Second- and third-generation drugs for immuno-oncology treatment—The more the better?

The blockade of immune checkpoints in cancer immunotherapy

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Oncology meets immunology: the cancer-immunity cycle.

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Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion

Schreiber, R. D., Old, L. J., & Smyth, M. J. (2011) · Science · doi:10.1126/science.1203486 · Cited by 6,474

Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival

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T cell exhaustion

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Cytokine Storm in a Phase 1 Trial of the Anti-CD28 Monoclonal Antibody TGN1412

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Immune Inhibitory Molecules LAG-3 and PD-1 Synergistically Regulate T-cell Function to Promote Tumoral Immune Escape

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CD40-CD40 ligand

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Licensing of natural killer cells by host major histocompatibility complex class I molecules

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Controlling Natural Killer Cell Responses: Integration of Signals for Activation and Inhibition

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Indoleamine 2,3-dioxygenase and tumor-induced tolerance

Munn, D. H., & Mellor, A. L. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31178 · Cited by 1,078

Homeostasis and Self-Tolerance in the Immune System: Turning Lymphocytes off

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Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts

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VISTA, a novel mouse Ig superfamily ligand that negatively regulates T cell responses

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High-throughput epitope discovery reveals frequent recognition of neo-antigens by CD4+ T cells in human melanoma

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Immunostimulatory monoclonal antibodies for cancer therapy

Melero, I., Hervas-Stubbs, S., Glennie, M., Pardoll, D. M., & Chen, L. (2007) · Nature Reviews Cancer · doi:10.1038/nrc2051 · Cited by 627

Specific T Helper Cell Requirement for Optimal Induction of Cytotoxic T Lymphocytes against Major Histocompatibility Complex Class II Negative Tumors

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Antagonist Antibodies to PD-1 and B7-H1 (PD-L1) in the Treatment of Advanced Human Cancer—Response

Sznol, M., & Chen, L. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-2234 · Cited by 528

OX40 Is a Potent Immune-Stimulating Target in Late-Stage Cancer Patients

Curti, B. D., Kovacsovics-Bankowski, M., Morris, N., Walker, E., Chisholm, L., Floyd, K., Walker, J., Gonzalez, I., Meeuwsen, T., Fox, B. A., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4174 · Cited by 496

Antagonist Antibodies to PD-1 and B7-H1 (PD-L1) in the Treatment of Advanced Human Cancer

Sznol, M., & Chen, L. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-2063 · Cited by 488

CD4+ Tregs and immune control

Fehérvari, Z., & Sakaguchi, S. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200423395 · Cited by 452

Radiotherapy and the Tumor Stroma: The Importance of Dose and Fractionation

Hellevik, T., & Martinez-Zubiaurre, I. (2014) · Frontiers in Oncology · doi:10.3389/fonc.2014.00001 · Cited by 442

Triggering of OX40 (CD134) on CD4+CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR

Valzasina, B., Guiducci, C., Dislich, H., Killeen, N., Weinberg, A. D., & Colombo, M. P. (2005) · Blood · doi:10.1182/blood-2004-07-2959 · Cited by 428

Agonistic CD40 Antibodies and Cancer Therapy

Vonderheide, R. H., & Glennie, M. J. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-2064 · Cited by 414

Tumor-induced perturbations of cytokines and immune cell networks

Burkholder, B., Huang, R.-Y., Burgess, R., Luo, S., Jones, V. S., Zhang, W., Lv, Z.-Q., Gao, C.-Y., Wang, B.-L., Zhang, Y.-M., et al. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2014.01.004 · Cited by 356

Trial watch: IDO inhibitors in cancer therapy

Vacchelli, E., Aranda, F., Eggermont, A., Sautès-Fridman, C., Tartour, E., Kennedy, E. P., Platten, M., Zitvogel, L., Kroemer, G., & Galluzzi, L. (2014) · OncoImmunology · doi:10.4161/21624011.2014.957994 · Cited by 326

Rationale for anti-OX40 cancer immunotherapy

Aspeslagh, S., Postel-Vinay, S., Rusakiewicz, S., Soria, J.-C., Zitvogel, L., & Marabelle, A. (2016) · European Journal of Cancer · doi:10.1016/j.ejca.2015.08.021 · Cited by 318

B7 family checkpoint regulators in immune regulation and disease

Ceeraz, S., Nowak, E. C., & Noelle, R. J. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.07.003 · Cited by 307

Molecular Pathways: Coexpression of Immune Checkpoint Molecules: Signaling Pathways and Implications for Cancer Immunotherapy

Nirschl, C. J., & Drake, C. G. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1972 · Cited by 306

Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies

Kohrt, H. E., Thielens, A., Marabelle, A., Sagiv-Barfi, I., Sola, C., Chanuc, F., Fuseri, N., Bonnafous, C., Czerwinski, D., Rajapaksa, A., et al. (2014) · Blood · doi:10.1182/blood-2013-08-519199 · Cited by 283

The ICOS/ICOSL Pathway Is Required for Optimal Antitumor Responses Mediated by Anti–CTLA-4 Therapy

Fu, T., He, Q., & Sharma, P. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1138 · Cited by 243

OX40 Agonists and Combination Immunotherapy: Putting the Pedal to the Metal

Linch, S. N., McNamara, M. J., & Redmond, W. L. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00034 · Cited by 238

VISTA is a novel broad-spectrum negative checkpoint regulator for cancer immunotherapy

Lines, J. L., Sempere, L. F., Broughton, T., Wang, L., & Noelle, R. (2014) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-14-0072 · Cited by 236

Systematic Review of Interventions to Improve the Provision of Information for Adults with Primary Brain Tumors and Their Caregivers

Langbecker, D., & Janda, M. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00001 · Cited by 228

CTLA-4 and PD-1 Pathway Blockade: Combinations in the Clinic

Callahan, M. K., Postow, M. A., & Wolchok, J. D. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2014.00385 · Cited by 224

Phase I Study of Recombinant Human CD40 Ligand in Cancer Patients

Vonderheide, R. H., Dutcher, J. P., Anderson, J. E., Eckhardt, S. G., Stephans, K. F., Razvillas, B., Garl, S., Butine, M. D., Perry, V. P., Armitage, R. J., et al. (2001) · Journal of Clinical Oncology · doi:10.1200/jco.2001.19.13.3280 · Cited by 223

Rationale for anti-GITR cancer immunotherapy

Knee, D. A., Hewes, B., & Brogdon, J. L. (2016) · European Journal of Cancer · doi:10.1016/j.ejca.2016.06.028 · Cited by 221

Combination CTLA-4 Blockade and 4-1BB Activation Enhances Tumor Rejection by Increasing T-Cell Infiltration, Proliferation, and Cytokine Production

Curran, M. A., Kim, M., Montalvo, W., Al-Shamkhani, A., & Allison, J. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019499 · Cited by 213

Prospect of Targeting the CD40 Pathway for Cancer Therapy

Vonderheide, R. H. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1893 · Cited by 186

Signaling Through NK Cell-Associated CD137 Promotes Both Helper Function for CD8+ Cytolytic T Cells and Responsiveness to IL-2 But Not Cytolytic Activity

Wilcox, R. A., Tamada, K., Strome, S. E., & Chen, L. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.8.4230 · Cited by 181

A first in man phase I trial of the oral immunomodulator, indoximod, combined with docetaxel in patients with metastatic solid tumors

Soliman, H. H., Jackson, E., Neuger, T., Dees, E. C., Harvey, R. D., Han, H., Ismail-Khan, R., Minton, S., Vahanian, N. N., Link, C., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.2357 · Cited by 174

Targeting of 4-1BB by monoclonal antibody PF-05082566 enhances T-cell function and promotes anti-tumor activity

Fisher, T. S., Kamperschroer, C., Oliphant, T., Love, V. A., Lira, P. D., Doyonnas, R., Bergqvist, S., Baxi, S. M., Rohner, A., Shen, A. C., et al. (2012) · Cancer Immunology, Immunotherapy · doi:10.1007/s00262-012-1237-1 · Cited by 166

Human plasmacytoid predendritic cells activate NK cells through glucocorticoid-induced tumor necrosis factor receptor-ligand (GITRL)

Hanabuchi, S., Watanabe, N., Wang, Y.-H., Wang, Y.-H., Ito, T., Shaw, J., Cao, W., Qin, F. X.-F., & Liu, Y.-J. (2006) · Blood · doi:10.1182/blood-2005-08-3419 · Cited by 164

Cutting Edge: OX40 Agonists Can Drive Regulatory T Cell Expansion if the Cytokine Milieu Is Right

Ruby, C. E., Yates, M. A., Hirschhorn-Cymerman, D., Chlebeck, P., Wolchok, J. D., Houghton, A. N., Offner, H., & Weinberg, A. D. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901112 · Cited by 164

The TNFRs OX40, 4-1BB, and CD40 as targets for cancer immunotherapy

Moran, A. E., Kovacsovics-Bankowski, M., & Weinberg, A. D. (2013) · Current Opinion in Immunology · doi:10.1016/j.coi.2013.01.004 · Cited by 162

Exploitation of natural killer cells for the treatment of acute leukemia

Handgretinger, R., Lang, P., & André, M. C. (2016) · Blood · doi:10.1182/blood-2015-12-629055 · Cited by 159

A phase I study of indoximod in patients with advanced malignancies

Soliman, H. H., Minton, S. E., Han, H. S., Ismail-Khan, R. R., Neuger, A. M., Khambati, F. A., Noyes, D. R., Lush, R. M., Chiappori, A., Roberts, J. D., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.8216 · Cited by 145

Signals from OX40 regulate nuclear factor of activated T cells c1 and T cell helper 2 lineage commitment

So, T., Song, J. J., Sugie, K., Altman, A., & Croft, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600205103 · Cited by 130

Prospects for TIM3-Targeted Antitumor Immunotherapy

Ngiow, S. F., Teng, M. W. L., & Smyth, M. J. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1487 · Cited by 128

Fc-dependent expression of CD137 on human NK cells: insights into “agonistic” effects of anti-CD137 monoclonal antibodies

Lin, W., Voskens, C., Zhang, X., Schindler, D. G., Wood, A., Burch, E. E., Wei, Y., Chen, L., Tian, G., Tamada, K., et al. (2008) · Blood · doi:10.1182/blood-2007-11-122465 · Cited by 121

Trial Watch: Immunostimulatory monoclonal antibodies in cancer therapy

Aranda, F., Vacchelli, E., Eggermont, A. M. M., Galon, J., Fridman, W. H., Zitvogel, L., Kroemer, G., & Galluzzi, L. (2014) · OncoImmunology · doi:10.4161/onci.27297 · Cited by 119

CD40–CD40Ligand interactions and their role in cytotoxic T lymphocyte priming and anti-tumor immunity

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Air Trapping on Chest CT Is Associated with Worse Ventilation Distribution in Infants with Cystic Fibrosis Diagnosed following Newborn Screening

Hall, G. L., Logie, K. M., Parsons, F., Schulzke, S. M., Nolan, G., Murray, C. P. J., Ranganathan, S., Robinson, P. J., Sly, P. D., Stick, S. M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023932 · Cited by 114

Tumor-specific CD4+ Melanoma Tumor-infiltrating Lymphocytes

Friedman, K. M., Prieto, P. A., Devillier, L., Gross, C. A., Yang, J. C., Wunderlich, J. R., Rosenberg, S. A., & Dudley, M. E. (2012) · Journal of Immunotherapy · doi:10.1097/cji.0b013e31825898c5 · Cited by 110

Multi-layered action mechanisms of CD137 (4-1BB)-targeted immunotherapies

Melero, I., Murillo, O., Dubrot, J., Hervás‐Stubbs, S., & Perez‐Gracia, J. L. (2008) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.05.005 · Cited by 107

Interim results of an ongoing Phase I, dose escalation study of MGA271 (Fc-optimized humanized anti-B7-H3 monoclonal antibody) in patients with refractory B7-H3-expressing neoplasms or neoplasms whose vasculature expresses B7-H3

Powderly, J. D., Cote, G. M., Flaherty, K. T., Szmulewitz, R. Z., Ribas, A., Weber, J. S., Loo, D. T., Baughman, J. E., Chen, F., Moore, P. A., et al. (2015) · Journal for ImmunoTherapy of Cancer · doi:10.1186/2051-1426-3-s2-o8 · Cited by 107

Immunogenic Apoptotic Cell Death and Anticancer Immunity

Vandenabeele, P., Vandecasteele, K., Bachert, C., Krysko, O., & Krysko, D. V. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-39406-0_6 · Cited by 106

Immune Checkpoint Modulation for Non–Small Cell Lung Cancer

Soria, J., Marabelle, A., Brahmer, J. R., & Gettinger, S. N. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-2959 · Cited by 102

Dynamic regulation of T cell activation and co‐stimulation through TCR‐microclusters

Saito, T., Yokosuka, T., & Hashimoto, A. S. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.11.036 · Cited by 98

T Cell Immunity to Lymphoma Following Treatment with Anti-CD40 Monoclonal Antibody

Tutt, A. L., O’Brien, L. M., Hussain, A., Crowther, G., French, R. R., & Glennie, M. J. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.6.2720 · Cited by 85

MART-1 peptide vaccination plus IMP321 (LAG-3Ig fusion protein) in patients receiving autologous PBMCs after lymphodepletion: results of a Phase I trial

Romano, E., Michielin, O. A., Voelter, V., Laurent, J., Bichat, H., Stravodimou, A., Romero, P. J., Speiser, D. E., Triebel, F., Leyvraz, S., et al. (2014) · Journal of Translational Medicine · doi:10.1186/1479-5876-12-97 · Cited by 84

Combination Therapy of Established Tumors by Antibodies Targeting Immune Activating and Suppressing Molecules

Takeda, K., Kojima, Y., Uno, T., Hayakawa, Y., Teng, M. W. L., Yoshizawa, H., Yagita∥, H., Gejyo, F., Okumura, K., & Smyth, M. J. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903033 · Cited by 82

Beyond Melanoma: Inhibiting The PD-1/PD-L1 Pathway in Solid Tumors

Gentzler, R. D., Hall, R. D., Kunk, P. R., Gaughan, E. M., Dillon, P. M., Slingluff, C. L., & Rahma, O. E. (2016) · Immunotherapy · doi:10.2217/imt-2015-0029 · Cited by 81

A model for cancer-suppressive inflammation

Haabeth, O. A. W., Bogen, B., & Corthay, A. (2012) · OncoImmunology · doi:10.4161/onci.21542 · Cited by 75

Glucocorticoid‐Induced TNFR‐Related (GITR) Protein and Its Ligand in Antitumor Immunity: Functional Role and Therapeutic Modulation

Placke, T., Kopp, H., & Salih, H. R. (2010) · Journal of Immunology Research · doi:10.1155/2010/239083 · Cited by 70

The development of immunomodulatory monoclonal antibodies as a new therapeutic modality for cancer: The Bristol-Myers Squibb experience

Berman, D., Korman, A. J., Peck, R., Feltquate, D., Lönberg, N., & Canetta, R. M. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.11.017 · Cited by 66

The Role of Coinhibitory Signaling Pathways in Transplantation and Tolerance

McGrath, M. M., & Najafian, N. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00047 · Cited by 63

Mogamulizumab for the treatment of cutaneous T-cell lymphoma: recent advances and clinical potential

Duvic, M. A., Evans, M., & Wang, C. (2016) · Therapeutic Advances in Hematology · doi:10.1177/2040620716636541 · Cited by 63

Emerging Co-signaling Networks in T Cell Immune Regulation

Jung, K., & Choi, I. (2013) · Immune Network · doi:10.4110/in.2013.13.5.184 · Cited by 55

Mogamulizumab: 2 birds, 1 stone

Wilcox, R. A. (2015) · Blood · doi:10.1182/blood-2015-02-625251 · Cited by 53

Indoleamine 2,3-dioxygenase mediates immune-independent human tumor cell resistance to olaparib, gamma radiation, and cisplatin

Vareki, S. M., Rytelewski, M., Figueredo, R., Chen, D., Ferguson, P. J., Vincent, M. D., Min, W., Zheng, X., & Koropatnick, J. D. (2014) · Oncotarget · doi:10.18632/oncotarget.1916 · Cited by 53

Preliminary results from a phase 1/2 study of INCB024360 combined with ipilimumab (ipi) in patients (pts) with melanoma.

Gibney, G. T., Hamid, O., Gangadhar, T. C., Lutzky, J., Olszanski, A. J., Gajewski, T. F., Chmielowski, B., Boasberg, P. D., Zhao, Y., Newton, R. C., et al. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2014.32.15_suppl.3010 · Cited by 52

GI24 enhances tumor invasiveness by regulating cell surface membrane‐type 1 matrix metalloproteinase

Sakr, M., Takino, T., Domoto, T., Nakano, H., Wong, R. W.-C., Sasaki, M., Nakanuma, Y., & Sato, H. (2010) · Cancer Science · doi:10.1111/j.1349-7006.2010.01675.x · Cited by 46

IDO Downregulation Induces Sensitivity to Pemetrexed, Gemcitabine, FK866, and Methoxyamine in Human Cancer Cells

Vareki, S. M., Chen, D., Cresce, C. D., Ferguson, P. J., Figueredo, R., Pampillo, M., Rytelewski, M., Vincent, M. D., Min, W., Zheng, X., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143435 · Cited by 45

Lysosome‐Related Effector Vesicles in T Lymphocytes and NK Cells

Lettau, M., Kabelitz, D., & Janßen, O. (2015) · Scandinavian Journal of Immunology · doi:10.1111/sji.12337 · Cited by 37

First-in-human phase 1 single-dose study of TRX-518, an anti-human glucocorticoid-induced tumor necrosis factor receptor (GITR) monoclonal antibody in adults with advanced solid tumors.

Koon, H. B., Shepard, D. R., Merghoub, T., Schaer, D., Sirard, C. A., & Wolchok, J. D. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.15_suppl.3017 · Cited by 36

A phase I study of PF-05082566 (anti-4-1BB) + rituximab in patients with CD20+ NHL.

Gopal, A. K., Bartlett, N. L., Levy, R., Houot, R., Smith, S. D., Segal, N. H., Thall, A. D., Mugundu, G. M., Huang, B., Davis, C. B., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2015.33.15_suppl.3004 · Cited by 24

Results of the phase Ib portion of a phase I/II trial of the indoleamine 2,3-dioxygenase pathway (IDO) inhibitor indoximod plus gemcitabine/nab-paclitaxel for the treatment of metastatic pancreatic cancer.

Bahary, N., Garrido‐Laguna, I., Wang‐Gillam, A., Nayak-Kapoor, A., Kennedy, E. P., Vahanian, N. N., & Link, C. J. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.4_suppl.452 · Cited by 22

Phase Ib study of PF-05082566 in combination with pembrolizumab in patients with advanced solid tumors.

Tolcher, A. W., Sznol, M., Hu‐Lieskovan, S., Papadopoulos, K. P., Patnaik, A., Rasco, D. W., Gravio, D. D., Huang, B., Gambhire, D., Chen, Y., et al. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.15_suppl.3002 · Cited by 17

Moving Programmed Death-1 Inhibitors to the Front Lines in Non–Small-Cell Lung Cancer

Gainor, J. F. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.68.1205 · Cited by 13

Novel immune checkpoint targets: moving beyond PD-1 and CTLA-4

Qin, S., Xu, L., Yi, M., Yu, S., Wu, K., & Luo, S. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1091-2 · Cited by 1,145

Next generation of immune checkpoint therapy in cancer: new developments and challenges

Marin-Acevedo, J. A., Dholaria, B., Soyano, A. E., Knutson, K. L., Chumsri, S., & Lou, Y. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0582-8 · Cited by 804

Oncolytic virotherapy: basic principles, recent advances and future directions

Lin, D., Shen, Y., & Liang, T. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01407-6 · Cited by 459

Oncolytic viruses as engineering platforms for combination immunotherapy

Twumasi-Boateng, K., Pettigrew, J. L., Kwok, Y. Y. E., Bell, J. C., & Nelson, B. H. (2018) · Nature Reviews Cancer · doi:10.1038/s41568-018-0009-4 · Cited by 417

The promising immune checkpoint LAG-3: from tumor microenvironment to cancer immunotherapy

Long, L., Zhang, X., Chen, F., Pan, Q., Phiphatwatchara, P., Zeng, Y., & Chen, H. (2018) · Genes & Cancer · doi:10.18632/genesandcancer.180 · Cited by 386