Review
. 2021 Jan; 13(2):.
doi: 10.3390/cancers13020309.

IFN-γ and CD38 in Hyperprogressive Cancer Development

Stefania Angelicola 1 Francesca Ruzzi 1 Lorena Landuzzi 2 Laura Scalambra 1 Francesco Gelsomino 3 Andrea Ardizzoni 3 Patrizia Nanni 1 Pier-Luigi Lollini 1 Arianna Palladini 1 
Affiliations
  • PMID: 33467713
  •     224 References
  •     3 citations

Abstract

Immune checkpoint inhibitors (ICIs) improve the survival of patients with multiple types of cancer. However, low response rates and atypical responses limit their success in clinical applications. The paradoxical acceleration of tumor growth after treatment, defined as hyperprogressive disease (HPD), is the most difficult problem facing clinicians and patients alike. The mechanisms that underlie hyperprogression (HP) are still unclear and controversial, although different factors are associated with the phenomenon. In this review, we propose two factors that have not yet been demonstrated to be directly associated with HP, but upon which it is important to focus attention. IFN-γ is a key cytokine in antitumor response and its levels increase during ICI therapy, whereas CD38 is an alternative immune checkpoint that is involved in immunosuppressive responses. As both factors are associated with resistance to ICI therapy, we have discussed their possible involvement in HPD with the conclusion that IFN-γ may contribute to HP onset through the activation of the inflammasome pathway, immunosuppressive enzyme IDO1 and activation-induced cell death (AICD) in effector T cells, while the role of CD38 in HP may be associated with the activation of adenosine receptors, hypoxia pathways and AICD-dependent T-cell depletion.

Keywords: CD38; IFN-γ; cancer; hyperprogression; hyperprogressive disease; immune checkpoint inhibitors; immunotherapy; macrophage; tumor microenvironment.

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Interferon gamma stabilizes the T helper cell type 1 phenotype.
Y Zhang, R Apilado, +5 authors, H Huang.
J Exp Med, 2001 Jul 18; 194(2). PMID: 11457891    Free PMC article.
Hyperprogression under Immune Checkpoint Inhibitor: a potential role for germinal immunogenetics.
Sadal Refae, Jocelyn Gal, +7 authors, Esma Saada-Bouzid.
Sci Rep, 2020 Feb 29; 10(1). PMID: 32107407    Free PMC article.
IL-27 induces the expression of IDO and PD-L1 in human cancer cells.
Grazia Carbotti, Gaia Barisione, +6 authors, Silvano Ferrini.
Oncotarget, 2015 Dec 15; 6(41). PMID: 26657115    Free PMC article.
F-actin dampens NLRP3 inflammasome activity via Flightless-I and LRRFIP2.
Danielle Burger, Céline Fickentscher, Philippe de Moerloose, Karim J Brandt.
Sci Rep, 2016 Jul 20; 6. PMID: 27431477    Free PMC article.
Considerations for successful cancer immunotherapy in aged hosts.
V Hurez, Á S Padrón, R S Svatek, T J Curiel.
Clin Exp Immunol, 2016 Oct 01; 187(1). PMID: 27690272    Free PMC article.
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Beyond EGFR, ALK and ROS1: Current evidence and future perspectives on newly targetable oncogenic drivers in lung adenocarcinoma.
Giuseppe Lamberti, Elisa Andrini, +5 authors, Andrea Ardizzoni.
Crit Rev Oncol Hematol, 2020 Oct 15; 156. PMID: 33053439
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IDO inhibits a tryptophan sufficiency signal that stimulates mTOR: A novel IDO effector pathway targeted by D-1-methyl-tryptophan.
Richard Metz, Sonja Rust, +5 authors, George C Prendergast.
Oncoimmunology, 2012 Dec 25; 1(9). PMID: 23264892    Free PMC article.
Highly Cited.
Predictive factors for hyperprogressive disease during nivolumab as anti-PD1 treatment in patients with advanced gastric cancer.
Akinori Sasaki, Yoshiaki Nakamura, +10 authors, Kohei Shitara.
Gastric Cancer, 2019 Jan 11; 22(4). PMID: 30627987
Highly Cited.
Novel functional germline variants in the VEGF receptor 2 gene and their effect on gene expression and microvessel density in lung cancer.
Dylan M Glubb, Elisa Cerri, +13 authors, Federico Innocenti.
Clin Cancer Res, 2011 Jun 30; 17(16). PMID: 21712447    Free PMC article.
Inhibition of JNK enhances TGF-beta1-activated Smad2 signaling in mouse embryonic lung.
Shu Wu, Kalyani Kasisomayajula, Jinghong Peng, Eduardo Bancalari.
Pediatr Res, 2009 Jan 08; 65(4). PMID: 19127219
Hyperprogressive disease during PD-1/PD-L1 blockade in patients with non-small-cell lung cancer.
C G Kim, K H Kim, +14 authors, H R Kim.
Ann Oncol, 2019 Apr 13; 30(7). PMID: 30977778
Highly Cited.
Genetic association study of NLRP1, CARD, and CASP1 inflammasome genes with chronic Chagas cardiomyopathy among Trypanosoma cruzi seropositive patients in Bolivia.
Steven J Clipman, Josephine Henderson-Frost, +3 authors, Robert H Gilman.
PLoS One, 2018 Feb 14; 13(2). PMID: 29438387    Free PMC article.
Novel clinical and radiomic predictors of rapid disease progression phenotypes among lung cancer patients treated with immunotherapy: An early report.
Ilke Tunali, Jhanelle E Gray, +5 authors, Matthew B Schabath.
Lung Cancer, 2019 Feb 25; 129. PMID: 30797495    Free PMC article.
B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells.
Takeshi Azuma, Sheng Yao, +3 authors, Lieping Chen.
Blood, 2008 Jan 29; 111(7). PMID: 18223165    Free PMC article.
Highly Cited.
Human CD38 and CD16 are functionally dependent and physically associated in natural killer cells.
Silvia Deaglio, Mercedes Zubiaur, +5 authors, Fabio Malavasi.
Blood, 2002 Mar 16; 99(7). PMID: 11895784
In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target.
Robert T Manguso, Hans W Pope, +16 authors, W Nicholas Haining.
Nature, 2017 Jul 21; 547(7664). PMID: 28723893    Free PMC article.
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CD38 ligation induces discrete cytokine mRNA expression in human cultured lymphocytes.
C M Ausiello, F Urbani, +2 authors, F Malavasi.
Eur J Immunol, 1995 May 01; 25(5). PMID: 7774653
IFN-gamma production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo.
Birgit Sawitzki, Cherry I Kingsley, +3 authors, Kathryn J Wood.
J Exp Med, 2005 Jun 22; 201(12). PMID: 15967822    Free PMC article.
The Multi-faceted Ecto-enzyme CD38: Roles in Immunomodulation, Cancer, Aging, and Metabolic Diseases.
Kelly A Hogan, Claudia C S Chini, Eduardo N Chini.
Front Immunol, 2019 Jun 20; 10. PMID: 31214171    Free PMC article.
Highly Cited. Review.
Impaired development of CD4+ CD25+ regulatory T cells in the absence of STAT1: increased susceptibility to autoimmune disease.
Takeaki Nishibori, Yoshinari Tanabe, Leon Su, Michael David.
J Exp Med, 2003 Dec 31; 199(1). PMID: 14699080    Free PMC article.
Blockade of Notch signaling promotes acetaminophen-induced liver injury.
Longfeng Jiang, Michael Ke, +6 authors, Bibo Ke.
Immunol Res, 2017 Mar 14; 65(3). PMID: 28286920    Free PMC article.
Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer.
Hossein Borghaei, Luis Paz-Ares, +25 authors, Julie R Brahmer.
N Engl J Med, 2015 Sep 29; 373(17). PMID: 26412456    Free PMC article.
Highly Cited.
The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells.
Francesca Fallarino, Ursula Grohmann, +10 authors, Paolo Puccetti.
J Immunol, 2006 May 20; 176(11). PMID: 16709834
Highly Cited.
CD38 as a prognostic marker in CLL.
Zoltan Matrai.
Hematology, 2005 Jul 16; 10(1). PMID: 16019444
Review.
Interleukin 21 controls tumour growth and tumour immunosurveillance in colitis-associated tumorigenesis in mice.
Dominik Jauch, Maria Martin, +4 authors, Stefan Fichtner-Feigl.
Gut, 2011 Sep 29; 60(12). PMID: 21948944
Transcriptional Landscape of Human Tissue Lymphocytes Unveils Uniqueness of Tumor-Infiltrating T Regulatory Cells.
Marco De Simone, Alberto Arrigoni, +28 authors, Massimiliano Pagani.
Immunity, 2016 Nov 17; 45(5). PMID: 27851914    Free PMC article.
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IFN-gamma triggered STAT1-PKB/AKT signalling pathway influences the function of alloantigen reactive regulatory T cells.
B Wei, S Baker, J Wieckiewicz, K J Wood.
Am J Transplant, 2009 Nov 06; 10(1). PMID: 19889125    Free PMC article.
Flow cytometric immunophenotypic analysis of 306 cases of multiple myeloma.
Pei Lin, Rebecca Owens, Guido Tricot, Carla S Wilson.
Am J Clin Pathol, 2004 Apr 15; 121(4). PMID: 15080299
Targeting immunosuppressive adenosine in cancer.
Dipti Vijayan, Arabella Young, Michele W L Teng, Mark J Smyth.
Nat Rev Cancer, 2017 Oct 24; 17(12). PMID: 29059149
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Selection, Analysis and Improvement of Anti-Angiogenesis Compounds Identified by an Anti-HIF-1α Screening and Validation System.
Chikezie Madu, Liyuan Li, Yi Lu.
J Cancer, 2016 Nov 24; 7(14). PMID: 27877208    Free PMC article.
Novel patterns of response under immunotherapy.
E Borcoman, Y Kanjanapan, +6 authors, C Le Tourneau.
Ann Oncol, 2019 Jan 19; 30(3). PMID: 30657859
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Human CD38 ligand. A 120-KDA protein predominantly expressed on endothelial cells.
S Deaglio, U Dianzani, +8 authors, F Malavasi.
J Immunol, 1996 Jan 15; 156(2). PMID: 8543826
Hyperprogression during anti-PD-1/PD-L1 therapy in patients with recurrent and/or metastatic head and neck squamous cell carcinoma.
E Saâda-Bouzid, C Defaucheux, +11 authors, C Le Tourneau.
Ann Oncol, 2017 Apr 19; 28(7). PMID: 28419181
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The binding of an anti-PD-1 antibody to FcγRΙ has a profound impact on its biological functions.
Tong Zhang, Xiaomin Song, +20 authors, Kang Li.
Cancer Immunol Immunother, 2018 Apr 25; 67(7). PMID: 29687231    Free PMC article.
Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive cancers.
Y Liu, Y Cheng, +7 authors, C Ma.
Oncogene, 2017 Jul 12; 36(44). PMID: 28692048    Free PMC article.
Highly Cited.
Hyperprogressors after Immunotherapy: Analysis of Genomic Alterations Associated with Accelerated Growth Rate.
Shumei Kato, Aaron Goodman, +3 authors, Razelle Kurzrock.
Clin Cancer Res, 2017 Mar 30; 23(15). PMID: 28351930    Free PMC article.
Highly Cited.
IL10 Release upon PD-1 Blockade Sustains Immunosuppression in Ovarian Cancer.
Purushottam Lamichhane, Lavakumar Karyampudi, +8 authors, Keith L Knutson.
Cancer Res, 2017 Oct 11; 77(23). PMID: 28993412    Free PMC article.
Toll-like receptor 2 ligand and interferon-γ suppress anti-tumor T cell responses by enhancing the immunosuppressive activity of monocytic myeloid-derived suppressor cells.
Hiroaki Shime, Akira Maruyama, +3 authors, Tsukasa Seya.
Oncoimmunology, 2018 Jan 04; 7(1). PMID: 29296526    Free PMC article.
Biomarkers for predicting efficacy of PD-1/PD-L1 inhibitors.
Ming Yi, Dechao Jiao, +4 authors, Kongming Wu.
Mol Cancer, 2018 Aug 25; 17(1). PMID: 30139382    Free PMC article.
Highly Cited. Review.
An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells.
Joshua D Mezrich, John H Fechner, +3 authors, Christopher A Bradfield.
J Immunol, 2010 Aug 20; 185(6). PMID: 20720200    Free PMC article.
Highly Cited.
Tumor Interferon Signaling Regulates a Multigenic Resistance Program to Immune Checkpoint Blockade.
Joseph L Benci, Bihui Xu, +16 authors, Andy J Minn.
Cell, 2016 Dec 03; 167(6). PMID: 27912061    Free PMC article.
Highly Cited.
CARD8 is a negative regulator for NLRP3 inflammasome, but mutant NLRP3 in cryopyrin-associated periodic syndromes escapes the restriction.
Sayaka Ito, Yukichi Hara, Tetsuo Kubota.
Arthritis Res Ther, 2014 Feb 13; 16(1). PMID: 24517500    Free PMC article.
Specific Activation of A3, A2A and A1 Adenosine Receptors in CD73-Knockout Mice Affects B16F10 Melanoma Growth, Neovascularization, Angiogenesis and Macrophage Infiltration.
Patrycja Koszałka, Monika Gołuńska, +5 authors, Jacek Bigda.
PLoS One, 2016 Mar 11; 11(3). PMID: 26964090    Free PMC article.
The Crosstalk between Nrf2 and Inflammasomes.
Paulina Hennig, Martha Garstkiewicz, +3 authors, Hans-Dietmar Beer.
Int J Mol Sci, 2018 Feb 14; 19(2). PMID: 29438305    Free PMC article.
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Myeloid-Derived Suppressor Cells Hinder the Anti-Cancer Activity of Immune Checkpoint Inhibitors.
Rebekka Weber, Viktor Fleming, +5 authors, Viktor Umansky.
Front Immunol, 2018 Jun 27; 9. PMID: 29942309    Free PMC article.
Highly Cited. Review.
Hyperprogressive Disease Is a New Pattern of Progression in Cancer Patients Treated by Anti-PD-1/PD-L1.
Stéphane Champiat, Laurent Dercle, +8 authors, Charles Ferté.
Clin Cancer Res, 2016 Nov 09; 23(8). PMID: 27827313
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IL-35 induces N2 phenotype of neutrophils to promote tumor growth.
Jiu-Ming Zou, Jian Qin, +9 authors, Zuo-Hua Feng.
Oncotarget, 2017 Apr 23; 8(20). PMID: 28432279    Free PMC article.
Tumour ischaemia by interferon-γ resembles physiological blood vessel regression.
Thomas Kammertoens, Christian Friese, +23 authors, Thomas Blankenstein.
Nature, 2017 Apr 27; 545(7652). PMID: 28445461    Free PMC article.
Highly Cited.
Phase 1/2 study of epacadostat in combination with ipilimumab in patients with unresectable or metastatic melanoma.
Geoffrey T Gibney, Omid Hamid, +10 authors, Jeffrey S Weber.
J Immunother Cancer, 2019 Mar 22; 7(1). PMID: 30894212    Free PMC article.
Constitutive IDO1 Expression in Human Tumors Is Driven by Cyclooxygenase-2 and Mediates Intrinsic Immune Resistance.
Marc Hennequart, Luc Pilotte, +4 authors, Benoît Van den Eynde.
Cancer Immunol Res, 2017 Aug 03; 5(8). PMID: 28765120
Highly Cited.
Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis.
Y E Chin, M Kitagawa, +2 authors, X Y Fu.
Mol Cell Biol, 1997 Sep 01; 17(9). PMID: 9271410    Free PMC article.
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A2aR antagonists: Next generation checkpoint blockade for cancer immunotherapy.
Robert D Leone, Ying-Chun Lo, Jonathan D Powell.
Comput Struct Biotechnol J, 2015 May 06; 13. PMID: 25941561    Free PMC article.
Highly Cited. Review.
Glycosylation and stabilization of programmed death ligand-1 suppresses T-cell activity.
Chia-Wei Li, Seung-Oe Lim, +21 authors, Mien-Chie Hung.
Nat Commun, 2016 Aug 31; 7. PMID: 27572267    Free PMC article.
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Targeting Adenosine Receptor Signaling in Cancer Immunotherapy.
Kevin Sek, Christina Mølck, +3 authors, Paul A Beavis.
Int J Mol Sci, 2018 Dec 06; 19(12). PMID: 30513816    Free PMC article.
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Hyperprogressive disease in early-phase immunotherapy trials: Clinical predictors and association with immune-related toxicities.
Yada Kanjanapan, Daphne Day, +16 authors, Philippe L Bedard.
Cancer, 2019 Feb 16; 125(8). PMID: 30768786
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CD38 as a prognostic factor in Chinese patients with chronic lymphocytic leukaemia.
Wei Xu, Jian-Yong Li, +5 authors, Hong-Xia Qiu.
Leuk Res, 2008 Aug 05; 33(2). PMID: 18674817
Chemotherapy regimen based on sorafenib combined with 5-FU on HIF-1α and VEGF expression and survival in advanced gastric cancer patients.
Ronghui Cheng, Hongmei Yong, +3 authors, Xueyi Zhou.
Oncol Lett, 2017 Apr 30; 13(4). PMID: 28454454    Free PMC article.
Hyperprogressive Disease In Cervical Small Cell Carcinoma Treated By Immune Checkpoint Inhibitor.
Zihan Xu, Liying Chen, +6 authors, Jianguo Sun.
Onco Targets Ther, 2019 Dec 06; 12. PMID: 31802899    Free PMC article.
Differential Expression of Immune-Regulatory Genes Associated with PD-L1 Display in Melanoma: Implications for PD-1 Pathway Blockade.
Janis M Taube, Geoffrey D Young, +10 authors, Suzanne L Topalian.
Clin Cancer Res, 2015 May 07; 21(17). PMID: 25944800    Free PMC article.
Highly Cited.
Kynurenine Pathway of Tryptophan Metabolism: Regulatory and Functional Aspects.
Abdulla A-B Badawy.
Int J Tryptophan Res, 2017 May 05; 10. PMID: 28469468    Free PMC article.
Highly Cited. Review.
Baseline Peripheral Blood Biomarkers Associated with Clinical Outcome of Advanced Melanoma Patients Treated with Ipilimumab.
Alexander Martens, Kilian Wistuba-Hamprecht, +21 authors, Benjamin Weide.
Clin Cancer Res, 2016 Jan 21; 22(12). PMID: 26787752    Free PMC article.
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Autocrine functions of VEGF in breast tumor cells: adhesion, survival, migration and invasion.
Martine Perrot-Applanat, Melanie Di Benedetto.
Cell Adh Migr, 2012 Dec 22; 6(6). PMID: 23257828    Free PMC article.
Review.
Review of Indications of FDA-Approved Immune Checkpoint Inhibitors per NCCN Guidelines with the Level of Evidence.
Raju K Vaddepally, Prakash Kharel, +2 authors, Abhinav B Chandra.
Cancers (Basel), 2020 Apr 05; 12(3). PMID: 32245016    Free PMC article.
Review.
Radiation Treatment in Women with Ovarian Cancer: Past, Present, and Future.
Emma C Fields, William P McGuire, Lilie Lin, Sarah M Temkin.
Front Oncol, 2017 Sep 06; 7. PMID: 28871275    Free PMC article.
Review.
Interferon-mediated enhancement of metastasis. Are MHC antigens involved?
P L Lollini, C De Giovanni, +3 authors, P Nanni.
Clin Exp Metastasis, 1987 Oct 01; 5(4). PMID: 3117468
Absence of CD38 delays arrival of neutrophils to the liver and innate immune response development during hepatic amoebiasis by Entamoeba histolytica.
L A Estrada-Figueroa, Y Ramírez-Jiménez, +4 authors, P Talamás-Rohana.
Parasite Immunol, 2011 Sep 17; 33(12). PMID: 21919917
IFN-γ production by allogeneic Foxp3+ regulatory T cells is essential for preventing experimental graft-versus-host disease.
Christian Koenecke, Chun-Wei Lee, +8 authors, Immo Prinz.
J Immunol, 2012 Aug 08; 189(6). PMID: 22869903
Interferon-γ produced by tumor-infiltrating NK cells and CD4+ T cells downregulates TNFSF15 expression in vascular endothelial cells.
Yi Lu, Xin Gu, +8 authors, Lu-Yuan Li.
Angiogenesis, 2013 Oct 22; 17(3). PMID: 24141405
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints.
Shohei Koyama, Esra A Akbay, +23 authors, Peter S Hammerman.
Nat Commun, 2016 Feb 18; 7. PMID: 26883990    Free PMC article.
Highly Cited.
The blockade of immune checkpoints in cancer immunotherapy.
Drew M Pardoll.
Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437870    Free PMC article.
Highly Cited. Review.
Insulin-like growth factor (IGF) signaling in tumorigenesis and the development of cancer drug resistance.
Sahitya K Denduluri, Olumuyiwa Idowu, +8 authors, Hue H Luu.
Genes Dis, 2015 May 20; 2(1). PMID: 25984556    Free PMC article.
Highly Cited.
Interferon Receptor Signaling Pathways Regulating PD-L1 and PD-L2 Expression.
Angel Garcia-Diaz, Daniel Sanghoon Shin, +16 authors, Antoni Ribas.
Cell Rep, 2017 May 13; 19(6). PMID: 28494868    Free PMC article.
Highly Cited.
SAR650984 directly induces multiple myeloma cell death via lysosomal-associated and apoptotic pathways, which is further enhanced by pomalidomide.
H Jiang, C Acharya, +12 authors, K C Anderson.
Leukemia, 2015 Sep 05; 30(2). PMID: 26338273
Hyperprogressive Disease in Anorectal Melanoma Treated by PD-1 Inhibitors.
Marjorie Faure, Philippe Rochigneux, +3 authors, Marine Gilabert.
Front Immunol, 2018 May 05; 9. PMID: 29725330    Free PMC article.
Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4.
Rikke B Holmgaard, Dmitriy Zamarin, +2 authors, James P Allison.
J Exp Med, 2013 Jun 12; 210(7). PMID: 23752227    Free PMC article.
Highly Cited.
CD38-Mediated Immunosuppression as a Mechanism of Tumor Cell Escape from PD-1/PD-L1 Blockade.
Limo Chen, Lixia Diao, +36 authors, Don L Gibbons.
Cancer Discov, 2018 Jul 18; 8(9). PMID: 30012853    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.
Can IDO activity predict primary resistance to anti-PD-1 treatment in NSCLC?
Andrea Botticelli, Bruna Cerbelli, +7 authors, Paolo Marchetti.
J Transl Med, 2018 Aug 08; 16(1). PMID: 30081936    Free PMC article.
CD38 deficiency in the tumor microenvironment attenuates glioma progression and modulates features of tumor-associated microglia/macrophages.
Ayelet Levy, Eran Blacher, +3 authors, Lior Mayo.
Neuro Oncol, 2012 Jun 16; 14(8). PMID: 22700727    Free PMC article.
PD-1+ regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer.
Takahiro Kamada, Yosuke Togashi, +13 authors, Hiroyoshi Nishikawa.
Proc Natl Acad Sci U S A, 2019 Apr 28; 116(20). PMID: 31028147    Free PMC article.
Highly Cited.
Indoleamine 2,3-dioxygenase-1 (IDO1) enhances survival and invasiveness of endometrial stromal cells via the activation of JNK signaling pathway.
Jie Mei, Ming-Qing Li, +4 authors, Xiao-Yong Zhu.
Int J Clin Exp Pathol, 2013 Feb 16; 6(3). PMID: 23411497    Free PMC article.
Epacadostat Plus Pembrolizumab in Patients With Advanced Solid Tumors: Phase I Results From a Multicenter, Open-Label Phase I/II Trial (ECHO-202/KEYNOTE-037).
Tara C Mitchell, Omid Hamid, +11 authors, Thomas F Gajewski.
J Clin Oncol, 2018 Sep 29; 36(32). PMID: 30265610    Free PMC article.
Highly Cited.
Melanoma Cell-Intrinsic PD-1 Receptor Functions Promote Tumor Growth.
Sonja Kleffel, Christian Posch, +19 authors, Tobias Schatton.
Cell, 2015 Sep 12; 162(6). PMID: 26359984    Free PMC article.
Highly Cited.
VEGF targets the tumour cell.
Hira Lal Goel, Arthur M Mercurio.
Nat Rev Cancer, 2013 Nov 23; 13(12). PMID: 24263190    Free PMC article.
Highly Cited. Review.
Paracrine Wnt5a-β-Catenin Signaling Triggers a Metabolic Program that Drives Dendritic Cell Tolerization.
Fei Zhao, Christine Xiao, +9 authors, Brent A Hanks.
Immunity, 2018 Jan 19; 48(1). PMID: 29343435    Free PMC article.
Highly Cited.
CD38 ligation results in activation of the Raf-1/mitogen-activated protein kinase and the CD3-zeta/zeta-associated protein-70 signaling pathways in Jurkat T lymphocytes.
M Zubiaur, M Izquierdo, +2 authors, J Sancho.
J Immunol, 1997 Jul 01; 159(1). PMID: 9200455
Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis.
M I Koukourakis, A Giatromanolaki, +5 authors, Tumour and Angiogenesis Research Group.
Br J Cancer, 2003 Aug 28; 89(5). PMID: 12942121    Free PMC article.
Highly Cited.
Blockade of Tumor-Expressed PD-1 promotes lung cancer growth.
Shisuo Du, Neal McCall, +6 authors, Bo Lu.
Oncoimmunology, 2018 Apr 11; 7(4). PMID: 29632720    Free PMC article.
Gene delivery of indoleamine 2,3-dioxygenase prolongs cardiac allograft survival by shaping the types of T-cell responses.
Guang Yu, Hong Dai, +7 authors, Feili Gong.
J Gene Med, 2008 May 03; 10(7). PMID: 18452241
Hyperprogressive Disease in Patients With Advanced Non-Small Cell Lung Cancer Treated With PD-1/PD-L1 Inhibitors or With Single-Agent Chemotherapy.
Roberto Ferrara, Laura Mezquita, +25 authors, Caroline Caramella.
JAMA Oncol, 2018 Sep 08; 4(11). PMID: 30193240    Free PMC article.
Highly Cited.
Interferon-γ Drives Treg Fragility to Promote Anti-tumor Immunity.
Abigail E Overacre-Delgoffe, Maria Chikina, +15 authors, Dario A A Vignali.
Cell, 2017 May 30; 169(6). PMID: 28552348    Free PMC article.
Highly Cited.
Role of IFN-gamma in induction of Foxp3 and conversion of CD4+ CD25- T cells to CD4+ Tregs.
Zhaojun Wang, Jian Hong, +7 authors, Jingwu Z Zhang.
J Clin Invest, 2006 Aug 15; 116(9). PMID: 16906223    Free PMC article.
Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells.
Stefani Spranger, Robbert M Spaapen, +4 authors, Thomas F Gajewski.
Sci Transl Med, 2013 Aug 30; 5(200). PMID: 23986400    Free PMC article.
Highly Cited.
Interferon-Gamma at the Crossroads of Tumor Immune Surveillance or Evasion.
Flávia Castro, Ana Patrícia Cardoso, +2 authors, Maria José Oliveira.
Front Immunol, 2018 May 22; 9. PMID: 29780381    Free PMC article.
Highly Cited. Review.
Angiopoietin-2 mRNA expression is increased in chronic lymphocytic leukemia patients with poor prognostic features.
F Vrbacky, L Smolej, +6 authors, J Maly.
Hematology, 2010 Jul 31; 15(4). PMID: 20670479
Regulation of the JNK pathway by TGF-beta activated kinase 1 in rheumatoid arthritis synoviocytes.
Deepa R Hammaker, David L Boyle, Tomoyuki Inoue, Gary S Firestein.
Arthritis Res Ther, 2007 Jun 15; 9(3). PMID: 17559674    Free PMC article.
Activation-induced cell death in T cells and autoimmunity.
Jian Zhang, Xuemei Xu, Yong Liu.
Cell Mol Immunol, 2005 Oct 13; 1(3). PMID: 16219166
Review.
Simultaneous Foxp3 and IDO expression is associated with sentinel lymph node metastases in breast cancer.
Aaron S Mansfield, Paivi S Heikkila, +3 authors, Marjut H K Leidenius.
BMC Cancer, 2009 Jul 17; 9. PMID: 19604349    Free PMC article.
Ischemia Is Related to Tumour Genetics in Uveal Melanoma.
Niels J Brouwer, Annemijn P A Wierenga, +7 authors, Martine J Jager.
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IFN-gamma induction of p21(WAF1) is required for cell cycle inhibition and suppression of apoptosis.
A C Hobeika, W Etienne, +2 authors, P S Subramaniam.
J Interferon Cytokine Res, 2000 Jan 19; 19(12). PMID: 10638704
Neuropilin 1 deficiency on CD4+Foxp3+ regulatory T cells impairs mouse melanoma growth.
Wiebke Hansen, Marina Hutzler, +10 authors, Iris Helfrich.
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Highly Cited.
Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors.
Esra A Akbay, Shohei Koyama, +24 authors, Kwok-Kin Wong.
Cancer Discov, 2013 Oct 01; 3(12). PMID: 24078774    Free PMC article.
Highly Cited.
Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab.
Christiane Meyer, Laurène Cagnon, +6 authors, Daniel E Speiser.
Cancer Immunol Immunother, 2013 Dec 21; 63(3). PMID: 24357148
Highly Cited.
Mutations Associated with Acquired Resistance to PD-1 Blockade in Melanoma.
Jesse M Zaretsky, Angel Garcia-Diaz, +26 authors, Antoni Ribas.
N Engl J Med, 2016 Jul 20; 375(9). PMID: 27433843    Free PMC article.
Highly Cited.
Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8(+) T cells directly within the tumor microenvironment.
Stefani Spranger, Holly K Koblish, +3 authors, Thomas F Gajewski.
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Immunogenomic Landscape Contributes to Hyperprogressive Disease after Anti-PD-1 Immunotherapy for Cancer.
Donghai Xiong, Yian Wang, +3 authors, Ming You.
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Compensatory upregulation of PD-1, LAG-3, and CTLA-4 limits the efficacy of single-agent checkpoint blockade in metastatic ovarian cancer.
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IFN regulatory factor 8 regulates MDM2 in germinal center B cells.
Jeff X Zhou, Chang Hoon Lee, +4 authors, Herbert C Morse.
J Immunol, 2009 Aug 04; 183(5). PMID: 19648273    Free PMC article.
Daratumumab depletes CD38+ immune regulatory cells, promotes T-cell expansion, and skews T-cell repertoire in multiple myeloma.
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Detailed analysis of adenosine A2a receptor (ADORA2A) and CD73 (5'-nucleotidase, ecto, NT5E) methylation and gene expression in head and neck squamous cell carcinoma patients.
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PDL1 Signals through Conserved Sequence Motifs to Overcome Interferon-Mediated Cytotoxicity.
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CD38 triggers cytotoxic responses in activated human natural killer cells.
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Blockade of adenosine A2A receptor enhances CD8+ T cells response and decreases regulatory T cells in head and neck squamous cell carcinoma.
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Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase.
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Chronic lymphocytic leukemia cells express CD38 in response to Th1 cell-derived IFN-γ by a T-bet-dependent mechanism.
Simone Bürgler, Aleix Gimeno, +7 authors, Ludvig A Munthe.
J Immunol, 2014 Dec 17; 194(2). PMID: 25505279
Clonal Deletion of Tumor-Specific T Cells by Interferon-γ Confers Therapeutic Resistance to Combination Immune Checkpoint Blockade.
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The Next-Generation of Combination Cancer Immunotherapy: Epigenetic Immunomodulators Transmogrify Immune Training to Enhance Immunotherapy.
Reza Bayat Mokhtari, Manpreet Sambi, +7 authors, Myron R Szewczuk.
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Hyperprogression of a mismatch repair-deficient colon cancer in a humanized mouse model following administration of immune checkpoint inhibitor pembrolizumab.
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Profiling Tumor Immune Microenvironment of Non-Small Cell Lung Cancer Using Multiplex Immunofluorescence.
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