-M1c melanoma patient

Cancer Immunology, Immunotherapy

Volumn 61, Issue 7, 2012, Pages 1033-1043

  Van Nuffel, An M T ^a   Benteyn, Daphné ^a   Wilgenhof, Sofie ^a,b   Corthals, Jurgen ^a   Heirman, Carlo ^a   Neyns, Bart ^a,b   Thielemans, Kris ^a,b   Bonehill, Aude ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

Administration route; Dendritic cell; Immunotherapy; Melanoma; TriMix

Indexed keywords

ALPHA2B INTERFERON; CD40 LIGAND; CD70 ANTIGEN; DACARBAZINE; EPITOPE; FLUORODEOXYGLUCOSE F 18; MELANOMA ANTIGEN; MELANOMA ANTIGEN 3; MELANOMA ANTIGEN C2; MESSENGER RNA; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ADULT; ANTIGEN DETECTION; ARTICLE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER STAGING; CASE REPORT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL LEVEL; CELL THERAPY; COMPUTER ASSISTED EMISSION TOMOGRAPHY; DENDRITIC CELL; DRUG HYPERSENSITIVITY; DRUG MEGADOSE; DRUG UPTAKE; ERYTHEMA; HUMAN; HUMAN TISSUE; LOCAL SKIN REACTION; LYMPHADENECTOMY; MALE; MELANOMA; MELANOMA SKIN CANCER; METASTATIC MELANOMA; MULTIPLE CYCLE TREATMENT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SKIN SWELLING; T LYMPHOCYTE; TREATMENT RESPONSE; TUMOR BIOPSY;

AMINO ACID SEQUENCE; ANTIGENS, CD70; CD40 LIGAND; DENDRITIC CELLS; ELECTROPORATION; HELIUM; HUMANS; HYPERSENSITIVITY, DELAYED; IMMUNOTHERAPY, ADOPTIVE; MALE; MELANOMA; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NEOPLASM STAGING; NITROGEN; OXYGEN; PROSPECTIVE STUDIES; RNA, MESSENGER; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 4;

EID: 84862772889     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1176-2     Document Type: Article

References (43)

1. MB Lens M Dawes 2004 Global perspectives of contemporary epidemiological trends of cutaneous malignant melanoma Br J Dermatol 150 2 179 185 14996086 10.1111/j.1365-2133.2004.05708.x 1:STN:280:DC%2BD2c7gsFarsg%3D%3D
2. CM Balch JE Gershenwald SJ Soong JF Thompson MB Atkins DR Byrd AC Buzaid AJ Cochran DG Coit S Ding AM Eggermont KT Flaherty PA Gimotty JM Kirkwood KM McMasters MC Mihm Jr. DL Morton MI Ross AJ Sober VK Sondak 2009 Final version of 2009 AJCC melanoma staging and classification J Clin Oncol 27 36 6199 6206 19917835 10.1200/JCO.2009.23.4799
3. T Boon PG Coulie BJ Van den Eynde P van der Bruggen 2006 Human T cell responses against melanoma Annu Rev Immunol 24 175 208 16551247 10.1146/annurev.immunol.24.021605.090733 1:CAS:528:DC%2BD28XkvFSqt7o%3D
4. FS Hodi SJ O'Day DF McDermott RW Weber JA Sosman JB Haanen R Gonzalez C Robert D Schadendorf JC Hassel W Akerley AJ van den Eertwegh J Lutzky P Lorigan JM Vaubel GP Linette D Hogg CH Ottensmeier C Lebbe C Peschel I Quirt JI Clark JD Wolchok JS Weber J Tian MJ Yellin GM Nichol A Hoos WJ Urba 2010 Improved survival with ipilimumab in patients with metastatic melanoma N Engl J Med 363 8 711 723 20525992 10.1056/NEJMoa1003466 1:CAS:528:DC%2BC3cXhtVCrtrbN
5. C Robert L Thomas I Bondarenko S O'Day M DJ C Garbe C Lebbe JF Baurain A Testori JJ Grob N Davidson J Richards M Maio A Hauschild WH Miller P Gascon M Lotem K Harmankaya R Ibrahim S Francis TT Chen R Humphrey A Hoos JD Wolchok 2011 Ipilimumab plus dacarbazine for previously untreated metastatic melanoma N Engl J Med 364 26 2517 2526 21639810 10.1056/NEJMoa1104621 1:CAS:528: DC%2BC3MXosVegtro%3D
6. DJ Schwartzentruber DH Lawson JM Richards RM Conry DM Miller J Treisman F Gailani L Riley K Conlon B Pockaj KL Kendra RL White R Gonzalez TM Kuzel B Curti PD Leming ED Whitman J Balkissoon DS Reintgen H Kaufman FM Marincola MJ Merino SA Rosenberg P Choyke D Vena P Hwu 2011 gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma N Engl J Med 364 22 2119 2127 21631324 10.1056/NEJMoa1012863 1:CAS:528:DC%2BC3MXnt1Cmt7Y%3D
7. J Banchereau RM Steinman 1998 Dendritic cells and the control of immunity Nature 392 6673 245 252 9521319 10.1038/32588 1:CAS:528:DyaK1cXitFWrsr8%3D
8. K Palucka H Ueno J Fay J Banchereau 2011 Dendritic cells and immunity against cancer J Intern Med 269 1 64 73 21158979 10.1111/j.1365-2796.2010.02317. x 1:CAS:528:DC%2BC3MXhsFKms7g%3D
9. S Tuyaerts JL Aerts J Corthals B Neyns C Heirman K Breckpot K Thielemans A Bonehill 2007 Current approaches in dendritic cell generation and future implications for cancer immunotherapy Cancer Immunol Immunother 56 10 1513 1537 17503040 10.1007/s00262-007-0334-z 1:CAS:528:DC%2BD2sXotVKksLY%3D
10. WJ Lesterhuis EH Aarntzen IJ De Vries DH Schuurhuis CG Figdor GJ Adema CJ Punt 2008 Dendritic cell vaccines in melanoma: from promise to proof? Crit Rev Oncol Hematol 66 2 118 134 18262431 10.1016/j.critrevonc.2007.12.007 1:STN:280:DC%2BD1c3islCqsA%3D%3D
11. AM Van Nuffel J Corthals B Neyns C Heirman K Thielemans A Bonehill 2010 Immunotherapy of cancer with dendritic cells loaded with tumor antigens and activated through mRNA electroporation Methods Mol Biol 629 405 452 20387165
12. DW Mullins SL Sheasley RM Ream TN Bullock YX Fu VH Engelhard 2003 Route of immunization with peptide-pulsed dendritic cells controls the distribution of memory and effector T cells in lymphoid tissues and determines the pattern of regional tumor control J Exp Med 198 7 1023 1034 14530375 10.1084/jem.20021348 1:CAS:528:DC%2BD3sXotVWgs78%3D
13. L Fong D Brockstedt C Benike L Wu EG Engleman 2001 Dendritic cells injected via different routes induce immunity in cancer patients J Immunol 166 6 4254 4259 11238679 1:CAS:528:DC%2BD3MXitVGmt70%3D
14. SL Sheasley-O'Neill CC Brinkman AR Ferguson MC Dispenza VH Engelhard 2007 Dendritic cell immunization route determines integrin expression and lymphoid and nonlymphoid tissue distribution of CD8 T cells J Immunol 178 3 1512 1522 17237400
15. AR Ferguson LA Nichols AL Zarling ED Thompson CC Brinkman KM Hargadon TN Bullock VH Engelhard 2008 Strategies and challenges in eliciting immunity to melanoma Immunol Rev 222 28 42 18363993 10.1111/j.1600-065X.2008.00620.x 1:CAS:528:DC%2BD1cXlsFejtrw%3D
16. A Bonehill AM Van Nuffel J Corthals S Tuyaerts C Heirman V Francois D Colau P van der Bruggen B Neyns K Thielemans 2009 Single-step antigen loading and activation of dendritic cells by mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients Clin Cancer Res 15 10 3366 3375 19417017 10.1158/1078-0432.CCR-08-2982 1:CAS:528:DC%2BD1MXmtVKmu74%3D
17. A Bonehill C Heirman S Tuyaerts A Michiels K Breckpot F Brasseur Y Zhang P Van Der Bruggen K Thielemans 2004 Messenger RNA-electroporated dendritic cells presenting MAGE-A3 simultaneously in HLA class I and class II molecules J Immunol 172 11 6649 6657 15153480 1:CAS:528:DC%2BD2cXktFSksbk%3D
18. A Bonehill S Tuyaerts AM Van Nuffel C Heirman TJ Bos K Fostier B Neyns K Thielemans 2008 Enhancing the T-cell stimulatory capacity of human dendritic cells by co-electroporation with CD40L, CD70 and constitutively active TLR4 encoding mRNA Mol Ther 16 6 1170 1180 18431362 10.1038/mt.2008.77 1:CAS:528:DC%2BD1cXmt1Orsrc%3D
19. S Wilgenhof AM Van Nuffel J Corthals C Heirman S Tuyaerts D Benteyn A De Coninck I Van Riet G Verfaillie J Vandeloo A Bonehill K Thielemans B Neyns 2011 Therapeutic vaccination with an autologous mRNA electroporated dendritic cell vaccine in patients with advanced melanoma J Immunother 34 5 448 456 21577140 10.1097/CJI.0b013e31821dcb31 1:CAS:528:DC%2BC3MXmt1ymtro%3D
20. Adema GJ, de Vries IJ, Punt CJ, Figdor CG (2005) Migration of dendritic cell based cancer vaccines: in vivo veritas? Curr Opin Immunol 17(2):170-174
21. EC Butcher M Williams K Youngman L Rott M Briskin 1999 Lymphocyte trafficking and regional immunity Adv Immunol 72 209 253 10361577 10.1016/S0065-2776(08)60022-X 1:CAS:528:DyaK1MXlsFGksbc%3D
22. AR Ferguson VH Engelhard 2010 CD8 T cells activated in distinct lymphoid organs differentially express adhesion proteins and coexpress multiple chemokine receptors J Immunol 184 8 4079 4086 20212096 10.4049/jimmunol.0901903 1:CAS:528:DC%2BC3cXkt1Wqsbw%3D
23. Y Morikawa K Tohya H Ishida N Matsuura K Kakudo 1995 Different migration patterns of antigen-presenting cells correlate with Th1/Th2-type responses in mice Immunology 85 4 575 581 7558152 1:CAS:528:DyaK2MXns1ymu7o%3D
24. MA Morse RE Coleman G Akabani N Niehaus D Coleman HK Lyerly 1999 Migration of human dendritic cells after injection in patients with metastatic malignancies Cancer Res 59 1 56 58 9892184 1:CAS:528:DyaK1MXmsFOhsA%3D%3D
25. A Grover GJ Kim G Lizee M Tschoi G Wang JR Wunderlich SA Rosenberg ST Hwang P Hwu 2006 Intralymphatic dendritic cell vaccination induces tumor antigen-specific, skin-homing T lymphocytes Clin Cancer Res 12 19 5801 5808 17020987 10.1158/1078-0432.CCR-05-2421 1:CAS:528:DC%2BD28XhtVartbjO
26. PW Kantoff CS Higano ND Shore ER Berger EJ Small DF Penson CH Redfern AC Ferrari R Dreicer RB Sims Y Xu MW Frohlich PF Schellhammer 2010 Sipuleucel-T immunotherapy for castration-resistant prostate cancer N Engl J Med 363 5 411 422 20818862 10.1056/NEJMoa1001294 1:CAS:528:DC%2BC3cXhtVGlurrN
27. L Engell-Noerregaard TH Hansen MH Andersen P Thor Straten IM Svane 2009 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 1 1 14 18719915 10.1007/s00262-008-0568-4 1:CAS:528:DC%2BD1cXht1yqs7nJ
28. M Ayyoub D Rimoldi P Guillaume P Romero JC Cerottini D Valmori D Speiser 2003 Tumor-reactive, SSX-2-specific CD8+ T cells are selectively expanded during immune responses to antigen-expressing tumors in melanoma patients Cancer Res 63 17 5601 5606 14500401 1:CAS:528:DC%2BD3sXntlers7o%3D
29. S Gnjatic D Atanackovic E Jager M Matsuo A Selvakumar NK Altorki RG Maki B Dupont G Ritter YT Chen A Knuth LJ Old 2003 Survey of naturally occurring CD4+ T cell responses against NY-ESO-1 in cancer patients: correlation with antibody responses Proc Natl Acad Sci USA 100 15 8862 8867 12853579 10.1073/pnas. 1133324100 1:CAS:528:DC%2BD3sXlvVyitLg%3D
30. E Sato SH Olson J Ahn B Bundy H Nishikawa F Qian AA Jungbluth D Frosina S Gnjatic C Ambrosone J Kepner T Odunsi G Ritter S Lele YT Chen H Ohtani LJ Old K Odunsi 2005 Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer Proc Natl Acad Sci USA 102 51 18538 18543 16344461 10.1073/pnas. 0509182102 1:CAS:528:DC%2BD28Xpt1Om
31. T Hanagiri N van Baren B Neyns T Boon PG Coulie 2006 Analysis of a rare melanoma patient with a spontaneous CTL response to a MAGE-A3 peptide presented by HLA-A1 Cancer Immunol Immunother 55 2 178 184 16187089 10.1007/s00262-005- 0063-0
32. DE Speiser P Baumgaertner C Barbey V Rubio-Godoy A Moulin P Corthesy E Devevre PY Dietrich D Rimoldi D Lienard JC Cerottini P Romero N Rufer 2006 A novel approach to characterize clonality and differentiation of human melanoma-specific T cell responses: spontaneous priming and efficient boosting by vaccination J Immunol 177 2 1338 1348 16818795 1:CAS:528:DC%2BD28XmsVaku7Y%3D
33. van der Bruggen P, Stroobant V, Vigneron N, Van den Eynde B. http://www.cancerimmunity.org/peptidedatabase/Tcellepitopes.htm. Accessed 28 June 2011
34. E De Plaen K Arden C Traversari JJ Gaforio JP Szikora C De Smet F Brasseur P van der Bruggen B Lethe C Lurquin, et al. 1994 Structure, chromosomal localization, and expression of 12 genes of the MAGE family Immunogenetics 40 5 360 369 7927540 10.1007/BF01246677 1:CAS:528:DyaK2MXivFSktbo%3D
35. V Corbiere J Chapiro V Stroobant W Ma C Lurquin B Lethe N van Baren BJ Van den Eynde T Boon PG Coulie 2011 Antigen spreading contributes to MAGE vaccination-induced regression of melanoma metastases Cancer Res 71 4 1253 1262 21216894 10.1158/0008-5472.CAN-10-2693 1:CAS:528:DC%2BC3MXhvFSjsL8%3D
36. N Hardwick B Chain 2011 Epitope spreading contributes to effective immunotherapy in metastatic melanoma patients Immunotherapy 3 6 731 733 21668310 10.2217/imt.11.62 1:CAS:528:DC%2BC3MXntlGltr4%3D
37. IJ de Vries MR Bernsen WJ Lesterhuis NM Scharenborg SP Strijk MJ Gerritsen DJ Ruiter CG Figdor CJ Punt GJ Adema 2005 Immunomonitoring tumor-specific T cells in delayed-type hypersensitivity skin biopsies after dendritic cell vaccination correlates with clinical outcome J Clin Oncol 23 24 5779 5787 16110035 10.1200/JCO.2005.06.478
38. F Edele R Molenaar D Gutle JC Dudda T Jakob B Homey R Mebius M Hornef SF Martin 2008 Cutting edge: instructive role of peripheral tissue cells in the imprinting of T cell homing receptor patterns J Immunol 181 6 3745 3749 18768825 1:CAS:528:DC%2BD1cXhtVKntLzN
39. Q Chen H Jackson M Shackleton P Parente W Hopkins S Sturrock D MacGregor E Maraskovsky TY Tai N Dimopoulos KA Masterman T Luke ID Davis W Chen J Cebon 2005 Characterization of antigen-specific CD8+ T lymphocyte responses in skin and peripheral blood following intradermal peptide vaccination Cancer Immun 5 5 15755075
40. G Bioley C Jandus S Tuyaerts D Rimoldi WW Kwok DE Speiser JM Tiercy K Thielemans JC Cerottini P Romero 2006 Melan-A/MART-1-specific CD4 T cells in melanoma patients: identification of new epitopes and ex vivo visualization of specific T cells by MHC class II tetramers J Immunol 177 10 6769 6779 17082590 1:CAS:528:DC%2BD28XhtFGrtrzN
41. JA Kyte S Trachsel B Risberg P thor Straten K Lislerud G Gaudernack 2009 Unconventional cytokine profiles and development of T cell memory in long-term survivors after cancer vaccination Cancer Immunol Immunother 58 10 1609 1626 19221745 10.1007/s00262-009-0670-2 1:CAS:528:DC%2BD1MXptVent7k%3D
42. EM Suso S Dueland AM Rasmussen T Vetrhus S Aamdal G Kvalheim G Gaudernack 2011 hTERT mRNA dendritic cell vaccination: complete response in a pancreatic cancer patient associated with response against several hTERT epitopes Cancer Immunol Immunother 60 6 809 818 21365467 10.1007/s00262-011-0991-9 1:CAS:528:DC%2BC3MXmsVajtL8%3D
43. F Annunziato S Romagnani 2009 Heterogeneity of human effector CD4+ T cells Arthritis Res Ther 11 6 257 20053303 10.1186/ar2843