Reviews:
Classification of current anticancer immunotherapies
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Abstract
Lorenzo Galluzzi1,2,3,4,*, Erika Vacchelli1,2,3, José-Manuel Bravo-San Pedro1,2,3, Aitziber Buqué1,2,3, Laura Senovilla1,2,3, Elisa Elena Baracco1,2,3,5, Norma Bloy1,2,3,5, Francesca Castoldi1,2,3,5,6, Jean-Pierre Abastado7, Patrizia Agostinis8, Ron N. Apte9, Fernando Aranda1,2,3,10, Maha Ayyoub11,12, Philipp Beckhove13, Jean-Yves Blay14,15, Laura Bracci16, Anne Caignard17,18, Chiara Castelli19, Federica Cavallo20, Estaban Celis21, Vincenzo Cerundolo22, Aled Clayton23,24, Mario P. Colombo19, Lisa Coussens25, Madhav V. Dhodapkar26, Alexander M. Eggermont3, Douglas T. Fearon27, Wolf H. Fridman2,4,28,29, Jitka Fučíková6,30, Dmitry I. Gabrilovich31, Jérôme Galon2,4,28,32, Abhishek Garg8, François Ghiringhelli33,34,35, Giuseppe Giaccone36,37, Eli Gilboa38, Sacha Gnjatic39, Axel Hoos40, Anne Hosmalin4,41,42,43, Dirk Jäger44, Pawel Kalinski45,46,47, Klas Kärre48, Oliver Kepp1,2,49, Rolf Kiessling50, John M. Kirkwood51, Eva Klein48, Alexander Knuth52, Claire E. Lewis53, Roland Liblau54,55,56, Michael T. Lotze45,46, Enrico Lugli57, Jean-Pierre Mach58, Fabrizio Mattei16, Domenico Mavilio57,59, Ignacio Melero60,61, Cornelis J. Melief62,63, Elizabeth A. Mittendorf64, Lorenzo Moretta65, Adekunke Odunsi66, Hideho Okada67, Anna Karolina Palucka68, Marcus E. Peter69, Kenneth J. Pienta70, Angel Porgador9, George C. Prendergast71,72,73, Gabriel A. Rabinovich74, Nicholas P. Restifo75, Naiyer Rizvi76, Catherine Sautès-Fridman2,4,28,29, Hans Schreiber77, Barbara Seliger78, Hiroshi Shiku79, Bruno Silva-Santos80, Mark J. Smyth81,82, Daniel E. Speiser83,84, Radek Spisek6,30, Pramod K. Srivastava85,86, James E. Talmadge87, Eric Tartour4,88,89,90, Sjoerd H. Van Der Burg91, Benoît J. Van Den Eynde92,93,94, Richard Vile95, Hermann Wagner96, Jeffrey S. Weber97, Theresa L. Whiteside46,98, Jedd D. Wolchok99,100, Laurence Zitvogel3,101,102, Weiping Zou103 and Guido Kroemer1,2,4,49,104,*
1 Equipe 11 labellisée pas la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France
2 INSERM, U1138, Paris, France
3 Gustave Roussy Cancer Campus, Villejuif, France
4 Université Paris Descartes/Paris V, Sorbonne Paris Cité, Paris, France
5 Faculté de Medicine, Université Paris Sud/Paris XI, Le Kremlin-Bicêtre, France
6 Sotio a.c., Prague, Czech Republic
7 Pole d’innovation thérapeutique en oncologie, Institut de Recherches Internationales Servier, Suresnes, France
8 Cell Death Research and Therapy (CDRT) Laboratory, Dept. of Cellular and Molecular Medicine, University of Leuven, Leuven, Belgium
9 The Shraga Segal Dept. of Microbiology, Immunology and Genetics, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel
10 Group of Immune receptors of the Innate and Adaptive System, Institut d’Investigacions Biomédiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
11 INSERM, U1102, Saint Herblain, France
12 Institut de Cancérologie de l’Ouest, Saint Herblain, France
13 Translational Immunology Division, German Cancer Research Center, Heidelberg, Germany
14 Equipe 11, Centre Léon Bérard (CLR), Lyon, France
15 Centre de Recherche en Cancérologie de Lyon (CRCL), Lyon, France
16 Dept. of Hematology, Oncology and Molecular Medicine, Istituto Superiore di Sanità, Rome, Italy
17 INSERM, U1160, Paris, France
18 Groupe Hospitalier Saint Louis-Lariboisière - F. Vidal, Paris, France
19 Unit of Immunotherapy of Human Tumors, Dept. of Experimental Oncology and Molecular Medicine, Fondazione IRCCS Istituto Nazionale Tumori, Milano, Italy
20 Molecular Biotechnology Center, Dept. of Molecular Biotechnology and Health Sciences, University of Torino, Torino, Italy
21 Cancer Immunology, Inflammation and Tolerance Program, Georgia Regents University Cancer Center, Augusta, GA, USA
22 MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, UK
23 Institute of Cancer & Genetics, School of Medicine, Cardiff University, Cardiff, UK
24 Velindre Cancer Centre, Cardiff, UK
25 Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA
26 Sect. of Hematology and Immunobiology, Yale Cancer Center, Yale University, New Haven, CT, USA
27 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
28 Université Pierre et Marie Curie/Paris VI, Paris, France
29 Equipe 13, Centre de Recherche des Cordeliers, Paris, France
30 Dept. of Immunology, 2nd Faculty of Medicine and University Hospital Motol, Charles University, Prague, Czech Republic
31 Dept. of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
32 Laboratory of Integrative Cancer Immunology, Centre de Recherche des Cordeliers, Paris, France
33 INSERM, UMR866, Dijon, France
34 Centre Georges François Leclerc, Dijon, France
35 Université de Bourgogne, Dijon, France
36 Center for Cancer Research, National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, MD, USA
37 Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC, USA
38 Dept. of Microbiology and Immunology, Sylvester Comprehensive Cancer Center, University of Miami, Miller School of Medicine, Miami, FL, USA
39 Sect. of Hematology/Oncology, Immunology, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA
40 Glaxo Smith Kline, Cancer Immunotherapy Consortium, Collegeville, PA, USA
41 INSERM, U1016, Paris, France
42 CNRS, UMR8104, Paris, France
43 Hôpital Cochin, AP-HP, Paris, France
44 National Center for Tumor Diseases, University Medical Center Heidelberg, Heidelberg, Germany
45 Dept. of Surgery, University of Pittsburgh, Pittsburgh, PA, USA
46 University of Pittsburgh Cancer Institute, Hillman Cancer Center, Pittsburgh, PA, USA
47 Dept. of Immunology and Infectious Diseases and Microbiology, University of Pittsburgh, Pittsburgh, PA, USA
48 Dept. of Microbiology, Tumor and Cell Biology, Karolinska Institute, Stockholm, Sweden
49 Metabolomics and Cell Biology Platforms, Gustave Roussy Cancer Campus, Villejuif, France
50 Dept. of Oncology, Karolinska Institute Hospital, Stockholm, Sweden
51 University of Pittsburgh Cancer Institute Laboratory, Pittsburgh, PA, USA
52 National Center for Cancer Care and Research, Hamad Medical Corporation, Doha, Qatar
53 Academic Unit of Inflammation and Tumour Targeting, Dept. of Oncology, University of Sheffield Medical School, Sheffield, UK
54 INSERM, UMR1043, Toulouse, France
55 CNRS, UMR5282, Toulouse, France
56 Laboratoire d’Immunologie, CHU Toulouse, Université Toulouse II, Toulouse, France
57 Unit of Clinical and Experimental Immunology, Humanitas Clinical and Research Institute, Rozzano, Italy
58 Dept. of Biochemistry, University of Lausanne, Epalinges, Switzerland
59 Dept. of Medical Biotechnologies and Translational Medicine, University of Milan, Rozzano, Italy
60 Dept. of Immunology, Centro de Investigación Médica Aplicada (CIMA), Universidad de Navarra, Pamplona, Spain
61 Dept. of Oncology, Clínica Universidad de Navarra, Pamplona, Spain
62 ISA Therapeutics, Leiden, The Netherlands
63 Dept. of Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, The Netherlands
64 Research Dept. of Surgical Oncology, The University of Texas, MD Anderson Cancer Center, Houston, TX, USA
65 Istituto Giannina Gaslini, Genova, Italy
66 Center for Immunotherapy, Roswell Park Cancer Institute, Buffalo, NY, USA
67 Dept. of Neurological Surgery, University of California San Francisco, San Francisco, CA, USA
68 The Jackson Laboratory for Genomics Medicine, Farmington, CT, USA
69 Div. of Hematology/Oncology, Northwestern University, Feinberg School of Medicine, Chicago, IL, USA
70 The James Buchanan Brady Urological Institute, The Johns Hopkins Medical Institutions, Baltimore, MD, USA
71 Lankenau Institute for Medical Research, Wynnewood, PA, USA
72 Dept. of Pathology, Anatomy and Cell Biology, Sidney Kimmel Medical College, Philadelphia, PA, USA
73 Cell Biology and Signaling Program, Kimmel Cancer Center, Thomas Jefferson University, Philadelphia, PA, USA
74 Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME), Buenos Aires, Argentina
75 National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, MD, USA
76 Memorial Sloan Kettering Cancer Center (MSKCC), New York, NY, USA
77 Dept. of Pathology, The Cancer Research Center, The University of Chicago, Chicago, IL, USA
78 Institute of Medical Immunology, Martin Luther University Halle-Wittenberg, Halle, Germany
79 Dept. of Immuno-GeneTherapy, Mie University Graduate School of Medicine, Tsu, Japan
80 Instituto de Medicina Molecular, Universidade de Lisboa, Lisboa, Portugal
81 Immunology in Cancer and Infection Laboratory, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia
82 School of Medicine, University of Queensland, Herston, Queensland, Australia
83 Dept. of Oncology, University of Lausanne, Lausanne, Switzerland
84 Ludwig Cancer Research Center, Lausanne, Switzerland
85 Dept. of Immunology, University of Connecticut School of Medicine, Farmington, CT, USA
86 Carole and Ray Neag Comprehensive Cancer Center, Farmington, CT, USA
87 Laboratory of Transplantation Immunology, Dept. of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE, USA
88 INSERM, U970, Paris, France
89 Paris-Cardiovascular Research Center (PARCC), Paris, France
90 Service d’Immunologie Biologique, Hôpital Européen Georges Pompidou (HEGP), AP-HP, Paris, France
91 Dept. of Clinical Oncology, Leiden University Medical Center, Leiden, The Netherlands
92 Ludwig Institute for Cancer Research, Brussels, Belgium
93 de Duve Institute, Brussels, Belgium
94 Université Catholique de Louvain, Brussels, Belgium
95 Dept. of Molecular Medicine and Immunology, Mayo Clinic College of Medicine, Rochester, MN, USA
96 Institute of Medical Microbiology, Immunology and Hygiene, Technical University Munich, Munich, Germany
97 Donald A. Adam Comprehensive Melanoma Research Center, Moffitt Cancer Center, Tampa, FL, USA
98 University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
99 Dept. of Medicine and Ludwig Center, Memorial Sloan Kettering Cancer Center (MSKCC), New York, NY, USA
100 Weill Cornell Medical College, New York, NY, USA
101 INSERM, U1015, Villejuif, France
102 Centre d’Investigation Clinique Biothérapie 507 (CICBT507), Gustave Roussy Cancer Campus, Villejuif, France
103 University of Michigan, School of Medicine, Ann Arbor, MI, USA
104 Pôle de Biologie, Hôpital Européen Georges Pompidou (HEGP), AP-HP, Paris, France
* share senior co-authorship
Correspondence:
Lorenzo Galluzzi, email:
Keywords: adoptive cell transfer, checkpoint blockers, dendritic cell-based interventions, DNA-based vaccines, immunostimulatory cytokines, peptide-based vaccines, oncolytic viruses, Toll-like receptor agonists
Received: November 02, 2014 Accepted: December 15, 2014 Published: December 18, 2014
Abstract
During the past decades, anticancer immunotherapy has evolved from a promising therapeutic option to a robust clinical reality. Many immunotherapeutic regimens are now approved by the US Food and Drug Administration and the European Medicines Agency for use in cancer patients, and many others are being investigated as standalone therapeutic interventions or combined with conventional treatments in clinical studies. Immunotherapies may be subdivided into “passive” and “active” based on their ability to engage the host immune system against cancer. Since the anticancer activity of most passive immunotherapeutics (including tumor-targeting monoclonal antibodies) also relies on the host immune system, this classification does not properly reflect the complexity of the drug-host-tumor interaction. Alternatively, anticancer immunotherapeutics can be classified according to their antigen specificity. While some immunotherapies specifically target one (or a few) defined tumor-associated antigen(s), others operate in a relatively non-specific manner and boost natural or therapy-elicited anticancer immune responses of unknown and often broad specificity. Here, we propose a critical, integrated classification of anticancer immunotherapies and discuss the clinical relevance of these approaches.
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