Harnessing the immune system to improve cancer therapy

Annals of Translational Medicine

Volumn 4, Issue 14, 2016, Pages

  Papaioannou, Nikos E ^a   Beniata, Ourania V ^a   Vitsos, Panagiotis ^a   Tsitsilonis, Ourania ^a   Samara, Pinelopi ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

Cancer immunotherapy; Checkpoint inhibitors; Dendritic cells (DCs); Monoclonal antibodies (mAbs); Peptide vaccines

Indexed keywords

ALPHA INTERFERON; BEVACIZUMAB; CANCER VACCINE; CHIMERIC ANTIGEN RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 2; IPILIMUMAB; MONOCLONAL ANTIBODY; MUCIN 1; NANOCARRIER; NIVOLUMAB; PEMBROLIZUMAB; SIPULEUCEL T; TALIMOGENE LAHERPAREPVEC; TUMOR ANTIGEN;

ACTIVE CANCER IMMUNOTHERAPY; ADOPTIVE CELL TRANSFER; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY DEPENDENT CELLULAR PHAGOCYTOSIS; ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL; CANCER IMMUNOTHERAPY; CELL TRANSFER; CHEMORADIOTHERAPY; CLINICAL TRIAL (TOPIC); COMPLEMENT DEPENDENT CYTOTOXICITY; DENDRITIC CELL; DRUG APPROVAL; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG RESPONSE; DRUG SAFETY; DRUG TARGETING; HUMAN; IMMUNE SYSTEM; IMMUNOMODULATION; IN VIVO STUDY; MOLECULARLY TARGETED THERAPY; NONHUMAN; PASSIVE CANCER IMMUNOTHERAPY; PHAGOCYTOSIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TUMOR IMMUNITY;

EID: 85006192443     PISSN: 23055839     EISSN: 23055847     Source Type: Journal    
DOI: 10.21037/atm.2016.04.01     Document Type: Review

References (102)

1. Koebel CM, Vermi W, Swann JB, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007;450:903-7.
2. 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.
3. Gross G, Waks T, Eshhar Z. Expression of immunoglobulin T cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci U S A 1989;86:10024-8.
4. Leach DR, Krummel MF, Allison JP. Enhancement of anti-tumor immunity by CTLA-4 blockade. Science 1996;271:1734-6.
5. Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity 2006;24:19-28.
6. Racila E, Link BK, Weng WK, et al. A polymorphism in the complement component C1qA correlates with prolonged response following rituximab therapy of follicular lymphoma. Clin Cancer Res 2008;14:6697-703.
7. Dunkelberger JR, Song WC. Complement and its role in innate and adaptive immune responses. Cell Res 2010;20:34-50.
8. Lundin J, Kimby E, Björkholm M, et al. Phase II trial of subcutaneous anti-CD52 monoclonal antibody alemtuzumab (Campath-1H) as first-line treatment for patients with B-cell chronic lymphocytic leukemia (B-CLL). Blood 2002;100:768-73.
9. Albert ML, Sauter B, Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 1998;392:86-9.
10. Bross PF, Beitz J, Chen G, et al. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clin Cancer Res 2001;7:1490-6.
11. Alderson RF, Toki BE, Roberge M, et al. Characterization of a CC49-based single-chain fragment beta-lactamase fusion protein for antibody-directed enzyme prodrug therapy (ADEPT). Bioconjug Chem 2006;17:410-8.
12. Li S, Schmitz KR, Jeffrey PD, Wiltzius JJ, et al. Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 2005;7:301-11.
13. Kim R. Cetuximab and panitumumab: are they interchangeable? Lancet Oncol 2009;10:1140-1.
14. Malenfant SJ, Eckmann KR, Barnett CM. Pertuzumab: a new targeted therapy for HER2-positive metastatic breast cancer. Pharmacotherapy 2014;34:60-71.
15. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumor activity. Nat Rev Cancer 2008;8:579-91.
16. Rech AJ, Vonderheide RH. Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells. Ann N Y Acad Sci 2009;1174:99-106.
17. Suryadevara CM, Gedeon PC, Sanchez-Perez L, et al. Are BiTEs the "missing link" in cancer therapy? Oncoimmunology 2015;4:e1008339.
18. Belardelli F, Ferrantini M, Proietti E, et al. Interferonalpha in tumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002;13:119-34.
19. Gaffen SL, Liu KD. Overview of interleukin-2 function, production and clinical applications. Cytokine 2004;28:109-23.
20. Zhan HL, Gao X, Pu XY, et al. A randomized controlled trial of postoperative tumor lysate-pulsed dendritic cells and cytokine-induced killer cells immunotherapy in patients with localized and locally advanced renal cell carcinoma. Chin Med J (Engl) 2012;125:3771-7.
21. Willemen Y, Van den Bergh JM, Lion E, et al. Engineering monocyte-derived dendritic cells to secrete interferon-a enhances their ability to promote adaptive and innate anti-tumor immune effector functions. Cancer Immunol Immunother 2015;64:831-42.
22. Akaza H, Tsukamoto T, Fujioka T, et al. Combined immunotherapy with low-dose IL-2 plus IFN-alpha for metastatic renal cell carcinoma: Survival benefit for selected patients with lung metastasis and serum sodium level. Jpn J Clin Oncol 2011;41:1023-30.
23. Schwartzentruber DJ, Lawson DH, Richards JM, et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 2011;364:2119-27.
24. Kilinc MO, Aulakh KS, Nair RE, et al. Reversing tumor immune suppression with intratumoral IL-12: activation of tumor-associated T effector/memory cells, induction of T suppressor apoptosis, and infiltration of CD8+ T effectors. J Immunol 2006;177:6962-73.
25. Zhao J, Zhao J, Perlman S. Differential effects of IL-12 on Tregs and non-Treg T cells: roles of IFN-γ, IL-2 and IL-2R. PLoS ONE 2012;7:e46241.
26. Leonard JP, Sherman ML, Fisher GL, et al. Effects of single-dose interleukin-12 exposure on interleukin-12- associated toxicity and interferon-gamma production. Blood 1997;90:2541-8.
27. Rook AH, Wood GS, Yoo EK, et al. Interleukin-12 therapy of cutaneous T cell lymphoma induces lesion regression and cytotoxic T cell responses. Blood 1999;94:902-8.
28. Younes A, Pro B, Robertson MJ, et al. Phase II clinical trial of interleukin-12 in patients with relapsed and refractory non-Hodgkin's lymphoma and Hodgkin's disease. Clin Cancer Res 2004;10:5432-8.
29. Little RF, Pluda JM, Wyvill KM, et al. Activity of subcutaneous interleukin-12 in AIDS-related Kaposi sarcoma. Blood 2006;107:4650-7.
30. Daud AI, DeConti RC, Andrews S, et al. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 2008;26:5896-5903.
31. Fallon J, Tighe R, Kradjian G, et al. The immunocytokine NHS-IL12 as a potential cancer therapeutic. Oncotarget 2014;5:1869-84.
32. Rosenberg SA, Yang JC, Sherry RM, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
33. Tran E, Turcotte S, Gros A, et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science 2014;344:641-5.
34. Wei C, Wang W, Pang W, et al. The CIK cells stimulated with combination of IL-2 and IL-15 provide an improved cytotoxic capacity against human lung adenocarcinoma. Tumour Biol 2014;35:1997-2007.
35. Sangiolo D. Cytokine induced killer cells as promising immunotherapy for solid tumors. J Cancer 2011;2:363-8.
36. Introna M, Golay J, Rambaldi A. Cytokine induced killer (CIK) cells for the treatment of hematological neoplasms. Immunol Lett 2013;155:27-30.
37. Laumbacher B, Gu S, Wank R. Activated monocytes prime naive T cells against autologous cancer: vigorous cancer destruction in vitro and in vivo. Scand J Immunol 2012;75:314-28.
38. Gattinoni L, Finkelstein SE, Klebanoff CA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumorspecific CD8+ T cells. J Exp Med 2005;202:907-12.
39. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
40. Johnson LA, Morgan RA, Dudley ME, et al. Gene therapy with human and mouse T cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009;114:535-46.
41. Eshhar Z, Waks T, Gross G, et al. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T cell receptors. Proc Natl Acad Sci USA 1993;90:720-4.
42. Chmielewski M, Kopecky C, Hombach AA, et al. IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res 2011;71:5697-706.
43. Pegram HJ, Lee JC, Hayman EG, et al. Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood 2012;119:4133-41.
44. Zhang L, Kerkar SP, Yu Z, et al. Improving adoptive T cell therapy by targeting and controlling IL-12 expression to the tumor environment. Mol Ther 2011;19:751-9.
45. Urbanska K, Lanitis E, Poussin M, et al. A universal strategy for adoptive immunotherapy of cancer through use of a novel T cell antigen receptor. Cancer Res 2012;72:1844-52.
46. Tamada K, Geng D, Sakoda Y, et al. Redirecting genemodified T cells toward various cancer types using tagged antibodies. Clin Cancer Res 2012;18:6436-45.
47. Haji-Fatahaliha M, Hosseini M, Akbarian A, et al. CARmodified T cell therapy for cancer: an updated review. Artif Cells Nanomed Biotechnol 2015;11:1-11.
48. Klebanoff CA, Rosenberg SA, Restifo NP. Prospects for gene-engineered T cell immunotherapy for solid cancers. Nat Med 2016;22:26-36.
49. Carpenito C, Milone MC, Hassan R, et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci USA 2009;106:3360-5.
50. Di Stasi A, De Angelis B, Rooney CM, et al. T lymphocytes coexpressing CCR4 and a chimeric antigen receptor targeting CD30 have improved homing and anti-tumor activity in a Hodgkin tumor model. Blood 2009;113:6392-402.
51. Parente-Pereira AC, Burnet J, Ellison D, et al. Trafficking of CAR-engineered human T cells following regional or systemic adoptive transfer in SCID beige mice. J Clin Immunol 2011;31:710-8.
52. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med 2011;365:1673-83.
53. Wu CY, Roybal KT, Puchner EM, et al. Remote control of therapeutic T cells through a small molecule-gated chimeric receptor. Science 2015;350:aab4077.
54. Juillerat A, Marechal A, Filhol JM, et al. Design of chimeric antigen receptors with integrated controllable transient functions. Sci Rep 2016;6:18950.
55. Pol J, Bloy N, Buqué A, et al. Trial watch: peptide-based anti-cancer vaccines. Oncoimmunology 2015;4:e974411.
56. Gnjatic S, Nishikawa H, Jungbluth AA, et al. NY-ESO-1: review of an immunogenic tumor antigen. Adv Cancer Res 2006;95:1-30.
57. Timmerman JM, Levy R. Cancer vaccines: pessimism in check. Nat Med 2004;10:1279-80.
58. Xiao YF, Jie MM, Li BS, et al. Peptide-based treatment: a promising cancer therapy. J Immunol Res 2015;2015:761820.
59. Noguchi M, Moriya F, Koga N, et al. A randomized phase II clinical trial of personalized peptide vaccination with metronomic low-dose cyclophosphamide in patients with metastatic castration-resistant prostate cancer. Cancer Immunol Immunother 2016;65:151-60.
60. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-52.
61. Palucka K, Banchereau J.Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012;12:265-77.
62. Duewell P, Kisser U, Heckelsmiller K, et al. ISCOMATRIX adjuvant combines immune activation with antigen delivery to dendritic cells in vivo leading to effective cross-priming of CD8+ T cells. J Immunol 2011;187:55-63.
63. Obeid J, Hu Y, Slingluff CL Jr. Vaccines, adjuvants, and dendritic cell activators-current status and future challenges. Semin Oncol 2015;42:549-61.
64. Ophir E, Bobisse S, Coukos G, et al. Personalized approaches to active immunotherapy in cancer. Biochim Biophys Acta 2016;1865:72-82.
65. Koido S, Homma S, Okamoto M, et al. Strategies to improve the immunogenicity of anti-cancer vaccines based on dendritic cell/malignant cell fusions. Oncoimmunology 2013;2:e25994.
66. de Gruijl TD, van den Eertwegh AJ, Pinedo HM, et al. Whole-cell cancer vaccination: from autologous to allogeneic tumor- and dendritic cell-based vaccines. Cancer Immunol Immunother 2008;57:1569-77.
67. Le DT, Pardoll DM, Jaffee EM. Cellular vaccine approaches. Cancer J 2010;16:304-10.
68. Amedei A, Niccolai E, Prisco D. Pancreatic cancer: role of the immune system in cancer progression and vaccine-based immunotherapy. Hum Vaccin Immunother 2014;10:3354-68.
69. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol 2002;2:116-26.
70. Buchbinder E, Hodi FS. Cytotoxic T lymphocyte antigen-4 and immune checkpoint blockade. J Clin Invest 2015;125:3377-83.
71. Keir ME, Butte MJ, Freeman GJ, et al. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008;26:677-704.
72. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 2010;236:219-42.
73. Bour-Jordan H, Esensten JH, Martinez-Llordella M, et al. Intrinsic and extrinsic control of peripheral T cell tolerance by co-stimulatory molecules of the CD28/B7 family. Immunol Rev 2011;241:180-205.
74. Wherry EJ. T cell exhaustion. Nat Immunol 2011;12:492-9.
75. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12:252-64.
76. Turnis ME, Andrews LP, Vignali DA. Inhibitory receptors as targets for cancer immunotherapy. Eur J Immunol 2015;45:1892-905.
77. Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015;373:23-34.
78. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
79. Robert C, Thomas L, Bondarenko I, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517-26.
80. Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.
81. Patnaik A, Kang SP, Rasco D, et al. Phase I study of Pembrolizumab (MK-3475; Anti-PD-1 Monoclonal Antibody) in patients with advanced solid tumors. Clin Cancer Res 2015;21:4286-93.
82. Ribas A, Puzanov I, Dummer R, et al. Pembrolizumab versus investigator- choice chemotherapy for ipilimumabrefractory melanoma (KEYNOTE-002): a randomized, controlled, phase 2 trial. Lancet Oncol 2015;16:908-18.
83. Weber JS, D'Angelo SP, Minor D, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomized, controlled, open-label, phase 3 trial. Lancet Oncol 2015;16:375-84.
84. Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer. N Engl J Med 2015;373:123-35.
85. Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for Metastatic Renal Cell Carcinoma: Results of a Randomized Phase II Trial. J Clin Oncol 2015;33:1430-7.
86. Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma. N Engl J Med 2015;373:1803-13.
87. O'Sullivan Coyne G, Madan RA, Gulley JL. Nivolumab: promising survival signal coupled with limited toxicity raises expectations. J Clin Oncol 2014;32:986-8.
88. Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013;369:122-33.
89. van den Pol AN, Davis JN. Highly attenuated recombinant vesicular stomatitis virus VSV-12'GFP displays immunogenic and oncolytic activity. J Virol 2013;87:1019-34.
90. Dranoff G. GM-CSF-secreting melanoma vaccines. Oncogene 2003;22:3188-92.
91. Liu BL, Robinson M, Han ZQ, et al. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumor properties. Gene Ther 2003;10:292-303.
92. Gil M, Komorowski MP, Seshadri M, et al. CXCL12/ CXCR4 blockade by oncolytic virotherapy inhibits ovarian cancer growth by decreasing immunosuppression and targeting cancer-initiating cells. J Immunol 2014;193:5327-37.
93. Andtbacka RH, Kaufman HL, Collichio F, et al. Talimogene Laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol 2015;33:2780-8.
94. Qiao J, Kottke T, Willmon C, et al. Purging metastases in lymphoid organs using a combination of antigennonspecific adoptive T cell therapy, oncolytic virotherapy and immunotherapy. Nat Med 2008;14:37-44.
95. Qiao J, Wang H, Kottke T, et al. Loading of oncolytic vesicular stomatitis virus onto antigen-specific T cells enhances the efficacy of adoptive T cell therapy of tumors. Gene Ther 2008;15:604-16.
96. Rojas JJ, Sampath P, Hou W, et al. Defining effective combinations of immune checkpoint blockade and oncolytic virotherapy. Clin Cancer Res 2015;21:5543-51.
97. Ferguson MS, Lemoine NR, Wang Y. Systemic delivery of oncolytic viruses: hopes and hurdles. Adv Virol 2012;2012:805629.
98. Irvine DJ, Hanson MC, Rakhra K, et al. Synthetic nanoparticles for vaccines and immunotherapy. Chem Rev 2015;115:11109-11146.
99. Lin AY, Almeida JP, Bear A, et al. Gold nanoparticle delivery of modified CpG stimulates macrophages and inhibits tumor growth for enhanced immunotherapy. PLoS One 2013;8:e63550.
100. Ma W, Chen M, Kaushal S, et al. PLGA nanoparticlemediated delivery of tumor antigenic peptides elicits effective immune responses. Int J Nanomedicine 2012;7:1475-87.
101. Kono K, Mimura K, Kiessling R. Immunogenic tumor cell death induced by chemoradiotherapy: molecular mechanisms and a clinical translation. Cell Death Dis 2013;4:e688.
102. Vatner RE, Cooper BT, Vanpouille-Box C, et al. Combinations of immunotherapy and radiation in cancer therapy. Front Oncol 2014;4:325.