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, Esteban Celis & 68 others Vincenzo Cerundolo, Aled Clayton, Mario P. Colombo, Lisa Coussens, Madhav V. Dhodapkar, Alexander M. Eggermont, Douglas T. Fearon, Wolf H. Fridman, Jitka Fucíková, 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

Research output: Contribution to journalArticle

192 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)12472-12508
Number of pages37
JournalOncotarget
Volume5
Issue number24
DOIs
StatePublished - Jan 1 2014

Fingerprint

Immunotherapy
Immune System
Neoplasms
Neoplasm Antigens
United States Food and Drug Administration
Therapeutics
Monoclonal Antibodies
Antigens
Pharmaceutical Preparations

Keywords

  • Adoptive cell transfer
  • Checkpoint blockers
  • DNA-based vaccines
  • Dendritic cell-based interventions
  • Immunostimulatory cytokines
  • Oncolytic viruses
  • Peptide-based vaccines
  • Toll-like receptor agonists

ASJC Scopus subject areas

  • Oncology

Cite this

Galluzzi, L., Vacchelli, E., Bravo-San Pedro, J. M., Buqué, A., Senovilla, L., Baracco, E. E., ... Kroemer, G. (2014). Classification of current anticancer immunotherapies. Oncotarget, 5(24), 12472-12508. https://doi.org/10.18632/oncotarget.2998

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

In: Oncotarget, Vol. 5, No. 24, 01.01.2014, p. 12472-12508.

Research output: Contribution to journalArticle

Galluzzi, L, Vacchelli, E, Bravo-San Pedro, JM, Buqué, A, Senovilla, L, Baracco, EE, Bloy, N, Castoldi, F, Abastado, JP, Agostinis, P, Apte, RN, Aranda, F, Ayyoub, M, Beckhove, P, Blay, JY, Bracci, L, Caignard, A, Castelli, C, Cavallo, F, Celis, E, Cerundolo, V, Clayton, A, Colombo, MP, Coussens, L, Dhodapkar, MV, Eggermont, AM, Fearon, DT, Fridman, WH, Fucíková, J, Gabrilovich, DI, Galon, J, Garg, A, Ghiringhelli, F, Giaccone, G, Gilboa, E, Gnjatic, S, Hoos, A, Hosmalin, A, Jäger, D, Kalinski, P, Kärre, K, Kepp, O, Kiessling, R, Kirkwood, JM, Klein, E, Knuth, A, Lewis, CE, Liblau, R, Lotze, MT, Lugli, E, Mach, JP, Mattei, F, Mavilio, D, Melero, I, Melief, CJ, Mittendorf, EA, Moretta, L, Odunsi, A, Okada, H, Palucka, AK, Peter, ME, Pienta, KJ, Porgador, A, Prendergast, GC, Rabinovich, GA, Restifo, NP, Rizvi, N, Sautès-Fridman, C, Schreiber, H, Seliger, B, Shiku, H, Silva-Santos, B, Smyth, MJ, Speiser, DE, Spisek, R, Srivastava, PK, Talmadge, JE, Tartour, E, Van Der Burg, SH, Van Den Eynde, BJ, Vile, R, Wagner, H, Weber, JS, Whiteside, TL, Wolchok, JD, Zitvogel, L, Zou, W & Kroemer, G 2014, 'Classification of current anticancer immunotherapies', Oncotarget, vol. 5, no. 24, pp. 12472-12508. https://doi.org/10.18632/oncotarget.2998
Galluzzi L, Vacchelli E, Bravo-San Pedro JM, Buqué A, Senovilla L, Baracco EE et al. Classification of current anticancer immunotherapies. Oncotarget. 2014 Jan 1;5(24):12472-12508. https://doi.org/10.18632/oncotarget.2998
Galluzzi, Lorenzo ; Vacchelli, Erika ; Bravo-San Pedro, José Manuel ; Buqué, Aitziber ; Senovilla, Laura ; Baracco, Elisa Elena ; Bloy, Norma ; Castoldi, Francesca ; Abastado, Jean Pierre ; Agostinis, Patrizia ; Apte, Ron N. ; Aranda, Fernando ; Ayyoub, Maha ; Beckhove, Philipp ; Blay, Jean Yves ; Bracci, Laura ; Caignard, Anne ; Castelli, Chiara ; Cavallo, Federica ; Celis, Esteban ; Cerundolo, Vincenzo ; Clayton, Aled ; Colombo, Mario P. ; Coussens, Lisa ; Dhodapkar, Madhav V. ; Eggermont, Alexander M. ; Fearon, Douglas T. ; Fridman, Wolf H. ; Fucíková, Jitka ; Gabrilovich, Dmitry I. ; Galon, Jérôme ; Garg, Abhishek ; Ghiringhelli, François ; Giaccone, Giuseppe ; Gilboa, Eli ; Gnjatic, Sacha ; Hoos, Axel ; Hosmalin, Anne ; Jäger, Dirk ; Kalinski, Pawel ; Kärre, Klas ; Kepp, Oliver ; Kiessling, Rolf ; Kirkwood, John M. ; Klein, Eva ; Knuth, Alexander ; Lewis, Claire E. ; Liblau, Roland ; Lotze, Michael T. ; Lugli, Enrico ; Mach, Jean Pierre ; Mattei, Fabrizio ; Mavilio, Domenico ; Melero, Ignacio ; Melief, Cornelis J. ; Mittendorf, Elizabeth A. ; Moretta, Lorenzo ; Odunsi, Adekunke ; Okada, Hideho ; Palucka, Anna Karolina ; Peter, Marcus E. ; Pienta, Kenneth J. ; Porgador, Angel ; Prendergast, George C. ; Rabinovich, Gabriel A. ; Restifo, Nicholas P. ; Rizvi, Naiyer ; Sautès-Fridman, Catherine ; Schreiber, Hans ; Seliger, Barbara ; Shiku, Hiroshi ; Silva-Santos, Bruno ; Smyth, Mark J. ; Speiser, Daniel E. ; Spisek, Radek ; Srivastava, Pramod K. ; Talmadge, James E. ; Tartour, Eric ; Van Der Burg, Sjoerd H. ; Van Den Eynde, Benoît J. ; Vile, Richard ; Wagner, Hermann ; Weber, Jeffrey S. ; Whiteside, Theresa L. ; Wolchok, Jedd D. ; Zitvogel, Laurence ; Zou, Weiping ; Kroemer, Guido. / Classification of current anticancer immunotherapies. In: Oncotarget. 2014 ; Vol. 5, No. 24. pp. 12472-12508.
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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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T1 - Classification of current anticancer immunotherapies

AU - Galluzzi, Lorenzo

AU - Vacchelli, Erika

AU - Bravo-San Pedro, José Manuel

AU - Buqué, Aitziber

AU - Senovilla, Laura

AU - Baracco, Elisa Elena

AU - Bloy, Norma

AU - Castoldi, Francesca

AU - Abastado, Jean Pierre

AU - Agostinis, Patrizia

AU - Apte, Ron N.

AU - Aranda, Fernando

AU - Ayyoub, Maha

AU - Beckhove, Philipp

AU - Blay, Jean Yves

AU - Bracci, Laura

AU - Caignard, Anne

AU - Castelli, Chiara

AU - Cavallo, Federica

AU - Celis, Esteban

AU - Cerundolo, Vincenzo

AU - Clayton, Aled

AU - Colombo, Mario P.

AU - Coussens, Lisa

AU - Dhodapkar, Madhav V.

AU - Eggermont, Alexander M.

AU - Fearon, Douglas T.

AU - Fridman, Wolf H.

AU - Fucíková, Jitka

AU - Gabrilovich, Dmitry I.

AU - Galon, Jérôme

AU - Garg, Abhishek

AU - Ghiringhelli, François

AU - Giaccone, Giuseppe

AU - Gilboa, Eli

AU - Gnjatic, Sacha

AU - Hoos, Axel

AU - Hosmalin, Anne

AU - Jäger, Dirk

AU - Kalinski, Pawel

AU - Kärre, Klas

AU - Kepp, Oliver

AU - Kiessling, Rolf

AU - Kirkwood, John M.

AU - Klein, Eva

AU - Knuth, Alexander

AU - Lewis, Claire E.

AU - Liblau, Roland

AU - Lotze, Michael T.

AU - Lugli, Enrico

AU - Mach, Jean Pierre

AU - Mattei, Fabrizio

AU - Mavilio, Domenico

AU - Melero, Ignacio

AU - Melief, Cornelis J.

AU - Mittendorf, Elizabeth A.

AU - Moretta, Lorenzo

AU - Odunsi, Adekunke

AU - Okada, Hideho

AU - Palucka, Anna Karolina

AU - Peter, Marcus E.

AU - Pienta, Kenneth J.

AU - Porgador, Angel

AU - Prendergast, George C.

AU - Rabinovich, Gabriel A.

AU - Restifo, Nicholas P.

AU - Rizvi, Naiyer

AU - Sautès-Fridman, Catherine

AU - Schreiber, Hans

AU - Seliger, Barbara

AU - Shiku, Hiroshi

AU - Silva-Santos, Bruno

AU - Smyth, Mark J.

AU - Speiser, Daniel E.

AU - Spisek, Radek

AU - Srivastava, Pramod K.

AU - Talmadge, James E.

AU - Tartour, Eric

AU - Van Der Burg, Sjoerd H.

AU - Van Den Eynde, Benoît J.

AU - Vile, Richard

AU - Wagner, Hermann

AU - Weber, Jeffrey S.

AU - Whiteside, Theresa L.

AU - Wolchok, Jedd D.

AU - Zitvogel, Laurence

AU - Zou, Weiping

AU - Kroemer, Guido

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KW - Adoptive cell transfer

KW - Checkpoint blockers

KW - DNA-based vaccines

KW - Dendritic cell-based interventions

KW - Immunostimulatory cytokines

KW - Oncolytic viruses

KW - Peptide-based vaccines

KW - Toll-like receptor agonists

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