Oncotarget

Reviews:

Classification of current anticancer immunotherapies

Lorenzo Galluzzi _, Erika Vacchelli, José-Manuel Bravo-San Pedro, Aitziber Buqué, Laura Senovilla, Elisa Elena Baracco, Norma Bloy, Francesca Castoldi, Jean-Pierre Abastado, Patrizia Agostinis, Ron N. Apte, Fernando Aranda, Maha Ayyoub, Philipp Beckhove, Jean-Yves Blay, Laura Bracci, Anne Caignard, Chiara Castelli, Federica Cavallo, Estaban Celis, Vincenzo Cerundolo, Aled Clayton, Mario P. Colombo, Lisa Coussens, Madhav V. Dhodapkar, Alexander M. Eggermont, Douglas T. Fearon, Wolf H. Fridman, Jitka Fučíková, Dmitry I. Gabrilovich, Jérôme Galon, Abhishek Garg, François Ghiringhelli, Giuseppe Giaccone, Eli Gilboa, Sacha Gnjatic, Axel Hoos, Anne Hosmalin, Dirk Jäger, Pawel Kalinski, Klas Kärre, Oliver Kepp, Rolf Kiessling, John M. Kirkwood, Eva Klein, Alexander Knuth, Claire E. Lewis, Roland Liblau, Michael T. Lotze, Enrico Lugli, Jean-Pierre Mach, Fabrizio Mattei, Domenico Mavilio, Ignacio Melero, Cornelis J. Melief, Elizabeth A. Mittendorf, Lorenzo Moretta, Adekunke Odunsi, Hideho Okada, Anna Karolina Palucka, Marcus E. Peter, Kenneth J. Pienta, Angel Porgador, George C. Prendergast, Gabriel A. Rabinovich, Nicholas P. Restifo, Naiyer Rizvi, Catherine Sautès-Fridman, Hans Schreiber, Barbara Seliger, Hiroshi Shiku, Bruno Silva-Santos, Mark J. Smyth, Daniel E. Speiser, Radek Spisek, Pramod K. Srivastava, James E. Talmadge, Eric Tartour, Sjoerd H. Van Der Burg, Benoît J. Van Den Eynde, Richard Vile, Hermann Wagner, Jeffrey  S. Weber, Theresa L. Whiteside, Jedd D. Wolchok, Laurence Zitvogel, Weiping Zou, Guido Kroemer

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Oncotarget. 2014; 5:12472-12508. https://doi.org/10.18632/oncotarget.2998

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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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