Dendritic cells in cancer immunotherapy clinical trials: Are we making progress?

Frontiers in Immunology

Volumn 4, Issue DEC, 2013, Pages

  Butterfield, Lisa H ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Antigen loading; Antigen presentation; Cancer vaccines; Dendritic cells; Tumor immunology

Indexed keywords

B7 ANTIGEN; BETA 2 MICROGLOBULIN; CD34 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; DENDRITIC CELL VACCINE; GLYCOPROTEIN GP 100; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN IDIOTYPE; INTERFERON; INTERLEUKIN 4; KEYHOLE LIMPET HEMOCYANIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MELAN A; MELANOMA ANTIGEN 1; MELANOMA ANTIGEN 3; MONOPHENOL MONOOXYGENASE; MUCIN 1; TOLL LIKE RECEPTOR; TRANSCRIPTOME; TUMOR ANTIGEN;

CANCER IMMUNOTHERAPY; CANCER PREVENTION; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL MATURATION; CLINICAL TRIAL (TOPIC); DENDRITIC CELL; DIABETES MELLITUS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL MONITORING; MELANOMA; PHASE 1 CLINICAL TRIAL (TOPIC); REVIEW;

EID: 84892144534     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00454     Document Type: Review

References (52)

1. Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med (1973) 137:1142-62. doi:10.1084/jem.137.5.1142
2. Inaba K, Steinman RM, Pack MW, Aya H, Inaba M, Sudo T, et al. Identification of proliferating dendritic cell precursors in mouse blood. J Exp Med (1992) 175:1157-67. doi:10.1084/jem.175.5.1157
3. Markowicz S, Engleman EG. Granulocyte-macrophage colony-stimulating factor promotes differentiation and survival of human peripheral blood dendritic cells in vitro. J Clin Invest (1990) 85:955-61. doi:10.1172/JCI114525
4. Romani N, Gruner S, Brang D, Kampgen E, Lenz A, Trockenbacher B, et al. Proliferating dendritic cell progenitors in human blood. J Exp Med (1994) 180:83-93. doi:10.1084/jem.180.1.83
5. Mukherji B, Chakraborty NG, Yamasaki S, Okino T, Yamase H, Sporn JR, et al. Induction of antigen-specific cytolytic T cells in situ in human melanoma by immunization with synthetic peptide-pulsed autologous antigen presenting cells. Proc Natl Acad Sci U S A (1995) 92:8078-82. doi:10.1073/pnas.92.17.8078
6. Palucka K, Ueno H, Fay J, Banchereau J. Dendritic cells and immunity against cancer. J Intern Med (2011) 269:64-73. doi:10.1111/j.1365-2796.2010.02317.x
7. Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer (2012) 12:265-77. doi:10.1038/nrc3258
8. Palucka K, Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity (2013) 39:38-48. doi:10.1016/j.immuni.2013.07.004
9. Hsu FJ, Benike C, Fagnoni F, Liles TM, Czerwinski D, Taidi B, et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat Med (1996) 2:52-8. doi:10.1038/nm0196-52
10. Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, Dummer R, et al. Vaccination of melanoma patients with peptide-or tumor lysate-pulsed dendritic cells. Nat Med (1998) 4:328-32. doi:10.1038/nm0398-328
11. Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N, Rolland A, et al. Immune and clinical responses in patients with metastatic melanoma to CD34(+) progenitor-derived dendritic cell vaccine. Cancer Res (2001) 61:6451-8.
12. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med (2004) 10:909-15. doi:10.1038/nm1100
13. Davis MM. A prescription for human immunology. Immunity (2008) 29:835-8. doi:10.1016/j.immuni.2008.12.003
14. Fuertes MB, Woo SR, Burnett B, Fu YX, Gajewski TF. Type I interferon response and innate immune sensing of cancer. Trends Immunol (2013) 34:67-73. doi:10.1016/j.it.2012.10.004
15. Galon J, Pages F, Marincola FM, Angell HK, Thurin M, Lugli A, et al. Cancer classification using the immunoscore: a worldwide task force. J Transl Med (2012) 10:205. doi:10.1186/1479-5876-10-205
16. Chang CC, Ferrone S. Immune selective pressure and HLA class I antigen defects in malignant lesions. Cancer Immunol Immunother (2007) 56:227-36. doi:10.1007/s00262-006-0183-1
17. Lopez-Albaitero A, Nayak JV, Ogino T, Machandia A, Gooding W, Deleo AB, et al. Role of antigen-processing machinery in the in vitro resistance of squamous cell carcinoma of the head and neck cells to recognition by CTL. J Immunol (2006) 176:3402-9.
18. Trefzer U, Hofmann M, Reinke S, Guo YJ, Audring H, Spagnoli G, et al. Concordant loss of melanoma differentiation antigens in synchronous and asynchronous melanoma metastases: implications for immunotherapy. Melanoma Res (2006) 16:137-45. doi:10.1097/01.cmr.0000200489.55099.20
19. Janssen EM, Droin NM, Lemmens EE, Pinkoski MJ, Bensinger SJ, Ehst BD, et al. CD4+ T-cell help controls CD8+ T-cell memory via TRAIL-mediated activation-induced cell death. Nature (2005) 434:88-93. doi:10.1038/nature03337
20. Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res (2009) 15:5323-37. doi:10.1158/1078-0432.CCR-09-0737
21. Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, Kapsenberg ML, et al. alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res (2004) 64:5934-7. doi:10.1158/0008-5472.CAN-04-1261
22. Giannoukakis N, Phillips B, Finegold D, Harnaha J, Trucco M. Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care (2011) 34:2026-32. doi:10.2337/dc11-0472
23. Ezzelarab MB, Zahorchak AF, Lu L, Morelli AE, Chalasani G, Demetris AJ, et al. Regulatory dendritic cell infusion prolongs kidney allograft survival in nonhuman primates. Am J Transplant (2013) 13:1989-2005. doi:10.1111/ajt.12310
24. Butterfield LH, Ribas A, Dissette VB, Amarnani SN, Vu HT, Oseguera D, et al. Determinant spreading associated with clinical response in dendritic cell-based immunotherapy for malignant melanoma. Clin Cancer Res (2003) 9:998-1008.
25. Grover A, Kim GJ, Lizee G, Tschoi M, Wang G, Wunderlich JR, et al. Intralymphatic dendritic cell vaccination induces tumor antigen-specific, skin-homing T lymphocytes. Clin Cancer Res (2006) 12:5801-8. doi:10.1158/1078-0432.CCR-05-2421
26. de Vries IJ, 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. doi:10.1038/nbt1154
27. Kvistborg P, Boegh M, Pedersen AW, Claesson MH, Zocca MB. Fast generation of dendritic cells. Cell Immunol (2009) 260:56-62. doi:10.1016/j.cellimm.2009.09.003
28. Engell-Noerregaard L, Hansen TH, Andersen MH, Thor Straten P, Svane IM. 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 (2009) 58:1-14. doi:10.1007/s00262-008-0568-4
29. Schadendorf D, Hauschild A, Ugurel S, Thoelke A, Egberts F, Kreissig M, et al. Dose-intensified bi-weekly temozolomide in patients with asymptomatic brain metastases from malignant melanoma: a phase II DeCOG/ADO study. Ann Oncol (2006) 17:1592-7. doi:10.1093/annonc/mdl148
30. Wierecky J, Muller MR, Wirths S, Halder-Oehler E, Dorfel D, Schmidt SM, et al. Immunologic and clinical responses after vaccinations with peptide-pulsed dendritic cells in metastatic renal cancer patients. Cancer Res (2006) 66:5910-8. doi:10.1158/0008-5472.CAN-05-3905
31. Van Tendeloo VF, van de Velde A, van Driessche A, Cools N, Anguille S, Ladell K, 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) 107:13824-9. doi:10.1073/pnas.1008051107
32. Rosenblatt J, Avivi I, Vasir B, Uhl L, Munshi NC, Katz T, et al. Vaccination with dendritic cell/tumor fusions following autologous stem cell transplant induces immunologic and clinical responses in multiple myeloma patients. Clin Cancer Res (2013) 19:3640-8. doi:10.1158/1078-0432.CCR-13-0282
33. Finn OJ. Cancer immunology. N Engl J Med (2008) 358:2704-15. doi:10.1056/NEJMra072739
34. Kimura T, Mckolanis JR, Dzubinski LA, Islam K, Potter DM, Salazar AM, et al. MUC1 vaccine for individuals with advanced adenoma of the colon: a cancer immunoprevention feasibility study. Cancer Prev Res (Phila) (2013) 6:18-26. doi:10.1158/1940-6207.CAPR-12-0275
35. Beatty P, Ranganathan S, Finn OJ. Prevention of colitis-associated colon cancer using a vaccine to target abnormal expression of the MUC1 tumor antigen. Oncoimmunology (2012) 1:263-70. doi:10.4161/onci.18950
36. Chiang CL, Kandalaft LE, Tanyi J, Hagemann AR, Motz GT, Svoronos N, et al. A dendritic cell vaccine pulsed with autologous hypochlorous acid-oxidized ovarian cancer lysate primes effective broad antitumor immunity: from bench to bedside. Clin Cancer Res (2013) 19:4801-15. doi:10.1158/1078-0432.CCR-13-1185
37. Olin MR, Andersen BM, Zellmer DM, Grogan PT, Popescu FE, Xiong Z, et al. Superior efficacy of tumor cell vaccines grown in physiologic oxygen. Clin Cancer Res (2010) 16:4800-8. doi:10.1158/1078-0432.CCR-10-1572
38. 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.
39. 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.
40. Quillien V, Moisan A, Carsin A, Lesimple T, Lefeuvre C, Adamski H, et al. Biodistribution of radiolabelled human dendritic cells injected by various routes. Eur J Nucl Med Mol Imaging (2005) 32:731-41. doi:10.1007/s00259-005-1825-9
41. Helfer BM, Balducci A, Nelson AD, Janjic JM, Gil RR, Kalinski P, et al. Functional assessment of human dendritic cells labeled for in vivo (19)F magnetic resonance imaging cell tracking. Cytotherapy (2010) 12:238-50. doi:10.3109/14653240903446902
42. Kalinski P, Edington H, Zeh HJ, Okada H, Butterfield LH, Kirkwood JM, et al. Dendritic cells in cancer immunotherapy: vaccines or autologous transplants? Immunol Res (2011) 50:235-47. doi:10.1007/s12026-011-8224-z
43. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol (2011) 8:151-60. doi:10.1038/nrclinonc.2010.223
44. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secretally: immunostimulation by anticancer drugs. Nat Rev Drug Discov (2012) 11:215-33. doi:10.1038/nrd3626
45. Jin P, Han TH, Ren J, Saunders S, Wang E, Marincola FM, et al. Molecular signatures of maturing dendritic cells: implications for testing the quality of dendritic cell therapies. J Transl Med (2010) 8:4. doi:10.1186/1479-5876-8-4
46. Castiello L, Sabatino M, Zhao Y, Tumaini B, Ren J, Ping J, et al. Quality controls in cellular immunotherapies: rapid assessment of clinical grade dendritic cells by gene expression profiling. Mol Ther (2013) 21:476-84. doi:10.1038/mt.2012.89
47. Butterfield LH, Gooding W, Whiteside TL. Development of a potency assay for human dendritic cells: IL-12p70 production. J Immunother (2008) 31:89-100. doi:10.1097/CJI.0b013e318158fce0
48. Okada H, Kalinski P, Ueda R, Hoji A, Kohanbash G, Donegan TE, et al. Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol (2011) 29:330-6. doi:10.1200/JCO.2010.30.7744
49. Butterfield LH, Palucka AK, Britten CM, Dhodapkar MV, Hakansson L, Janetzki S, et al. Recommendations from the iSBTc-SITC/FDA/NCI Workshop on Immunotherapy Biomarkers. Clin Cancer Res (2011) 17:3064-76. doi:10.1158/1078-0432.CCR-10-2234
50. Britten CM, Janetzki S, Butterfield LH, Ferrari G, Gouttefangeas C, Huber C, et al. T cell assays and MIATA: the essential minimum for maximum impact. Immunity (2012) 37:1-2. doi:10.1016/j.immuni.2012.07.010
51. Nicolette CA, Healey D, Tcherepanova I, Whelton P, Monesmith T, Coombs L, et al. Dendritic cells for active immunotherapy: optimizing design and manufacture in order to develop commercially and clinically viable products. Vaccine (2007) 25(Suppl 2):B47-60. doi:10.1016/j.vaccine.2007.06.006
52. Galluzzi L, Senovilla L, Vacchelli E, Eggermont A, Fridman WH, Galon J, et al. Trial watch: dendritic cell-based interventions for cancer therapy. Oncoimmunology (2012) 1:1111-34. doi:10.4161/onci.21494