. 2022 Jan; 21(1):28.
doi: 10.1186/s12943-021-01489-2.

Combination strategies with PD-1/PD-L1 blockade: current advances and future directions

Ming Yi 1 Xiaoli Zheng 2 Mengke Niu 1 Shuangli Zhu 1 Hong Ge 3 Kongming Wu 4 
  • PMID: 35062949
  •     326 References
  •     4 citations


Antibodies targeting programmed cell death protein-1 (PD-1) or its ligand PD-L1 rescue T cells from exhausted status and revive immune response against cancer cells. Based on the immense success in clinical trials, ten α-PD-1 (nivolumab, pembrolizumab, cemiplimab, sintilimab, camrelizumab, toripalimab, tislelizumab, zimberelimab, prolgolimab, and dostarlimab) and three α-PD-L1 antibodies (atezolizumab, durvalumab, and avelumab) have been approved for various types of cancers. Nevertheless, the low response rate of α-PD-1/PD-L1 therapy remains to be resolved. For most cancer patients, PD-1/PD-L1 pathway is not the sole speed-limiting factor of antitumor immunity, and it is insufficient to motivate effective antitumor immune response by blocking PD-1/PD-L1 axis. It has been validated that some combination therapies, including α-PD-1/PD-L1 plus chemotherapy, radiotherapy, angiogenesis inhibitors, targeted therapy, other immune checkpoint inhibitors, agonists of the co-stimulatory molecule, stimulator of interferon genes agonists, fecal microbiota transplantation, epigenetic modulators, or metabolic modulators, have superior antitumor efficacies and higher response rates. Moreover, bifunctional or bispecific antibodies containing α-PD-1/PD-L1 moiety also elicited more potent antitumor activity. These combination strategies simultaneously boost multiple processes in cancer-immunity cycle, remove immunosuppressive brakes, and orchestrate an immunosupportive tumor microenvironment. In this review, we summarized the synergistic antitumor efficacies and mechanisms of α-PD-1/PD-L1 in combination with other therapies. Moreover, we focused on the advances of α-PD-1/PD-L1-based immunomodulatory strategies in clinical studies. Given the heterogeneity across patients and cancer types, individualized combination selection could improve the effects of α-PD-1/PD-L1-based immunomodulatory strategies and relieve treatment resistance.

Keywords: Angiogenesis inhibitor; Bispecific antibody; Combination therapy; Gut microbiota; PD-1; PD-L1; Radiotherapy; STING.

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A Phase I Trial of Regional Mesothelin-Targeted CAR T-cell Therapy in Patients with Malignant Pleural Disease, in Combination with the Anti-PD-1 Agent Pembrolizumab.
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Cancer Discov, 2021 Jul 17; 11(11). PMID: 34266984    Free PMC article.
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Lancet Oncol, 2021 May 21; 22(6). PMID: 34015311
Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer.
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Randomized Phase II Trial of Nivolumab With Stereotactic Body Radiotherapy Versus Nivolumab Alone in Metastatic Head and Neck Squamous Cell Carcinoma.
Sean McBride, Eric Sherman, +16 authors, Nancy Lee.
J Clin Oncol, 2020 Aug 22; 39(1). PMID: 32822275    Free PMC article.
Antiangiogenic therapy reverses the immunosuppressive breast cancer microenvironment.
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Biomark Res, 2021 Jul 24; 9(1). PMID: 34294146    Free PMC article.
Novel roles of c-Met in the survival of renal cancer cells through the regulation of HO-1 and PD-L1 expression.
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J Biol Chem, 2015 Feb 04; 290(13). PMID: 25645920    Free PMC article.
Expression of Vascular Endothelial Growth Factor in Ovarian Cancer Inhibits Tumor Immunity through the Accumulation of Myeloid-Derived Suppressor Cells.
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Clin Cancer Res, 2016 Jul 13; 23(2). PMID: 27401249
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Immune escape to PD-L1/PD-1 blockade: seven steps to success (or failure).
J M Kim, D S Chen.
Ann Oncol, 2016 May 22; 27(8). PMID: 27207108
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ARCTIC: durvalumab with or without tremelimumab as third-line or later treatment of metastatic non-small-cell lung cancer.
D Planchard, N Reinmuth, +15 authors, D Kowalski.
Ann Oncol, 2020 Mar 24; 31(5). PMID: 32201234
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Robert D Leone, Leisha A Emens.
J Immunother Cancer, 2018 Jun 20; 6(1). PMID: 29914571    Free PMC article.
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Direct and Indirect Modulation of T Cells by VEGF-A Counteracted by Anti-Angiogenic Treatment.
Morgane Bourhis, Juliette Palle, Isabelle Galy-Fauroux, Magali Terme.
Front Immunol, 2021 Apr 16; 12. PMID: 33854498    Free PMC article.
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Cancer Res, 2010 Jun 10; 70(13). PMID: 20530679
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TIGIT/CD155 blockade enhances anti-PD-L1 therapy in head and neck squamous cell carcinoma by targeting myeloid-derived suppressor cells.
Liang Mao, Yao Xiao, +3 authors, Zhi-Jun Sun.
Oral Oncol, 2021 Aug 02; 121. PMID: 34333450
Camrelizumab plus carboplatin and pemetrexed versus chemotherapy alone in chemotherapy-naive patients with advanced non-squamous non-small-cell lung cancer (CameL): a randomised, open-label, multicentre, phase 3 trial.
Caicun Zhou, Gongyan Chen, +34 authors, CameL Study Group.
Lancet Respir Med, 2020 Dec 22; 9(3). PMID: 33347829
MAHOGANY: margetuximab combination in HER2+ unresectable/metastatic gastric/gastroesophageal junction adenocarcinoma.
Daniel Vt Catenacci, Minori Rosales, +4 authors, Yoon-Koo Kang.
Future Oncol, 2020 Dec 03; 17(10). PMID: 33263418
Severe immune-related adverse events are common with sequential PD-(L)1 blockade and osimertinib.
A J Schoenfeld, K C Arbour, +7 authors, M D Hellmann.
Ann Oncol, 2019 Mar 09; 30(5). PMID: 30847464    Free PMC article.
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Cell Rep Med, 2020 Dec 31; 1(9). PMID: 33377134    Free PMC article.
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Cancer Res, 2018 Jul 04; 78(17). PMID: 29967259
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Atezolizumab plus nab-paclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (IMpassion130): updated efficacy results from a randomised, double-blind, placebo-controlled, phase 3 trial.
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Lancet Oncol, 2019 Dec 02; 21(1). PMID: 31786121
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Phase I Trial of M7824 (MSB0011359C), a Bifunctional Fusion Protein Targeting PD-L1 and TGFβ, in Advanced Solid Tumors.
Julius Strauss, Christopher R Heery, +12 authors, James L Gulley.
Clin Cancer Res, 2018 Jan 05; 24(6). PMID: 29298798    Free PMC article.
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Camrelizumab Plus Apatinib in Patients With Advanced Cervical Cancer (CLAP): A Multicenter, Open-Label, Single-Arm, Phase II Trial.
Chunyan Lan, Jingxian Shen, +15 authors, Xin Huang.
J Clin Oncol, 2020 Oct 15; 38(34). PMID: 33052760    Free PMC article.
The PEMDAC phase 2 study of pembrolizumab and entinostat in patients with metastatic uveal melanoma.
Lars Ny, Henrik Jespersen, +15 authors, Jonas A Nilsson.
Nat Commun, 2021 Aug 29; 12(1). PMID: 34453044    Free PMC article.
cGAS-STING, an important pathway in cancer immunotherapy.
Minlin Jiang, Peixin Chen, +8 authors, Caicun Zhou.
J Hematol Oncol, 2020 Jun 24; 13(1). PMID: 32571374    Free PMC article.
Chimeric antigen receptor T cells: a novel therapy for solid tumors.
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Manipulating Gut Microbiota Composition to Enhance the Therapeutic Effect of Cancer Immunotherapy.
Ming Yi, Dechao Jiao, +3 authors, Kongming Wu.
Integr Cancer Ther, 2019 Sep 14; 18. PMID: 31517538    Free PMC article.
Pembrolizumab plus chemotherapy versus chemotherapy alone for first-line treatment of advanced oesophageal cancer (KEYNOTE-590): a randomised, placebo-controlled, phase 3 study.
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Lancet, 2021 Aug 30; 398(10302). PMID: 34454674
Nivolumab Plus Erlotinib in Patients With EGFR-Mutant Advanced NSCLC.
Scott Gettinger, Matthew D Hellmann, +12 authors, Naiyer Rizvi.
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A novel bispecific nanobody with PD-L1/TIGIT dual immune checkpoint blockade.
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Durvalumab as third-line or later treatment for advanced non-small-cell lung cancer (ATLANTIC): an open-label, single-arm, phase 2 study.
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Lancet Oncol, 2018 Mar 17; 19(4). PMID: 29545095    Free PMC article.
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Metronomic chemotherapy with low-dose cyclophosphamide plus gemcitabine can induce anti-tumor T cell immunity in vivo.
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Cancer Immunol Immunother, 2012 Aug 29; 62(2). PMID: 22926062
The Folate Pathway Inhibitor Pemetrexed Pleiotropically Enhances Effects of Cancer Immunotherapy.
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Clin Cancer Res, 2019 Aug 15; 25(23). PMID: 31409612
Gemcitabine nanoparticles promote antitumor immunity against melanoma.
Yuan Zhang, Xin Bush, Bingfang Yan, Justin A Chen.
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Martin Reck, Delvys Rodríguez-Abreu, +16 authors, KEYNOTE-024 Investigators.
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Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system.
T Iwahara, J Fujimoto, +6 authors, T Yamamoto.
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Guido Kroemer, Lorenzo Galluzzi, Oliver Kepp, Laurence Zitvogel.
Annu Rev Immunol, 2012 Nov 20; 31. PMID: 23157435
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TGFβ drives immune evasion in genetically reconstituted colon cancer metastasis.
Daniele V F Tauriello, Sergio Palomo-Ponce, +15 authors, Eduard Batlle.
Nature, 2018 Feb 15; 554(7693). PMID: 29443964
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Combined nivolumab and ipilimumab versus ipilimumab alone in patients with advanced melanoma: 2-year overall survival outcomes in a multicentre, randomised, controlled, phase 2 trial.
F Stephen Hodi, Jason Chesney, +18 authors, Michael A Postow.
Lancet Oncol, 2016 Sep 14; 17(11). PMID: 27622997    Free PMC article.
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The PD1:PD-L1/2 Pathway from Discovery to Clinical Implementation.
Kankana Bardhan, Theodora Anagnostou, Vassiliki A Boussiotis.
Front Immunol, 2016 Dec 27; 7. PMID: 28018338    Free PMC article.
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Qian Liu, Shengnan Yu, +3 authors, Kongming Wu.
Mol Cancer, 2018 Feb 20; 17(1). PMID: 29455669    Free PMC article.
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Impact of 5-Fu/oxaliplatin on mouse dendritic cells and synergetic effect with a colon cancer vaccine.
Xinqiang Hong, Tiangeng Dong, +4 authors, Weixin Niu.
Chin J Cancer Res, 2018 Jun 05; 30(2). PMID: 29861605    Free PMC article.
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Blockade of checkpoint receptor PVRIG unleashes anti-tumor immunity of NK cells in murine and human solid tumors.
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J Hematol Oncol, 2021 Jun 28; 14(1). PMID: 34174928    Free PMC article.
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LAG-3 and PD-1+LAG-3 inhibition promote anti-tumor immune responses in human autologous melanoma/T cell co-cultures.
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Making the first move in EGFR-driven or ALK-driven NSCLC: first-generation or next-generation TKI?
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Pembrolizumab Plus Pegylated Interferon alfa-2b or Ipilimumab for Advanced Melanoma or Renal Cell Carcinoma: Dose-Finding Results from the Phase Ib KEYNOTE-029 Study.
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Cancer immunotherapy using anti-TIM3/PD-1 bispecific antibody: a patent evaluation of EP3356411A1.
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Nat Rev Clin Oncol, 2018 Jun 07; 15(8). PMID: 29872177
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Avelumab plus standard-of-care chemoradiotherapy versus chemoradiotherapy alone in patients with locally advanced squamous cell carcinoma of the head and neck: a randomised, double-blind, placebo-controlled, multicentre, phase 3 trial.
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Single-Arm Phases 1 and 2 Trial of Niraparib in Combination With Pembrolizumab in Patients With Recurrent Platinum-Resistant Ovarian Carcinoma.
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Safety and Antitumor Activity of α-PD-L1 Antibody as Monotherapy or in Combination with α-TIM-3 Antibody in Patients with Microsatellite Instability-High/Mismatch Repair-Deficient Tumors.
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A Phase II Study of Pembrolizumab in EGFR-Mutant, PD-L1+, Tyrosine Kinase Inhibitor Naïve Patients With Advanced NSCLC.
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Combined VEGFR and CTLA-4 blockade increases the antigen-presenting function of intratumoral DCs and reduces the suppressive capacity of intratumoral MDSCs.
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A Dual-Bioresponsive Drug-Delivery Depot for Combination of Epigenetic Modulation and Immune Checkpoint Blockade.
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Blocking TGF-β Signaling To Enhance The Efficacy Of Immune Checkpoint Inhibitor.
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Phase Ib study of atezolizumab combined with cobimetinib in patients with solid tumors.
M D Hellmann, T-W Kim, +18 authors, J Bendell.
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Bintrafusp Alfa, a Bifunctional Fusion Protein Targeting TGF-β and PD-L1, in Second-Line Treatment of Patients With NSCLC: Results From an Expansion Cohort of a Phase 1 Trial.
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Durable Clinical Benefit With Nivolumab Plus Ipilimumab in DNA Mismatch Repair-Deficient/Microsatellite Instability-High Metastatic Colorectal Cancer.
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Next-generation immuno-oncology agents: current momentum shifts in cancer immunotherapy.
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Safety and clinical activity with an anti-PD-1 antibody JS001 in advanced melanoma or urologic cancer patients.
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ICOS agonism by JTX-2011 (vopratelimab) requires initial T cell priming and Fc cross-linking for optimal T cell activation and anti-tumor immunity in preclinical models.
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Cancer-associated fibroblasts: an emerging target of anti-cancer immunotherapy.
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Phase Ib Study of Crizotinib plus Pembrolizumab in Patients with Previously Untreated Advanced Non-Small Cell Lung Cancer with ALK Translocation.
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Safety, Efficacy, and Pharmacodynamics of Tremelimumab Plus Durvalumab for Patients With Unresectable Hepatocellular Carcinoma: Randomized Expansion of a Phase I/II Study.
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Ming Yi, Linping Xu, +3 authors, Kongming Wu.
J Hematol Oncol, 2020 Mar 31; 13(1). PMID: 32222150    Free PMC article.
Systematically optimized BCMA/CS1 bispecific CAR-T cells robustly control heterogeneous multiple myeloma.
Eugenia Zah, Eunwoo Nam, +6 authors, Yvonne Y Chen.
Nat Commun, 2020 May 10; 11(1). PMID: 32385241    Free PMC article.
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Joseph Conlon, Dara L Burdette, +10 authors, Katherine A Fitzgerald.
J Immunol, 2013 Apr 16; 190(10). PMID: 23585680    Free PMC article.
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Safety and Clinical Activity of Pembrolizumab and Multisite Stereotactic Body Radiotherapy in Patients With Advanced Solid Tumors.
Jason J Luke, Jeffrey M Lemons, +17 authors, Steven J Chmura.
J Clin Oncol, 2018 Feb 14; 36(16). PMID: 29437535    Free PMC article.
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Yang Liu, Yinping Dong, +3 authors, Jinming Yu.
J Hematol Oncol, 2018 Aug 18; 11(1). PMID: 30115069    Free PMC article.
Highly Cited. Review.
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.
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Durvalumab With or Without Tremelimumab vs Standard Chemotherapy in First-line Treatment of Metastatic Non-Small Cell Lung Cancer: The MYSTIC Phase 3 Randomized Clinical Trial.
Naiyer A Rizvi, Byoung Chul Cho, +28 authors, MYSTIC Investigators.
JAMA Oncol, 2020 Apr 10; 6(5). PMID: 32271377    Free PMC article.
Clinical relevance of PD-L1 expression and CD8+ T cells infiltration in patients with EGFR-mutated and ALK-rearranged lung cancer.
Si-Yang Liu, Zhong-Yi Dong, +12 authors, Yi-Long Wu.
Lung Cancer, 2018 Nov 16; 125. PMID: 30429043
The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.
Vyara Matson, Jessica Fessler, +5 authors, Thomas F Gajewski.
Science, 2018 Jan 06; 359(6371). PMID: 29302014    Free PMC article.
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Novel immune checkpoint targets: moving beyond PD-1 and CTLA-4.
Shuang Qin, Linping Xu, +3 authors, Suxia Luo.
Mol Cancer, 2019 Nov 07; 18(1). PMID: 31690319    Free PMC article.
Highly Cited. Review.
Engineering a Smart Agent for Enhanced Immunotherapy Effect by Simultaneously Blocking PD-L1 and CTLA-4.
Chunjuan Jiang, Le Zhang, +5 authors, Shaoli Song.
Adv Sci (Weinh), 2021 Sep 03; 8(20). PMID: 34473430    Free PMC article.
Increased Hepatotoxicity Associated with Sequential Immune Checkpoint Inhibitor and Crizotinib Therapy in Patients with Non-Small Cell Lung Cancer.
Jessica J Lin, Emily Chin, +8 authors, Alice T Shaw.
J Thorac Oncol, 2018 Sep 12; 14(1). PMID: 30205166    Free PMC article.
Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.
Ayelet Sivan, Leticia Corrales, +9 authors, Thomas F Gajewski.
Science, 2015 Nov 07; 350(6264). PMID: 26541606    Free PMC article.
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PD-1 Blockade and CD27 Stimulation Activate Distinct Transcriptional Programs That Synergize for CD8+ T-Cell-Driven Antitumor Immunity.
Sarah L Buchan, Mohannad Fallatah, +8 authors, Aymen Al-Shamkhani.
Clin Cancer Res, 2018 Mar 09; 24(10). PMID: 29514845    Free PMC article.
CDK4/6 Inhibition Augments Antitumor Immunity by Enhancing T-cell Activation.
Jiehui Deng, Eric S Wang, +44 authors, Kwok-Kin Wong.
Cancer Discov, 2017 Nov 05; 8(2). PMID: 29101163    Free PMC article.
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Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis.
Giovanna Schiavoni, Antonella Sistigu, +10 authors, Laura Bracci.
Cancer Res, 2010 Dec 16; 71(3). PMID: 21156650
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Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients.
V Gopalakrishnan, C N Spencer, +67 authors, J A Wargo.
Science, 2017 Nov 04; 359(6371). PMID: 29097493    Free PMC article.
Highly Cited.
Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients.
Diwakar Davar, Amiran K Dzutsev, +29 authors, Hassane M Zarour.
Science, 2021 Feb 06; 371(6529). PMID: 33542131    Free PMC article.
Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study.
Jedd D Wolchok, Bart Neyns, +14 authors, Celeste Lebbé.
Lancet Oncol, 2009 Dec 17; 11(2). PMID: 20004617
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5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity.
Julie Vincent, Grégoire Mignot, +7 authors, François Ghiringhelli.
Cancer Res, 2010 Apr 15; 70(8). PMID: 20388795
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Development of PARP and Immune-Checkpoint Inhibitor Combinations.
Ross A Stewart, Patrick G Pilié, Timothy A Yap.
Cancer Res, 2018 Dec 01; 78(24). PMID: 30498083
Durvalumab plus platinum-etoposide versus platinum-etoposide in first-line treatment of extensive-stage small-cell lung cancer (CASPIAN): a randomised, controlled, open-label, phase 3 trial.
Luis Paz-Ares, Mikhail Dvorkin, +22 authors, CASPIAN investigators.
Lancet, 2019 Oct 09; 394(10212). PMID: 31590988
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CTLA-4: new insights into its biological function and use in tumor immunotherapy.
Jackson G Egen, Michael S Kuhns, James P Allison.
Nat Immunol, 2002 Jun 28; 3(7). PMID: 12087419
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Radiotherapy and anti-PD-1/PD-L1 combinations in lung cancer: building better translational research platforms.
T Kordbacheh, J Honeychurch, +2 authors, T Illidge.
Ann Oncol, 2018 Jan 09; 29(2). PMID: 29309540
FGFR-TKI resistance in cancer: current status and perspectives.
Sitong Yue, Yukun Li, +4 authors, Daichao Wu.
J Hematol Oncol, 2021 Feb 12; 14(1). PMID: 33568192    Free PMC article.
Circulating myeloid-derived suppressor cells increase in patients undergoing neo-adjuvant chemotherapy for breast cancer.
Robert Wesolowski, Megan C Duggan, +15 authors, William E Carson.
Cancer Immunol Immunother, 2017 Jul 09; 66(11). PMID: 28688082    Free PMC article.
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Mol Cell Biol, 2005 Oct 18; 25(21). PMID: 16227604    Free PMC article.
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The construction, expression, and enhanced anti-tumor activity of YM101: a bispecific antibody simultaneously targeting TGF-β and PD-L1.
Ming Yi, Jing Zhang, +6 authors, Kongming Wu.
J Hematol Oncol, 2021 Feb 18; 14(1). PMID: 33593403    Free PMC article.
A novel tetravalent bispecific antibody targeting programmed death 1 and tyrosine-protein kinase Met for treatment of gastric cancer.
Weihua Hou, Qingyun Yuan, +4 authors, Min Yu.
Invest New Drugs, 2018 Dec 05; 37(5). PMID: 30511201
Immune-Related Adverse Events Associated with Immune Checkpoint Blockade.
Michael A Postow, Robert Sidlow, Matthew D Hellmann.
N Engl J Med, 2018 Jan 11; 378(2). PMID: 29320654
Highly Cited. Review.
Tumor-selective blockade of CD47 signaling with a CD47/PD-L1 bispecific antibody for enhanced anti-tumor activity and limited toxicity.
Yan Wang, Haiqing Ni, +15 authors, Junjian Liu.
Cancer Immunol Immunother, 2020 Aug 08; 70(2). PMID: 32761423
Co-stimulatory agonists: An insight into the immunotherapy of cancer.
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EXCLI J, 2021 Jul 17; 20. PMID: 34267616    Free PMC article.
Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients.
Emanuela Romano, Monika Kusio-Kobialka, +7 authors, Daniel E Speiser.
Proc Natl Acad Sci U S A, 2015 Apr 29; 112(19). PMID: 25918390    Free PMC article.
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Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study.
Corey J Langer, Shirish M Gadgeel, +17 authors, KEYNOTE-021 investigators.
Lancet Oncol, 2016 Oct 18; 17(11). PMID: 27745820    Free PMC article.
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Novel therapies emerging in oncology to target the TGF-β pathway.
Byung-Gyu Kim, Ehsan Malek, +2 authors, James J Driscoll.
J Hematol Oncol, 2021 Apr 08; 14(1). PMID: 33823905    Free PMC article.
Advances and perspectives of PARP inhibitors.
Ming Yi, Bing Dong, +3 authors, Suxia Luo.
Exp Hematol Oncol, 2019 Nov 19; 8. PMID: 31737426    Free PMC article.
Cytokines in Cancer Immunotherapy.
Thomas A Waldmann.
Cold Spring Harb Perspect Biol, 2017 Nov 05; 10(12). PMID: 29101107    Free PMC article.
Highly Cited. Review.
STING agonist loaded lipid nanoparticles overcome anti-PD-1 resistance in melanoma lung metastasis via NK cell activation.
Takashi Nakamura, Takanori Sato, +6 authors, Hideyoshi Harashima.
J Immunother Cancer, 2021 Jul 04; 9(7). PMID: 34215690    Free PMC article.
Efficacy and safety of camrelizumab combined with apatinib in advanced triple-negative breast cancer: an open-label phase II trial.
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J Immunother Cancer, 2020 May 26; 8(1). PMID: 32448804    Free PMC article.
Lenvatinib plus pembrolizumab in patients with advanced endometrial cancer: an interim analysis of a multicentre, open-label, single-arm, phase 2 trial.
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Lancet Oncol, 2019 Mar 30; 20(5). PMID: 30922731
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Efficacy and Safety of Nivolumab Plus Ipilimumab in Patients With Advanced Hepatocellular Carcinoma Previously Treated With Sorafenib: The CheckMate 040 Randomized Clinical Trial.
Thomas Yau, Yoon-Koo Kang, +18 authors, Chiun Hsu.
JAMA Oncol, 2020 Oct 02; 6(11). PMID: 33001135    Free PMC article.
Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer.
Christina Twyman-Saint Victor, Andrew J Rech, +22 authors, Andy J Minn.
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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.
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PEGylated IL-10 (Pegilodecakin) Induces Systemic Immune Activation, CD8+ T Cell Invigoration and Polyclonal T Cell Expansion in Cancer Patients.
Aung Naing, Jeffrey R Infante, +21 authors, Martin Oft.
Cancer Cell, 2018 Nov 14; 34(5). PMID: 30423297    Free PMC article.
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Akshaya Chandrasekaran, Kevin M Elias.
Mol Cancer Ther, 2021 Sep 15; 20(11). PMID: 34518297    Free PMC article.
Nivolumab plus Ipilimumab in Advanced Non-Small-Cell Lung Cancer.
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N Engl J Med, 2019 Sep 29; 381(21). PMID: 31562796
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Safety and Efficacy of Durvalumab With or Without Tremelimumab in Patients With PD-L1-Low/Negative Recurrent or Metastatic HNSCC: The Phase 2 CONDOR Randomized Clinical Trial.
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JAMA Oncol, 2018 Nov 02; 5(2). PMID: 30383184    Free PMC article.
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The CDK4/6 Inhibitor Abemaciclib Induces a T Cell Inflamed Tumor Microenvironment and Enhances the Efficacy of PD-L1 Checkpoint Blockade.
David A Schaer, Richard P Beckmann, +19 authors, Michael Kalos.
Cell Rep, 2018 Mar 15; 22(11). PMID: 29539425
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Jifeng Yu, Hao Sun, +4 authors, Zhongxing Jiang.
Exp Hematol Oncol, 2020 Dec 10; 9(1). PMID: 33292670    Free PMC article.
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Robert S Kerbel.
N Engl J Med, 2008 May 09; 358(19). PMID: 18463380    Free PMC article.
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The epigenetic immunomodulator, HBI-8000, enhances the response and reverses resistance to checkpoint inhibitors.
Reid P Bissonnette, Rosemary M Cesario, +2 authors, Mireille Gillings.
BMC Cancer, 2021 Sep 01; 21(1). PMID: 34461854    Free PMC article.
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Oncoimmunology, 2021 Aug 06; 10(1). PMID: 34350059    Free PMC article.
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Roland E Kontermann.
MAbs, 2012 Mar 29; 4(2). PMID: 22453100    Free PMC article.
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Combination cancer immunotherapy targeting PD-1 and GITR can rescue CD8.
Bei Wang, Wen Zhang, +21 authors, Dimitris Skokos.
Sci Immunol, 2018 Nov 06; 3(29). PMID: 30389797
Pembrolizumab plus Chemotherapy in Metastatic Non-Small-Cell Lung Cancer.
Leena Gandhi, Delvys Rodríguez-Abreu, +27 authors, KEYNOTE-189 Investigators.
N Engl J Med, 2018 Apr 17; 378(22). PMID: 29658856
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Blocking TIM-3 in Treatment-refractory Advanced Solid Tumors: A Phase Ia/b Study of LY3321367 with or without an Anti-PD-L1 Antibody.
James J Harding, Victor Moreno, +16 authors, Maria J de Miguel.
Clin Cancer Res, 2021 Jan 31; 27(8). PMID: 33514524
Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small-cell lung cancer (IMpower130): a multicentre, randomised, open-label, phase 3 trial.
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Lancet Oncol, 2019 May 28; 20(7). PMID: 31122901
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Avelumab plus axitinib versus sunitinib in advanced renal cell carcinoma: biomarker analysis of the phase 3 JAVELIN Renal 101 trial.
Robert J Motzer, Paul B Robbins, +20 authors, Toni K Choueiri.
Nat Med, 2020 Sep 09; 26(11). PMID: 32895571    Free PMC article.
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Sci Transl Med, 2017 Apr 14; 9(385). PMID: 28404865
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Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2.
Tadashi Yokosuka, Masako Takamatsu, +3 authors, Takashi Saito.
J Exp Med, 2012 May 30; 209(6). PMID: 22641383    Free PMC article.
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Bempegaldesleukin (NKTR-214) plus Nivolumab in Patients with Advanced Solid Tumors: Phase I Dose-Escalation Study of Safety, Efficacy, and Immune Activation (PIVOT-02).
Adi Diab, Nizar M Tannir, +20 authors, Daniel C Cho.
Cancer Discov, 2020 May 23; 10(8). PMID: 32439653
Pembrolizumab plus axitinib versus sunitinib monotherapy as first-line treatment of advanced renal cell carcinoma (KEYNOTE-426): extended follow-up from a randomised, open-label, phase 3 trial.
Thomas Powles, Elizabeth R Plimack, +17 authors, Brian I Rini.
Lancet Oncol, 2020 Dec 08; 21(12). PMID: 33284113
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
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J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
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PARP Inhibitor Efficacy Depends on CD8+ T-cell Recruitment via Intratumoral STING Pathway Activation in BRCA-Deficient Models of Triple-Negative Breast Cancer.
Constantia Pantelidou, Olmo Sonzogni, +14 authors, Geoffrey I Shapiro.
Cancer Discov, 2019 Apr 25; 9(6). PMID: 31015319    Free PMC article.
Highly Cited.
Oncology meets immunology: the cancer-immunity cycle.
Daniel S Chen, Ira Mellman.
Immunity, 2013 Jul 31; 39(1). PMID: 23890059
Highly Cited. Review.
Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors.
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Science, 2017 Nov 04; 359(6371). PMID: 29097494
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The Intersection between Tumor Angiogenesis and Immune Suppression.
Osama E Rahma, F Stephen Hodi.
Clin Cancer Res, 2019 Apr 05; 25(18). PMID: 30944124
Safety and Efficacy of Durvalumab and Tremelimumab Alone or in Combination in Patients with Advanced Gastric and Gastroesophageal Junction Adenocarcinoma.
Ronan J Kelly, Jeeyun Lee, +21 authors, Geoffrey Y Ku.
Clin Cancer Res, 2019 Nov 05; 26(4). PMID: 31676670    Free PMC article.
RAS-targeted therapies: is the undruggable drugged?
Amanda R Moore, Scott C Rosenberg, Frank McCormick, Shiva Malek.
Nat Rev Drug Discov, 2020 Jun 13; 19(8). PMID: 32528145    Free PMC article.
Distinct Roles of VEGFA and ANGPT2 in Lung Adenocarcinoma and Squamous Cell Carcinoma.
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First-Line Atezolizumab plus Chemotherapy in Extensive-Stage Small-Cell Lung Cancer.
Leora Horn, Aaron S Mansfield, +19 authors, IMpower133 Study Group.
N Engl J Med, 2018 Oct 04; 379(23). PMID: 30280641
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The efficacy and safety of combination of PD-1 and CTLA-4 inhibitors: a meta-analysis.
Kongju Wu, Ming Yi, +3 authors, Kongming Wu.
Exp Hematol Oncol, 2019 Nov 02; 8. PMID: 31673481    Free PMC article.
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Lancet Oncol, 2013 Jan 02; 14(1). PMID: 23276369
Highly Cited. Review.
CTLA-4 (CD152): A versatile receptor for immune-based therapy.
Holger Lingel, Monika C Brunner-Weinzierl.
Semin Immunol, 2019 Oct 13; 42. PMID: 31604536
Elements of cancer immunity and the cancer-immune set point.
Daniel S Chen, Ira Mellman.
Nature, 2017 Jan 20; 541(7637). PMID: 28102259
Highly Cited. Review.
Durvalumab, with or without tremelimumab, plus platinum-etoposide versus platinum-etoposide alone in first-line treatment of extensive-stage small-cell lung cancer (CASPIAN): updated results from a randomised, controlled, open-label, phase 3 trial.
Jonathan W Goldman, Mikhail Dvorkin, +23 authors, CASPIAN investigators.
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A human CD137×PD-L1 bispecific antibody promotes anti-tumor immunity via context-dependent T cell costimulation and checkpoint blockade.
Cecile Geuijen, Paul Tacken, +38 authors, Mark Throsby.
Nat Commun, 2021 Jul 23; 12(1). PMID: 34290245    Free PMC article.
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Julian A Marin-Acevedo, ErinMarie O Kimbrough, +2 authors, Yanyan Lou.
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A Phase I Study of APX005M and Cabiralizumab with or without Nivolumab in Patients with Melanoma, Kidney Cancer, or Non-Small Cell Lung Cancer Resistant to Anti-PD-1/PD-L1.
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Clin Cancer Res, 2021 Jun 19; 27(17). PMID: 34140403
Sintilimab plus a bevacizumab biosimilar (IBI305) versus sorafenib in unresectable hepatocellular carcinoma (ORIENT-32): a randomised, open-label, phase 2-3 study.
Zhenggang Ren, Jianming Xu, +38 authors, ORIENT-32 study group.
Lancet Oncol, 2021 Jun 19; 22(7). PMID: 34143971
Pembrolizumab versus Ipilimumab in Advanced Melanoma.
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N Engl J Med, 2015 Apr 22; 372(26). PMID: 25891173
Highly Cited.
Phase II Trial of IL-12 Plasmid Transfection and PD-1 Blockade in Immunologically Quiescent Melanoma.
Alain P Algazi, Christopher G Twitty, +21 authors, Adil I Daud.
Clin Cancer Res, 2020 May 08; 26(12). PMID: 32376655
RAS/MAPK Activation Is Associated with Reduced Tumor-Infiltrating Lymphocytes in Triple-Negative Breast Cancer: Therapeutic Cooperation Between MEK and PD-1/PD-L1 Immune Checkpoint Inhibitors.
Sherene Loi, Sathana Dushyanthen, +22 authors, Justin M Balko.
Clin Cancer Res, 2015 Oct 31; 22(6). PMID: 26515496    Free PMC article.
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Oxaliplatin induces immunogenic cell death in hepatocellular carcinoma cells and synergizes with immune checkpoint blockade therapy.
Hanzhang Zhu, Yuqiang Shan, +3 authors, Changku Jia.
Cell Oncol (Dordr), 2020 Aug 17; 43(6). PMID: 32797385
An orally available non-nucleotide STING agonist with antitumor activity.
Bo-Sheng Pan, Samanthi A Perera, +38 authors, George H Addona.
Science, 2020 Aug 21; 369(6506). PMID: 32820094
Gene modification strategies for next-generation CAR T cells against solid cancers.
Yonggui Tian, Yilu Li, Yupei Shao, Yi Zhang.
J Hematol Oncol, 2020 May 20; 13(1). PMID: 32423475    Free PMC article.
Blockade of mutant RAS oncogenic signaling with a special emphasis on KRAS.
Robert Roskoski.
Pharmacol Res, 2021 Aug 28; 172. PMID: 34450320
Phase 1b Study of Sintilimab Plus Anlotinib as First-line Therapy in Patients With Advanced NSCLC.
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J Thorac Oncol, 2021 Feb 02; 16(4). PMID: 33524601
Combination strategies to maximize the benefits of cancer immunotherapy.
Shaoming Zhu, Tian Zhang, +5 authors, Chong-Xian Pan.
J Hematol Oncol, 2021 Sep 29; 14(1). PMID: 34579759    Free PMC article.
MET-Oncogenic and JAK2-Inactivating Alterations Are Independent Factors That Affect Regulation of PD-L1 Expression in Lung Cancer.
Maria Saigi, Juan J Alburquerque-Bejar, +8 authors, Montse Sanchez-Cespedes.
Clin Cancer Res, 2018 Jun 15; 24(18). PMID: 29898990
HDAC Inhibition Upregulates PD-1 Ligands in Melanoma and Augments Immunotherapy with PD-1 Blockade.
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Highly Cited.
Dual PD-L1 and TGF-b blockade in patients with recurrent respiratory papillomatosis.
Yvette Robbins, Jay Friedman, +10 authors, Scott Norberg.
J Immunother Cancer, 2021 Sep 01; 9(8). PMID: 34462327    Free PMC article.
Blocking siglec-10hi tumor-associated macrophages improves anti-tumor immunity and enhances immunotherapy for hepatocellular carcinoma.
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Exp Hematol Oncol, 2021 Jun 12; 10(1). PMID: 34112250    Free PMC article.
Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity.
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The biology of combination immunotherapy in recurrent metastatic head and neck cancer.
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J Thorac Oncol, 2020 Sep 12; 15(12). PMID: 32916308
An Open-label Randomized Phase 2 study of Durvalumab Alone or in Combination with Tremelimumab in Patients with Advanced Germ Cell Tumors (APACHE): Results from the First Planned Interim Analysis.
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Eur Urol, 2018 Sep 24; 75(1). PMID: 30243800
Double-edged roles of protein tyrosine phosphatase SHP2 in cancer and its inhibitors in clinical trials.
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Cell Immunol, 2020 Apr 20; 352. PMID: 32305131
Nivolumab plus ipilimumab versus sunitinib in first-line treatment for advanced renal cell carcinoma: extended follow-up of efficacy and safety results from a randomised, controlled, phase 3 trial.
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Highly Cited.
Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4.
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Combination Immunotherapy with CAR T Cells and Checkpoint Blockade for the Treatment of Solid Tumors.
Rachel Grosser, Leonid Cherkassky, Navin Chintala, Prasad S Adusumilli.
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