Journal Article
. 2016 Jun; 15(12):2719-32.
doi: 10.1016/j.celrep.2016.05.058.

CD40 Stimulation Obviates Innate Sensors and Drives T Cell Immunity in Cancer

Katelyn T Byrne 1 Robert H Vonderheide 2 
Affiliations
  • PMID: 27292635
  •     72 References
  •     100 citations

Abstract

Cancer immunotherapies are more effective in tumors with robust T cell infiltrates, but mechanisms to convert T cell-devoid tumors with active immunosuppression to those capable of recruiting T cells remain incompletely understood. Here, using genetically engineered mouse models of pancreatic ductal adenocarcinoma (PDA), we demonstrate that a single dose of agonistic CD40 antibody with chemotherapy rendered PDA susceptible to T cell-dependent destruction and potentiated durable remissions. CD40 stimulation caused a clonal expansion of T cells in the tumor, but the addition of chemotherapy optimized myeloid activation and T cell function. Although recent data highlight the requirement for innate sensors in cancer immunity, these canonical pathways-including TLRs, inflammasome, and type I interferon/STING-played no role in mediating the efficacy of CD40 and chemotherapy. Thus, CD40 functions as a non-redundant mechanism to convert the tumor microenvironment immunologically. Our data provide a rationale for a newly initiated clinical trial of CD40 and chemotherapy in PDA.

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Highly Cited.
Cellular determinants and therapeutic implications of inflammation in pancreatic cancer.
Meredith L Stone, Gregory L Beatty.
Pharmacol Ther, 2019 Jun 04; 201. PMID: 31158393    Free PMC article.
Review.
In situ vaccination with defined factors overcomes T cell exhaustion in distant tumors.
Danny N Khalil, Nathan Suek, +18 authors, Taha Merghoub.
J Clin Invest, 2019 Jul 23; 129(8). PMID: 31329159    Free PMC article.
Concepts for agonistic targeting of CD40 in immuno-oncology.
David M Richards, Julian P Sefrin, +2 authors, Christian Merz.
Hum Vaccin Immunother, 2019 Aug 14; 16(2). PMID: 31403344    Free PMC article.
Review.
Differential Effects of Depleting versus Programming Tumor-Associated Macrophages on Engineered T Cells in Pancreatic Ductal Adenocarcinoma.
Ingunn M Stromnes, Adam L Burrack, +8 authors, Sunil R Hingorani.
Cancer Immunol Res, 2019 Apr 28; 7(6). PMID: 31028033    Free PMC article.
Recent insights into the biology of pancreatic cancer.
Wantong Yao, Anirban Maitra, Haoqiang Ying.
EBioMedicine, 2020 Mar 07; 53. PMID: 32139179    Free PMC article.
Review.
Modulating inflammation for cancer therapy.
Birgit Ritter, Florian R Greten.
J Exp Med, 2019 Apr 27; 216(6). PMID: 31023715    Free PMC article.
Highly Cited. Review.
Beyond cDC1: Emerging Roles of DC Crosstalk in Cancer Immunity.
Rajkumar Noubade, Sonia Majri-Morrison, Kristin V Tarbell.
Front Immunol, 2019 May 31; 10. PMID: 31143179    Free PMC article.
Review.
Sufficiency of CD40 activation and immune checkpoint blockade for T cell priming and tumor immunity.
Alexander H Morrison, Mark S Diamond, +2 authors, Robert H Vonderheide.
Proc Natl Acad Sci U S A, 2020 Mar 28; 117(14). PMID: 32213589    Free PMC article.
Tumor Cell-Intrinsic USP22 Suppresses Antitumor Immunity in Pancreatic Cancer.
Jinyang Li, Salina Yuan, +4 authors, Ben Z Stanger.
Cancer Immunol Res, 2019 Dec 25; 8(3). PMID: 31871120    Free PMC article.
Dendritic Cell Paucity Leads to Dysfunctional Immune Surveillance in Pancreatic Cancer.
Samarth Hegde, Varintra E Krisnawan, +16 authors, David G DeNardo.
Cancer Cell, 2020 Mar 19; 37(3). PMID: 32183949    Free PMC article.
Proimmunogenic impact of MEK inhibition synergizes with agonist anti-CD40 immunostimulatory antibodies in tumor therapy.
Daniel Baumann, Tanja Hägele, +12 authors, Rienk Offringa.
Nat Commun, 2020 May 03; 11(1). PMID: 32358491    Free PMC article.
CCL5 mediates CD40-driven CD4+ T cell tumor infiltration and immunity.
Austin P Huffman, Jeffrey H Lin, +2 authors, Robert H Vonderheide.
JCI Insight, 2020 Apr 24; 5(10). PMID: 32324594    Free PMC article.
Tumor cell-intrinsic EPHA2 suppresses anti-tumor immunity by regulating PTGS2 (COX-2).
Nune Markosyan, Jinyang Li, +13 authors, Robert H Vonderheide.
J Clin Invest, 2019 Jun 05; 129(9). PMID: 31162144    Free PMC article.
Antiangiogenic immunotherapy suppresses desmoplastic and chemoresistant intestinal tumors in mice.
Simone Ragusa, Borja Prat-Luri, +17 authors, Tatiana V Petrova.
J Clin Invest, 2020 Feb 06; 130(3). PMID: 32015230    Free PMC article.
The impact of immunotherapy on the survival of pancreatic adenocarcinoma patients who received definitive surgery of the pancreatic tumor: a retrospective analysis of the National Cancer Database.
Saber Amin, Michael Baine, +2 authors, Chi Lin.
Radiat Oncol, 2020 Jun 05; 15(1). PMID: 32493354    Free PMC article.
The impact of neoadjuvant and adjuvant immunotherapy on the survival of pancreatic cancer patients: a retrospective analysis.
Saber Amin, Michael Baine, Jane Meza, Chi Lin.
BMC Cancer, 2020 Jun 11; 20(1). PMID: 32517661    Free PMC article.
The impact of immunotherapy on the survival of pancreatic adenocarcinoma patients who do not receive definitive surgery of the tumor.
Saber Amin, Michael Baine, +2 authors, Chi Lin.
Clin Transl Radiat Oncol, 2020 Jul 03; 24. PMID: 32613090    Free PMC article.
Macrophages as regulators of tumour immunity and immunotherapy.
David G DeNardo, Brian Ruffell.
Nat Rev Immunol, 2019 Feb 06; 19(6). PMID: 30718830    Free PMC article.
Highly Cited. Review.
Regulatory T cells in tumor microenvironment: new mechanisms, potential therapeutic strategies and future prospects.
Chunxiao Li, Ping Jiang, +2 authors, Junjie Wang.
Mol Cancer, 2020 Jul 19; 19(1). PMID: 32680511    Free PMC article.
Review.
The interplay between innate and adaptive immunity in cancer shapes the productivity of cancer immunosurveillance.
Renee B Chang, Gregory L Beatty.
J Leukoc Biol, 2020 Apr 10; 108(1). PMID: 32272502    Free PMC article.
Review.
Tumor Cell-Intrinsic Factors Underlie Heterogeneity of Immune Cell Infiltration and Response to Immunotherapy.
Jinyang Li, Katelyn T Byrne, +26 authors, Ben Z Stanger.
Immunity, 2018 Jul 01; 49(1). PMID: 29958801    Free PMC article.
Highly Cited.
Type 1 conventional dendritic cells are systemically dysregulated early in pancreatic carcinogenesis.
Jeffrey H Lin, Austin P Huffman, +6 authors, Robert H Vonderheide.
J Exp Med, 2020 May 27; 217(8). PMID: 32453421    Free PMC article.
Novel combination immunotherapy for pancreatic cancer: potent anti-tumor effects with CD40 agonist and interleukin-15 treatment.
Jonas Rm Van Audenaerde, Elly Marcq, +13 authors, Evelien Ljm Smits.
Clin Transl Immunology, 2020 Aug 22; 9(8). PMID: 32821382    Free PMC article.
T-Cell Immunity in Pancreatic Cancer.
Reham Ajina, Louis M Weiner.
Pancreas, 2020 Aug 25; 49(8). PMID: 32833941    Free PMC article.
Review.
Combination immunotherapy and radiation therapy strategies for pancreatic cancer-targeting multiple steps in the cancer immunity cycle.
Snehal Gajiwala, Anna Torgeson, +2 authors, Shane Lloyd.
J Gastrointest Oncol, 2019 Jan 04; 9(6). PMID: 30603120    Free PMC article.
Review.
Inflammation, Biomarkers and Immuno-Oncology Pathways in Pancreatic Cancer.
Belinda Lee, Peter Gibbs.
J Pers Med, 2019 May 01; 9(2). PMID: 31035449    Free PMC article.
The Association of the Sequence of Immunotherapy With the Survival of Unresectable Pancreatic Adenocarcinoma Patients: A Retrospective Analysis of the National Cancer Database.
Saber Amin, Michael J Baine, Jane L Meza, Chi Lin.
Front Oncol, 2020 Sep 29; 10. PMID: 32983998    Free PMC article.
The Achilles' Heel of Pancreatic Cancer: Targeting pancreatic cancer's unique immunologic characteristics and metabolic dependencies in clinical trials.
Despina Siolas, Christy Morrissey, Paul Eliezer Oberstein.
J Pancreatol, 2020 Nov 03; 3(3). PMID: 33133736    Free PMC article.
Targeting Multiple Receptors to Increase Checkpoint Blockade Efficacy.
David J Zahavi, Louis M Weiner.
Int J Mol Sci, 2019 Jan 10; 20(1). PMID: 30621125    Free PMC article.
Review.
Tumor-Derived Myeloid Cell Chemoattractants and T Cell Exclusion in Pancreatic Cancer.
Robert H Vonderheide, Adham S Bear.
Front Immunol, 2020 Dec 12; 11. PMID: 33304355    Free PMC article.
Review.
Challenges and Opportunities for Pancreatic Cancer Immunotherapy.
Adham S Bear, Robert H Vonderheide, Mark H O'Hara.
Cancer Cell, 2020 Sep 19; 38(6). PMID: 32946773    Free PMC article.
Review.
Immune modulation resulting from MR-guided high intensity focused ultrasound in a model of murine breast cancer.
Brett Z Fite, James Wang, +16 authors, Katherine W Ferrara.
Sci Rep, 2021 Jan 15; 11(1). PMID: 33441763    Free PMC article.
The Functional Crosstalk between Myeloid-Derived Suppressor Cells and Regulatory T Cells within the Immunosuppressive Tumor Microenvironment.
Maximilian Haist, Henner Stege, Stephan Grabbe, Matthias Bros.
Cancers (Basel), 2021 Jan 13; 13(2). PMID: 33430105    Free PMC article.
Review.
CXCL13 shapes immunoactive tumor microenvironment and enhances the efficacy of PD-1 checkpoint blockade in high-grade serous ovarian cancer.
Moran Yang, Jiaqi Lu, +5 authors, Haiou Liu.
J Immunother Cancer, 2021 Jan 17; 9(1). PMID: 33452206    Free PMC article.
Tumor Burden and Immunotherapy: Impact on Immune Infiltration and Therapeutic Outcomes.
Samuel I Kim, Christopher R Cassella, Katelyn T Byrne.
Front Immunol, 2021 Feb 19; 11. PMID: 33597954    Free PMC article.
Review.
Targeting Innate Immunity in Cancer Therapy.
Srikrishnan Rameshbabu, Brian W Labadie, Anna Argulian, Akash Patnaik.
Vaccines (Basel), 2021 Feb 13; 9(2). PMID: 33572196    Free PMC article.
Review.
Epigenetic and Transcriptional Control of the Epidermal Growth Factor Receptor Regulates the Tumor Immune Microenvironment in Pancreatic Cancer.
Jinyang Li, Salina Yuan, +11 authors, Ben Z Stanger.
Cancer Discov, 2020 Nov 08; 11(3). PMID: 33158848    Free PMC article.
The role of tumor heterogeneity in immune-tumor interactions.
Shelby M Knoche, Alaina C Larson, +2 authors, Joyce C Solheim.
Cancer Metastasis Rev, 2021 Mar 09; 40(2). PMID: 33682030    Free PMC article.
Review.
Agonistic CD40 Antibodies in Cancer Treatment.
Dijana Djureinovic, Meina Wang, Harriet M Kluger.
Cancers (Basel), 2021 Apr 04; 13(6). PMID: 33804039    Free PMC article.
Review.
Systemic inflammation is a determinant of outcomes of CD40 agonist-based therapy in pancreatic cancer patients.
Max M Wattenberg, Veronica M Herrera, +3 authors, Gregory L Beatty.
JCI Insight, 2021 Jan 27; 6(5). PMID: 33497362    Free PMC article.
Therapeutic potential of interleukin-15 in cancer (Review).
Gheorghita Isvoranu, Mihaela Surcel, +4 authors, Marioara Chiritoiu-Butnaru.
Exp Ther Med, 2021 May 15; 22(1). PMID: 33986840    Free PMC article.
Review.
Sequential Treatment of Bioresponsive Nanoparticles Elicits Antiangiogenesis and Apoptosis and Synergizes with a CD40 Agonist for Antitumor Immunity.
Xiang Ling, Xiaomin Jiang, +4 authors, Wenbin Lin.
ACS Nano, 2020 Dec 22; 15(1). PMID: 33347262    Free PMC article.
C4b-binding protein α-chain enhances antitumor immunity by facilitating the accumulation of tumor-infiltrating lymphocytes in the tumor microenvironment in pancreatic cancer.
Kosuke Sasaki, Shigetsugu Takano, +6 authors, Masayuki Ohtsuka.
J Exp Clin Cancer Res, 2021 Jun 26; 40(1). PMID: 34167573    Free PMC article.
Epithelial cell transforming 2 is regulated by Yes-associated protein 1 and mediates pancreatic cancer progression and metastasis.
Ce Li, Zhenzi Peng, +8 authors, Qiang Wang.
Am J Physiol Gastrointest Liver Physiol, 2021 Jan 28; 320(3). PMID: 33501895    Free PMC article.
Tumor-Associated Macrophages in Pancreatic Ductal Adenocarcinoma: Therapeutic Opportunities and Clinical Challenges.
Ashleigh R Poh, Matthias Ernst.
Cancers (Basel), 2021 Jul 03; 13(12). PMID: 34201127    Free PMC article.
Review.
Ovarian Cancer Immunotherapy and Personalized Medicine.
Susan Morand, Monika Devanaboyina, +2 authors, John Nemunaitis.
Int J Mol Sci, 2021 Jul 03; 22(12). PMID: 34207103    Free PMC article.
Review.
Agonistic CD40 therapy induces tertiary lymphoid structures but impairs responses to checkpoint blockade in glioma.
Luuk van Hooren, Alessandra Vaccaro, +16 authors, Anna Dimberg.
Nat Commun, 2021 Jul 07; 12(1). PMID: 34226552    Free PMC article.
Type 1 conventional dendritic cells and interferons are required for spontaneous CD4+ and CD8+ T-cell protective responses to breast cancer.
Raphaël Mattiuz, Carine Brousse, +9 authors, Karine Crozat.
Clin Transl Immunology, 2021 Jul 20; 10(7). PMID: 34277006    Free PMC article.
CD40 stimulation as a molecular adjuvant for cancer vaccines and other immunotherapies.
Timothy N J Bullock.
Cell Mol Immunol, 2021 Jul 21; 19(1). PMID: 34282297    Free PMC article.
Review.
Dendritic cell targeting with Fc-enhanced CD40 antibody agonists induces durable antitumor immunity in humanized mouse models of bladder cancer.
Christopher S Garris, Jeffrey L Wong, Jeffrey V Ravetch, David A Knorr.
Sci Transl Med, 2021 May 21; 13(594). PMID: 34011627    Free PMC article.
TNF blockade uncouples toxicity from antitumor efficacy induced with CD40 chemoimmunotherapy.
Meredith L Stone, Jesse Lee, +11 authors, Gregory L Beatty.
JCI Insight, 2021 Jun 09; 6(14). PMID: 34101617    Free PMC article.
Pre-clinical evaluation of immunoPET imaging using agonist CD40 monoclonal antibody in pancreatic tumor-bearing mice.
Sadaf Aghevlian, Bo Wu, +4 authors, Katherine W Ferrara.
Nucl Med Biol, 2021 May 08; 98-99. PMID: 33962357    Free PMC article.
Tumour-intrinsic resistance to immune checkpoint blockade.
Anusha Kalbasi, Antoni Ribas.
Nat Rev Immunol, 2019 Oct 02; 20(1). PMID: 31570880    Free PMC article.
Highly Cited. Review.
The CD155/TIGIT axis promotes and maintains immune evasion in neoantigen-expressing pancreatic cancer.
William A Freed-Pastor, Laurens J Lambert, +21 authors, Tyler Jacks.
Cancer Cell, 2021 Aug 07; 39(10). PMID: 34358448    Free PMC article.
Low neoantigen expression and poor T-cell priming underlie early immune escape in colorectal cancer.
Peter M K Westcott, Nathan J Sacks, +13 authors, Tyler Jacks.
Nat Cancer, 2021 Nov 06; 2(10). PMID: 34738089    Free PMC article.
Radiation combines with immune checkpoint blockade to enhance T cell priming in a murine model of poorly immunogenic pancreatic cancer.
Courtney T Stump, Kevin Roehle, Nataly Manjarrez Orduno, Stephanie K Dougan.
Open Biol, 2021 Nov 18; 11(11). PMID: 34784792    Free PMC article.
Immunotherapy in Pancreatic Adenocarcinoma: Beyond "Copy/Paste".
Robert Hester, Pawel K Mazur, Florencia McAllister.
Clin Cancer Res, 2021 Jul 02; 27(23). PMID: 34193514    Free PMC article.
Review.
Brief exposure of skin to near-infrared laser augments early vaccine responses.
Shinya Yokomizo, Wataru Katagiri, +8 authors, Satoshi Kashiwagi.
Nanophotonics, 2021 Dec 07; 10(12). PMID: 34868804    Free PMC article.
Neoadjuvant Selicrelumab, an Agonist CD40 Antibody, Induces Changes in the Tumor Microenvironment in Patients with Resectable Pancreatic Cancer.
Katelyn T Byrne, Courtney B Betts, +26 authors, Robert H Vonderheide.
Clin Cancer Res, 2021 Jun 12; 27(16). PMID: 34112709    Free PMC article.
Site-Dependent Immune Escape Due to Impaired Dendritic Cell Cross-Priming.
Mark S Diamond, Jeffrey H Lin, Robert H Vonderheide.
Cancer Immunol Res, 2021 Jun 20; 9(8). PMID: 34145076    Free PMC article.
Gain-of-function p53R172H mutation drives accumulation of neutrophils in pancreatic tumors, promoting resistance to immunotherapy.
Despina Siolas, Emily Vucic, +2 authors, Dafna Bar-Sagi.
Cell Rep, 2021 Aug 26; 36(8). PMID: 34433022    Free PMC article.
Approaches of the Innate Immune System to Ameliorate Adaptive Immunotherapy for B-Cell Non-Hodgkin Lymphoma in Their Microenvironment.
Takashi Watanabe.
Cancers (Basel), 2022 Jan 12; 14(1). PMID: 35008305    Free PMC article.
Review.
LncRNA PCGEM1 in Human Cancers: Functions, Mechanisms and Promising Clinical Utility.
Yuanshuai Su, Xinyu Gu, +3 authors, Lanjuan Li.
Front Oncol, 2022 Mar 11; 12. PMID: 35265529    Free PMC article.
Review.
Immunotherapy in Combination with Well-Established Treatment Strategies in Pancreatic Cancer: Current Insights.
Christo Kole, Nikolaos Charalampakis, +3 authors, Dimitrios Schizas.
Cancer Manag Res, 2022 Mar 19; 14. PMID: 35300059    Free PMC article.
Review.
Translational advances in pancreatic ductal adenocarcinoma therapy.
Abdel Nasser Hosein, Stephanie K Dougan, Andrew J Aguirre, Anirban Maitra.
Nat Cancer, 2022 Mar 31; 3(3). PMID: 35352061
Review.
Distinct myeloid antigen-presenting cells dictate differential fates of tumor-specific CD8+ T cells in pancreatic cancer.
Adam L Burrack, Zoe C Schmiechen, +8 authors, Ingunn M Stromnes.
JCI Insight, 2022 Apr 09; 7(7). PMID: 35393950    Free PMC article.
A review of mechanisms of resistance to immune checkpoint inhibitors and potential strategies for therapy.
Yu Fujiwara, Arjun Mittra, Abdul Rafeh Naqash, Naoko Takebe.
Cancer Drug Resist, 2020 Jun 18; 3(3). PMID: 35582437    Free PMC article.
Review.
The dark side of immunotherapy: pancreatic cancer.
Gianluca Mucciolo, Cecilia Roux, +3 authors, Paola Cappello.
Cancer Drug Resist, 2020 May 11; 3(3). PMID: 35582441    Free PMC article.
Review.
Sotigalimab and/or nivolumab with chemotherapy in first-line metastatic pancreatic cancer: clinical and immunologic analyses from the randomized phase 2 PRINCE trial.
Lacey J Padrón, Deena M Maurer, +34 authors, Robert H Vonderheide.
Nat Med, 2022 Jun 07;. PMID: 35662283