. 2016 Jun; 100(2):275-90.
doi: 10.1189/jlb.5RI0116-013RR.

Combinatorial approach to cancer immunotherapy: strength in numbers

Anna E Vilgelm 1 Douglas B Johnson 2 Ann Richmond 3 
  • PMID: 27256570
  •     180 References
  •     43 citations


Immune-checkpoint blockade therapy with antibodies targeting CTLA-4 and PD-1 has revolutionized melanoma treatment by eliciting responses that can be remarkably durable and is now advancing to other malignancies. However, not all patients respond to immune-checkpoint inhibitors. Extensive preclinical evidence suggests that combining immune-checkpoint inhibitors with other anti-cancer treatments can greatly improve the therapeutic benefit. The first clinical success of the combinatorial approach to cancer immunotherapy was demonstrated using a dual-checkpoint blockade with CTLA-4 and PD-1 inhibitors, which resulted in accelerated FDA approval of this therapeutic regimen. In this review, we discuss the combinations of current and emerging immunotherapeutic agents in clinical and preclinical development and summarize the insights into potential mechanisms of synergistic anti-tumor activity gained from animal studies. These promising combinatorial partners for the immune-checkpoint blockade include therapeutics targeting additional inhibitory receptors of T cells, such as TIM-3, LAG-3, TIGIT, and BTLA, and agonists of T cell costimulatory receptors 4-1BB, OX40, and GITR, as well as agents that promote cancer cell recognition by the immune system, such as tumor vaccines, IDO inhibitors, and agonists of the CD40 receptor of APCs. We also review the therapeutic potential of regimens combining the immune-checkpoint blockade with therapeutic interventions that have been shown to enhance immunogenicity of cancer cells, including oncolytic viruses, RT, epigenetic therapy, and senescence-inducing therapy.

Keywords: immune checkpoints; immunogenic cell death; melanoma; senescence.

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Increased frequency of ICOS+ CD4 T cells as a pharmacodynamic biomarker for anti-CTLA-4 therapy.
Derek Ng Tang, Yu Shen, +5 authors, Padmanee Sharma.
Cancer Immunol Res, 2014 Apr 30; 1(4). PMID: 24777852    Free PMC article.
Highly Cited.
Combined targeting of costimulatory (OX40) and coinhibitory (CTLA-4) pathways elicits potent effector T cells capable of driving robust antitumor immunity.
William L Redmond, Stefanie N Linch, Melissa J Kasiewicz.
Cancer Immunol Res, 2014 Apr 30; 2(2). PMID: 24778278    Free PMC article.
Agonistic anti-CD137 antibody treatment leads to antitumor response in mice with liver cancer.
Vanessa Gauttier, Jean-Paul Judor, +3 authors, Sophie Conchon.
Int J Cancer, 2014 May 03; 135(12). PMID: 24789574
Tim-3: an emerging target in the cancer immunotherapy landscape.
Ana C Anderson.
Cancer Immunol Res, 2014 May 06; 2(5). PMID: 24795351
Highly Cited. Review.
Therapeutic vaccines for cancer: an overview of clinical trials.
Ignacio Melero, Gustav Gaudernack, +8 authors, Håkan Mellstedt.
Nat Rev Clin Oncol, 2014 Jul 09; 11(9). PMID: 25001465
Highly Cited. Review.
Noncanonical NF-κB activation mediates STAT3-stimulated IDO upregulation in myeloid-derived suppressor cells in breast cancer.
Jinpu Yu, Yue Wang, +6 authors, Xiubao Ren.
J Immunol, 2014 Jul 27; 193(5). PMID: 25063873    Free PMC article.
Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells.
KiBem Kim, Andrew D Skora, +8 authors, Shibin Zhou.
Proc Natl Acad Sci U S A, 2014 Jul 30; 111(32). PMID: 25071169    Free PMC article.
Highly Cited.
Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy.
Antonio M Grimaldi, Ester Simeone, +15 authors, Paolo A Ascierto.
Oncoimmunology, 2014 Aug 02; 3. PMID: 25083318    Free PMC article.
Highly Cited.
Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in orthotopic glioma through the induction of immunogenic cell death.
Carolien A Koks, Abhishek D Garg, +7 authors, Stefaan W Van Gool.
Int J Cancer, 2014 Sep 12; 136(5). PMID: 25208916
Highly Cited.
Anti-CTLA-4 therapy broadens the melanoma-reactive CD8+ T cell response.
Pia Kvistborg, Daisy Philips, +13 authors, Ton N Schumacher.
Sci Transl Med, 2014 Sep 19; 6(254). PMID: 25232180
Highly Cited.
Combined BRAF and MEK inhibition versus BRAF inhibition alone in melanoma.
Georgina V Long, Daniil Stroyakovskiy, +32 authors, Keith Flaherty.
N Engl J Med, 2014 Sep 30; 371(20). PMID: 25265492
Highly Cited.
Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade.
Simon J Dovedi, Amy L Adlard, +11 authors, Tim M Illidge.
Cancer Res, 2014 Oct 03; 74(19). PMID: 25274032
Highly Cited.
Lymphocyte Activation Gene 3 (LAG-3) modulates the ability of CD4 T-cells to be suppressed in vivo.
Nicholas M Durham, Christopher J Nirschl, +4 authors, Charles G Drake.
PLoS One, 2014 Nov 06; 9(11). PMID: 25372844    Free PMC article.
Combination of 4-1BB agonist and PD-1 antagonist promotes antitumor effector/memory CD8 T cells in a poorly immunogenic tumor model.
Shihao Chen, Li-Fen Lee, +12 authors, John C Lin.
Cancer Immunol Res, 2014 Nov 13; 3(2). PMID: 25387892
Highly Cited.
Universes collide: combining immunotherapy with targeted therapy for cancer.
Jennifer A Wargo, Zachary A Cooper, Keith T Flaherty.
Cancer Discov, 2014 Nov 15; 4(12). PMID: 25395294    Free PMC article.
Nivolumab in previously untreated melanoma without BRAF mutation.
Caroline Robert, Georgina V Long, +25 authors, Paolo A Ascierto.
N Engl J Med, 2014 Nov 18; 372(4). PMID: 25399552
Highly Cited.
OX40- and CD27-mediated costimulation synergizes with anti-PD-L1 blockade by forcing exhausted CD8+ T cells to exit quiescence.
Sarah Buchan, Teresa Manzo, +12 authors, Ronjon Chakraverty.
J Immunol, 2014 Nov 19; 194(1). PMID: 25404365    Free PMC article.
Genetic basis for clinical response to CTLA-4 blockade in melanoma.
Alexandra Snyder, Vladimir Makarov, +18 authors, Timothy A Chan.
N Engl J Med, 2014 Nov 20; 371(23). PMID: 25409260    Free PMC article.
Highly Cited.
Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients.
Roy S Herbst, Jean-Charles Soria, +19 authors, F Stephen Hodi.
Nature, 2014 Nov 28; 515(7528). PMID: 25428504    Free PMC article.
Highly Cited.
PD-1 blockade induces responses by inhibiting adaptive immune resistance.
Paul C Tumeh, Christina L Harview, +23 authors, Antoni Ribas.
Nature, 2014 Nov 28; 515(7528). PMID: 25428505    Free PMC article.
Highly Cited.
The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function.
Robert J Johnston, Laetitia Comps-Agrar, +9 authors, Jane L Grogan.
Cancer Cell, 2014 Dec 04; 26(6). PMID: 25465800
Highly Cited.
Stereotactic Radiation Therapy Augments Antigen-Specific PD-1-Mediated Antitumor Immune Responses via Cross-Presentation of Tumor Antigen.
Andrew B Sharabi, Christopher J Nirschl, +5 authors, Charles G Drake.
Cancer Immunol Res, 2014 Dec 21; 3(4). PMID: 25527358    Free PMC article.
Highly Cited.
Combination immunotherapy with 4-1BB activation and PD-1 blockade enhances antitumor efficacy in a mouse model of subcutaneous tumor.
Yoshitaro Shindo, Kiyoshi Yoshimura, +10 authors, Masaaki Oka.
Anticancer Res, 2015 Jan 01; 35(1). PMID: 25550543
Anticancer immunotherapy by CTLA-4 blockade: obligatory contribution of IL-2 receptors and negative prognostic impact of soluble CD25.
Dalil Hannani, Marie Vétizou, +30 authors, Laurence Zitvogel.
Cell Res, 2015 Jan 15; 25(2). PMID: 25582080    Free PMC article.
Highly Cited.
Induced PD-L1 expression mediates acquired resistance to agonistic anti-CD40 treatment.
Alfred Zippelius, Jens Schreiner, Petra Herzig, Philipp Müller.
Cancer Immunol Res, 2015 Jan 28; 3(3). PMID: 25623164
Genetic basis for clinical response to CTLA-4 blockade.
Ignacio Melero, Juan J Lasarte.
N Engl J Med, 2015 Feb 19; 372(8). PMID: 25693025
Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer.
Christina Twyman-Saint Victor, Andrew J Rech, +22 authors, Andy J Minn.
Nature, 2015 Mar 11; 520(7547). PMID: 25754329    Free PMC article.
Highly Cited.
Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial.
Jeffrey S Weber, Sandra P D'Angelo, +25 authors, James Larkin.
Lancet Oncol, 2015 Mar 22; 16(4). PMID: 25795410
Highly Cited.
An unexpected journey: how cancer immunotherapy has paved the way for an HIV-1 cure.
Kellie N Smith, Franck Housseau.
Discov Med, 2015 Apr 02; 19(104). PMID: 25828527
The future of immune checkpoint therapy.
Padmanee Sharma, James P Allison.
Science, 2015 Apr 04; 348(6230). PMID: 25838373
Highly Cited. Review.
TIGIT and PD-1 impair tumor antigen-specific CD8⁺ T cells in melanoma patients.
Joe-Marc Chauvin, Ornella Pagliano, +8 authors, Hassane M Zarour.
J Clin Invest, 2015 Apr 14; 125(5). PMID: 25866972    Free PMC article.
Highly Cited.
Pembrolizumab versus Ipilimumab in Advanced Melanoma.
Caroline Robert, Jacob Schachter, +20 authors, KEYNOTE-006 investigators.
N Engl J Med, 2015 Apr 22; 372(26). PMID: 25891173
Highly Cited.
Nivolumab and ipilimumab versus ipilimumab in untreated melanoma.
Michael A Postow, Jason Chesney, +18 authors, F Stephen Hodi.
N Engl J Med, 2015 Apr 22; 372(21). PMID: 25891304    Free PMC article.
Highly Cited.
Trial watch: IDO inhibitors in cancer therapy.
Erika Vacchelli, Fernando Aranda, +7 authors, Lorenzo Galluzzi.
Oncoimmunology, 2015 May 06; 3(10). PMID: 25941578    Free PMC article.
Highly Cited. Review.
Combinatorial strategies for the induction of immunogenic cell death.
Lucillia Bezu, Ligia C Gomes-de-Silva, +6 authors, Guido Kroemer.
Front Immunol, 2015 May 13; 6. PMID: 25964783    Free PMC article.
Highly Cited. Review.
Epigenetics meets immune checkpoints.
Alessia Covre, Sandra Coral, +3 authors, Michele Maio.
Semin Oncol, 2015 May 13; 42(3). PMID: 25965370
Classifying Cancers Based on T-cell Infiltration and PD-L1.
Michele W L Teng, Shin Foong Ngiow, Antoni Ribas, Mark J Smyth.
Cancer Res, 2015 May 16; 75(11). PMID: 25977340    Free PMC article.
Highly Cited. Review.
Talimogene Laherparepvec Improves Durable Response Rate in Patients With Advanced Melanoma.
Robert H I Andtbacka, Howard L Kaufman, +26 authors, Robert S Coffin.
J Clin Oncol, 2015 May 28; 33(25). PMID: 26014293
Highly Cited.
Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma.
James Larkin, Vanna Chiarion-Sileni, +28 authors, Jedd D Wolchok.
N Engl J Med, 2015 Jun 02; 373(1). PMID: 26027431    Free PMC article.
Highly Cited.
Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer.
Julie Brahmer, Karen L Reckamp, +22 authors, David R Spigel.
N Engl J Med, 2015 Jun 02; 373(2). PMID: 26028407    Free PMC article.
Highly Cited.
Differential Activity of Nivolumab, Pembrolizumab and MPDL3280A according to the Tumor Expression of Programmed Death-Ligand-1 (PD-L1): Sensitivity Analysis of Trials in Melanoma, Lung and Genitourinary Cancers.
Luisa Carbognin, Sara Pilotto, +11 authors, Giampaolo Tortora.
PLoS One, 2015 Jun 19; 10(6). PMID: 26086854    Free PMC article.
Highly Cited.
4-1BB Agonists: Multi-Potent Potentiators of Tumor Immunity.
Todd Bartkowiak, Michael A Curran.
Front Oncol, 2015 Jun 25; 5. PMID: 26106583    Free PMC article.
Highly Cited. Review.
Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): a randomised, controlled, phase 2 trial.
Antoni Ribas, Igor Puzanov, +33 authors, Adil Daud.
Lancet Oncol, 2015 Jun 28; 16(8). PMID: 26115796    Free PMC article.
Highly Cited.
Combining an Aurora Kinase Inhibitor and a Death Receptor Ligand/Agonist Antibody Triggers Apoptosis in Melanoma Cells and Prevents Tumor Growth in Preclinical Mouse Models.
Yan Liu, Oriana E Hawkins, +5 authors, Ann Richmond.
Clin Cancer Res, 2015 Jul 15; 21(23). PMID: 26152738    Free PMC article.
Therapeutic Advances and Treatment Options in Metastatic Melanoma.
Douglas B Johnson, Jeffrey A Sosman.
JAMA Oncol, 2015 Jul 17; 1(3). PMID: 26181188
CD70: An emerging target in cancer immunotherapy.
J Jacobs, V Deschoolmeester, +6 authors, P Pauwels.
Pharmacol Ther, 2015 Jul 28; 155. PMID: 26213107
Therapeutic cancer vaccines.
Cornelis J M Melief, Thorbald van Hall, +2 authors, Sjoerd H van der Burg.
J Clin Invest, 2015 Jul 28; 125(9). PMID: 26214521    Free PMC article.
Highly Cited. Review.
HDAC Inhibition Upregulates PD-1 Ligands in Melanoma and Augments Immunotherapy with PD-1 Blockade.
David M Woods, Andressa L Sodré, +3 authors, Jeffrey Weber.
Cancer Immunol Res, 2015 Aug 25; 3(12). PMID: 26297712    Free PMC article.
Highly Cited.
Prognostic and Predictive Value of DAMPs and DAMP-Associated Processes in Cancer.
Jitka Fucikova, Irena Moserova, +8 authors, Radek Spisek.
Front Immunol, 2015 Aug 25; 6. PMID: 26300886    Free PMC article.
Clinical Activity, Toxicity, Biomarkers, and Future Development of CTLA-4 Checkpoint Antagonists.
Margaret K Callahan, Jedd D Wolchok.
Semin Oncol, 2015 Sep 01; 42(4). PMID: 26320062
Antagonists of PD-1 and PD-L1 in Cancer Treatment.
Evan J Lipson, Patrick M Forde, +3 authors, Suzanne L Topalian.
Semin Oncol, 2015 Sep 01; 42(4). PMID: 26320063    Free PMC article.
Highly Cited. Review.
Beyond CTLA-4 and PD-1, the Generation Z of Negative Checkpoint Regulators.
Isabelle Le Mercier, J Louise Lines, Randolph J Noelle.
Front Immunol, 2015 Sep 09; 6. PMID: 26347741    Free PMC article.
Highly Cited. Review.
Genomic correlates of response to CTLA-4 blockade in metastatic melanoma.
Eliezer M Van Allen, Diana Miao, +19 authors, Levi A Garraway.
Science, 2015 Sep 12; 350(6257). PMID: 26359337    Free PMC article.
Highly Cited.
Emerging immune checkpoints for cancer therapy.
Xiaodong Li, Wenwei Hu, +8 authors, Changping Wu.
Acta Oncol, 2015 Sep 12; 54(10). PMID: 26361073
Combined therapies that induce senescence and stabilize p53 block melanoma growth and prompt antitumor immune responses.
Anna Vilgelm, Ann Richmond.
Oncoimmunology, 2015 Sep 26; 4(8). PMID: 26405565    Free PMC article.
BTLA marks a less-differentiated tumor-infiltrating lymphocyte subset in melanoma with enhanced survival properties.
Cara L Haymaker, Richard C Wu, +8 authors, Laszlo G Radvanyi.
Oncoimmunology, 2015 Sep 26; 4(8). PMID: 26405566    Free PMC article.
Antitumor activity of epigenetic immunomodulation combined with CTLA-4 blockade in syngeneic mouse models.
A Covre, S Coral, +8 authors, M Maio.
Oncoimmunology, 2015 Sep 26; 4(8). PMID: 26405573    Free PMC article.
Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma.
Robert J Motzer, Bernard Escudier, +25 authors, CheckMate 025 Investigators.
N Engl J Med, 2015 Sep 26; 373(19). PMID: 26406148    Free PMC article.
Highly Cited.
TIGIT predominantly regulates the immune response via regulatory T cells.
Sema Kurtulus, Kaori Sakuishi, +6 authors, Ana C Anderson.
J Clin Invest, 2015 Sep 29; 125(11). PMID: 26413872    Free PMC article.
Highly Cited.
A systematic evaluation of abscopal responses following radiotherapy in patients with metastatic melanoma treated with ipilimumab.
Ravi A Chandra, Tyler J Wilhite, +6 authors, Jonathan D Schoenfeld.
Oncoimmunology, 2015 Oct 10; 4(11). PMID: 26451318    Free PMC article.
Highly Cited.
Checkpoint blockade in combination with cancer vaccines.
Michael A Morse, H Kim Lyerly.
Vaccine, 2015 Oct 21; 33(51). PMID: 26482147
Fueling the engine and releasing the break: combinational therapy of cancer vaccines and immune checkpoint inhibitors.
Jennifer Kleponis, Richard Skelton, Lei Zheng.
Cancer Biol Med, 2015 Oct 22; 12(3). PMID: 26487965    Free PMC article.
Characterization of the human T cell response to in vitro CD27 costimulation with varlilumab.
Venky Ramakrishna, Karuna Sundarapandiyan, +3 authors, Tibor Keler.
J Immunother Cancer, 2015 Oct 27; 3. PMID: 26500773    Free PMC article.
Low dose cyclophosphamide: Mechanisms of T cell modulation.
Mutsa Tatenda Madondo, Michael Quinn, Magdalena Plebanski.
Cancer Treat Rev, 2015 Dec 02; 42. PMID: 26620820
Molecular and Translational Classifications of DAMPs in Immunogenic Cell Death.
Abhishek D Garg, Lorenzo Galluzzi, +49 authors, Patrizia Agostinis.
Front Immunol, 2015 Dec 05; 6. PMID: 26635802    Free PMC article.
Highly Cited.
Rationale for anti-OX40 cancer immunotherapy.
Sandrine Aspeslagh, Sophie Postel-Vinay, +3 authors, Aurélien Marabelle.
Eur J Cancer, 2015 Dec 10; 52. PMID: 26645943
Highly Cited. Review.
Connecting the Dots: Therapy-Induced Senescence and a Tumor-Suppressive Immune Microenvironment.
Anna E Vilgelm, C Andrew Johnson, +11 authors, Ann Richmond.
J Natl Cancer Inst, 2016 Jan 01; 108(6). PMID: 26719346    Free PMC article.
The Role of Adaptive Immunity in the Efficacy of Targeted Cancer Therapies.
Meng Michelle Xu, Yang Pu, Yuan Zhang, Yang-Xin Fu.
Trends Immunol, 2016 Jan 19; 37(2). PMID: 26778079    Free PMC article.
Activation of human dendritic cells through CD40 cross-linking.
C Caux, C Massacrier, +4 authors, J Banchereau.
J Exp Med, 1994 Oct 01; 180(4). PMID: 7523569    Free PMC article.
Highly Cited.
CD4/major histocompatibility complex class II interaction analyzed with CD4- and lymphocyte activation gene-3 (LAG-3)-Ig fusion proteins.
B Huard, P Prigent, +2 authors, F Triebel.
Eur J Immunol, 1995 Sep 01; 25(9). PMID: 7589152
Enhancement of antitumor immunity by CTLA-4 blockade.
D R Leach, M F Krummel, J P Allison.
Science, 1996 Mar 22; 271(5256). PMID: 8596936
Highly Cited.
Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation.
M Cella, D Scheidegger, +3 authors, G Alber.
J Exp Med, 1996 Aug 01; 184(2). PMID: 8760829    Free PMC article.
Highly Cited.
Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors.
I Melero, W W Shuford, +5 authors, L Chen.
Nat Med, 1997 Jun 01; 3(6). PMID: 9176498
Highly Cited.
A new member of the tumor necrosis factor/nerve growth factor receptor family inhibits T cell receptor-induced apoptosis.
G Nocentini, L Giunchi, +5 authors, C Riccardi.
Proc Natl Acad Sci U S A, 1997 Jun 10; 94(12). PMID: 9177197    Free PMC article.
Highly Cited.
Presence of the T-cell activation marker OX-40 on tumor infiltrating lymphocytes and draining lymph node cells from patients with melanoma and head and neck cancers.
J T Vetto, S Lum, +4 authors, A Weinberg.
Am J Surg, 1997 Oct 27; 174(3). PMID: 9324133
CD27, a member of the tumor necrosis factor receptor superfamily, activates NF-kappaB and stress-activated protein kinase/c-Jun N-terminal kinase via TRAF2, TRAF5, and NF-kappaB-inducing kinase.
H Akiba, H Nakano, +9 authors, K Okumura.
J Biol Chem, 1998 May 28; 273(21). PMID: 9582383
Prevention of allogeneic fetal rejection by tryptophan catabolism.
D H Munn, M Zhou, +5 authors, A L Mellor.
Science, 1998 Aug 26; 281(5380). PMID: 9712583
Highly Cited.
Immune biomarkers of treatment failure for a patient on a phase I clinical trial of pembrolizumab plus radiotherapy.
Gregory S Alexander, Joshua D Palmer, +8 authors, Bo Lu.
J Hematol Oncol, 2016 Sep 25; 9(1). PMID: 27663515    Free PMC article.
Is There Still Room for Cancer Vaccines at the Era of Checkpoint Inhibitors.
Soumaya Karaki, Marie Anson, +4 authors, Eric Tartour.
Vaccines (Basel), 2016 Nov 10; 4(4). PMID: 27827885    Free PMC article.
Potential applications of nanoparticles in cancer immunotherapy.
Yimei Jia, Abdelwahab Omri, Lakshmi Krishnan, Michael J McCluskie.
Hum Vaccin Immunother, 2016 Nov 22; 13(1). PMID: 27870598    Free PMC article.
Biomimetic biodegradable artificial antigen presenting cells synergize with PD-1 blockade to treat melanoma.
A K Kosmides, R A Meyer, +4 authors, J P Schneck.
Biomaterials, 2016 Dec 13; 118. PMID: 27940380    Free PMC article.
Advancing Immune and Cell-Based Therapies Through Imaging.
Vladimir Ponomarev.
Mol Imaging Biol, 2017 Mar 09; 19(3). PMID: 28271366    Free PMC article.
The Five Immune Forces Impacting DNA-Based Cancer Immunotherapeutic Strategy.
Suneetha Amara, Venkataswarup Tiriveedhi.
Int J Mol Sci, 2017 Mar 18; 18(3). PMID: 28304339    Free PMC article.
Retroviral Replicating Vector Delivery of miR-PDL1 Inhibits Immune Checkpoint PDL1 and Enhances Immune Responses In Vitro.
Amy H Lin, Christopher G Twitty, +5 authors, Douglas J Jolly.
Mol Ther Nucleic Acids, 2017 Mar 23; 6. PMID: 28325288    Free PMC article.
Biological and clinical significance of tryptophan-catabolizing enzymes in cutaneous T-cell lymphomas.
Pilvi Maliniemi, Kirsi Laukkanen, +7 authors, Annamari Ranki.
Oncoimmunology, 2017 Apr 14; 6(3). PMID: 28405495    Free PMC article.
Immune System, Friend or Foe of Oncolytic Virotherapy?
Anna C Filley, Mahua Dey.
Front Oncol, 2017 Jun 08; 7. PMID: 28589085    Free PMC article.
Toxicity and Immunogenicity in Murine Melanoma following Exposure to Physical Plasma-Derived Oxidants.
Sander Bekeschus, Katrin Rödder, +6 authors, Rajesh Kumar Gandhirajan.
Oxid Med Cell Longev, 2017 Aug 02; 2017. PMID: 28761621    Free PMC article.
Improving radiotherapy in cancer treatment: Promises and challenges.
Helen H W Chen, Macus Tien Kuo.
Oncotarget, 2017 Oct 06; 8(37). PMID: 28977985    Free PMC article.
MDM2 Antagonists Counteract Drug-Induced DNA Damage.
Anna E Vilgelm, Priscilla Cobb, +12 authors, Ann Richmond.
EBioMedicine, 2017 Oct 17; 24. PMID: 29030058    Free PMC article.
Nanoparticles: augmenting tumor antigen presentation for vaccine and immunotherapy treatments of cancer.
Charles B Chesson, Andrew Zloza.
Nanomedicine (Lond), 2017 Nov 04; 12(23). PMID: 29098928    Free PMC article.
New Strategies Using Antibody Combinations to Increase Cancer Treatment Effectiveness.
Isabel Corraliza-Gorjón, Beatriz Somovilla-Crespo, +2 authors, Leonor Kremer.
Front Immunol, 2018 Jan 10; 8. PMID: 29312320    Free PMC article.
Anticancer Mechanisms in Two Murine Bone Marrow-Derived Dendritic Cell Subsets Activated with TLR4 Agonists.
Alexander Bagaev, Aleksey Pichugin, +3 authors, Ravshan I Ataullakhanov.
J Immunol, 2018 Mar 04; 200(8). PMID: 29500244    Free PMC article.
Short- and long-term evolution in our arms race with cancer: Why the war on cancer is winnable.
Jay A Rosenheim.
Evol Appl, 2018 Jun 22; 11(6). PMID: 29928294    Free PMC article.
Targeting the IDO1 pathway in cancer: from bench to bedside.
Ming Liu, Xu Wang, +4 authors, Yong Li.
J Hematol Oncol, 2018 Aug 03; 11(1). PMID: 30068361    Free PMC article.
Highly Cited. Review.
Epigenetic treatment of multiple myeloma mediates tumor intrinsic and extrinsic immunomodulatory effects.
Lien De Beck, Sarah Melhaoui, +5 authors, Ken Maes.
Oncoimmunology, 2018 Oct 06; 7(10). PMID: 30288346    Free PMC article.
Stimulation of natural killer cells with rhCD137 ligand enhances tumor-targeting antibody efficacy in gastric cancer.
Toshihiro Misumi, Kazuaki Tanabe, Nobuaki Fujikuni, Hideki Ohdan.
PLoS One, 2018 Oct 16; 13(10). PMID: 30321186    Free PMC article.
Breaking Therapy Resistance: An Update on Oncolytic Newcastle Disease Virus for Improvements of Cancer Therapy.
Volker Schirrmacher, Stefaan van Gool, Wilfried Stuecker.
Biomedicines, 2019 Sep 05; 7(3). PMID: 31480379    Free PMC article.
Checkpoint molecules coordinately restrain hyperactivated effector T cells in the tumor microenvironment.
Min Yang, Wenwen Du, +9 authors, Binfeng Lu.
Oncoimmunology, 2020 Feb 23; 9(1). PMID: 32076578    Free PMC article.
Blockade of PD-1 and LAG-3 Immune Checkpoints Combined with Vaccination Restores the Function of Antiviral Tissue-Resident CD8+ TRM Cells and Reduces Ocular Herpes Simplex Infection and Disease in HLA Transgenic Rabbits.
Soumyabrata Roy, Pierre-Gregoire Coulon, +11 authors, Lbachir BenMohamed.
J Virol, 2019 Jun 21; 93(18). PMID: 31217250    Free PMC article.
Blockade of LAG-3 Immune Checkpoint Combined With Therapeutic Vaccination Restore the Function of Tissue-Resident Anti-viral CD8+ T Cells and Protect Against Recurrent Ocular Herpes Simplex Infection and Disease.
Soumyabrata Roy, Pierre-Grégoire Coulon, +7 authors, Lbachir BenMohamed.
Front Immunol, 2019 Jan 09; 9. PMID: 30619285    Free PMC article.
Immune-enrichment of non-small cell lung cancer baseline biopsies for multiplex profiling define prognostic immune checkpoint combinations for patient stratification.
Anne Monette, Derek Bergeron, +7 authors, Réjean Lapointe.
J Immunother Cancer, 2019 Mar 30; 7(1). PMID: 30922393    Free PMC article.
Cancer Nano-Immunotherapy from the Injection to the Target: The Role of Protein Corona.
Idoia Mikelez-Alonso, Antonio Aires, Aitziber L Cortajarena.
Int J Mol Sci, 2020 Jan 18; 21(2). PMID: 31947622    Free PMC article.
Armed oncolytic viruses: A kick-start for anti-tumor immunity.
J F de Graaf, L de Vor, R A M Fouchier, B G van den Hoogen.
Cytokine Growth Factor Rev, 2018 Mar 27; 41. PMID: 29576283    Free PMC article.
Highly Cited. Review.
Combining Oncolytic Viruses With Cancer Immunotherapy: Establishing a New Generation of Cancer Treatment.
Tao Shi, Xueru Song, +2 authors, Jia Wei.
Front Immunol, 2020 May 16; 11. PMID: 32411132    Free PMC article.
Combinatorial assessment of ctDNA release and mutational burden predicts anti-PD(L)1 therapy outcome in nonsmall-cell lung cancer.
Wenfeng Fang, Yuxiang Ma, +11 authors, Li Zhang.
Clin Transl Med, 2020 Jun 09; 10(1). PMID: 32508057    Free PMC article.
Biological Factors behind Melanoma Response to Immune Checkpoint Inhibitors.
Magdalena Olbryt, Marcin Rajczykowski, Wiesława Widłak.
Int J Mol Sci, 2020 Jun 11; 21(11). PMID: 32517213    Free PMC article.
Features associated with melanoma metastasis in Latvia.
Dace Pjanova, Dace Ruklisa, +3 authors, Ingrida Cema.
Oncol Lett, 2020 Aug 31; 20(4). PMID: 32863930    Free PMC article.
Balancing Cancer Immunotherapy Efficacy and Toxicity.
Douglas B Johnson, Baruch D Jakubovic, Vincent Sibaud, Meghan E Sise.
J Allergy Clin Immunol Pract, 2020 Jul 01; 8(9). PMID: 32599218    Free PMC article.
Progress of immune checkpoint LAG-3 in immunotherapy.
Chanchan Shan, Xing Li, Jian Zhang.
Oncol Lett, 2020 Sep 24; 20(5). PMID: 32963613    Free PMC article.
The promising immune checkpoint LAG-3: from tumor microenvironment to cancer immunotherapy.
Long Long, Xue Zhang, +4 authors, Honglei Chen.
Genes Cancer, 2019 Jan 04; 9(5-6). PMID: 30603054    Free PMC article.
Highly Cited. Review.
Combinatorial Approach to Improve Cancer Immunotherapy: Rational Drug Design Strategy to Simultaneously Hit Multiple Targets to Kill Tumor Cells and to Activate the Immune System.
Shweta Joshi, Donald L Durden.
J Oncol, 2019 Mar 12; 2019. PMID: 30853982    Free PMC article.
Molecular background of skin melanoma development and progression: therapeutic implications.
Magdalena Olbryt.
Postepy Dermatol Alergol, 2019 Jul 20; 36(2). PMID: 31320844    Free PMC article.
Immune Checkpoint Receptors Tim-3 and PD-1 Regulate Monocyte and T Lymphocyte Function in Septic Patients.
Qi Xia, Li Wei, +3 authors, Yi Zhang.
Mediators Inflamm, 2019 Jan 01; 2018. PMID: 30595665    Free PMC article.
Enhanced Antitumor Immune Response in 2'-5' Oligoadenylate Synthetase-Like 1- (OASL1-) Deficient Mice upon Cisplatin Chemotherapy and Radiotherapy.
Chan Kyu Sim, Jung Hoon Lee, +2 authors, Myeong Sup Lee.
J Immunol Res, 2019 May 03; 2019. PMID: 31049360    Free PMC article.
Targeted Delivery of CXCL9 and OX40L by Mesenchymal Stem Cells Elicits Potent Antitumor Immunity.
Pan Yin, Liming Gui, +6 authors, Wei-Qiang Gao.
Mol Ther, 2020 Aug 23; 28(12). PMID: 32827461    Free PMC article.
Magnesium in Combinatorial With Valproic Acid Suppressed the Proliferation and Migration of Human Bladder Cancer Cells.
Tianye Li, Yang Yu, +7 authors, Bing Wang.
Front Oncol, 2020 Dec 29; 10. PMID: 33363019    Free PMC article.
Endocrine toxicities of immune checkpoint inhibitors.
Jordan J Wright, Alvin C Powers, Douglas B Johnson.
Nat Rev Endocrinol, 2021 Apr 21; 17(7). PMID: 33875857    Free PMC article.
Metabolic modulation by CDK4/6 inhibitor promotes chemokine-mediated recruitment of T cells into mammary tumors.
Roman V Uzhachenko, Vijaya Bharti, +11 authors, Anna E Vilgelm.
Cell Rep, 2021 Apr 08; 35(1). PMID: 33826903    Free PMC article.
Immune-checkpoint inhibitors: long-term implications of toxicity.
Douglas B Johnson, Caroline A Nebhan, Javid J Moslehi, Justin M Balko.
Nat Rev Clin Oncol, 2022 Jan 28; 19(4). PMID: 35082367    Free PMC article.
CD40- and 41BB-specific antibody fusion proteins with PDL1 blockade-restricted agonism.
Juliane Medler, Kirstin Kucka, +7 authors, Harald Wajant.
Theranostics, 2022 Feb 25; 12(4). PMID: 35198053    Free PMC article.