. 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 
  • PMID: 33467713
  •     224 References
  •     3 citations


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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Gastric Cancer, 2019 Jan 11; 22(4). PMID: 30627987
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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.
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Pediatr Res, 2009 Jan 08; 65(4). PMID: 19127219
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Ann Oncol, 2019 Apr 13; 30(7). PMID: 30977778
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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.
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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
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C M Ausiello, F Urbani, +2 authors, F Malavasi.
Eur J Immunol, 1995 May 01; 25(5). PMID: 7774653
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The Multi-faceted Ecto-enzyme CD38: Roles in Immunomodulation, Cancer, Aging, and Metabolic Diseases.
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Front Immunol, 2019 Jun 20; 10. PMID: 31214171    Free PMC article.
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Takeaki Nishibori, Yoshinari Tanabe, Leon Su, Michael David.
J Exp Med, 2003 Dec 31; 199(1). PMID: 14699080    Free PMC article.
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J Immunol, 2006 May 20; 176(11). PMID: 16709834
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CD38 as a prognostic marker in CLL.
Zoltan Matrai.
Hematology, 2005 Jul 16; 10(1). PMID: 16019444
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Transcriptional Landscape of Human Tissue Lymphocytes Unveils Uniqueness of Tumor-Infiltrating T Regulatory Cells.
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Immunity, 2016 Nov 17; 45(5). PMID: 27851914    Free PMC article.
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B Wei, S Baker, J Wieckiewicz, K J Wood.
Am J Transplant, 2009 Nov 06; 10(1). PMID: 19889125    Free PMC article.
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Chikezie Madu, Liyuan Li, Yi Lu.
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S Deaglio, U Dianzani, +8 authors, F Malavasi.
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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.
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Oncogene, 2017 Jul 12; 36(44). PMID: 28692048    Free PMC article.
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Shumei Kato, Aaron Goodman, +3 authors, Razelle Kurzrock.
Clin Cancer Res, 2017 Mar 30; 23(15). PMID: 28351930    Free PMC article.
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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.
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Oncoimmunology, 2018 Jan 04; 7(1). PMID: 29296526    Free PMC article.
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Joseph L Benci, Bihui Xu, +16 authors, Andy J Minn.
Cell, 2016 Dec 03; 167(6). PMID: 27912061    Free PMC article.
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Sayaka Ito, Yukichi Hara, Tetsuo Kubota.
Arthritis Res Ther, 2014 Feb 13; 16(1). PMID: 24517500    Free PMC article.
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Hyperprogressive Disease Is a New Pattern of Progression in Cancer Patients Treated by Anti-PD-1/PD-L1.
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Constitutive IDO1 Expression in Human Tumors Is Driven by Cyclooxygenase-2 and Mediates Intrinsic Immune Resistance.
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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
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Hyperprogressive Disease In Cervical Small Cell Carcinoma Treated By Immune Checkpoint Inhibitor.
Zihan Xu, Liying Chen, +6 authors, Jianguo Sun.
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Baseline Peripheral Blood Biomarkers Associated with Clinical Outcome of Advanced Melanoma Patients Treated with Ipilimumab.
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Cell Adh Migr, 2012 Dec 22; 6(6). PMID: 23257828    Free PMC article.
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Parasite Immunol, 2011 Sep 17; 33(12). PMID: 21919917
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J Immunol, 2012 Aug 08; 189(6). PMID: 22869903
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Drew M Pardoll.
Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437870    Free PMC article.
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Cell Rep, 2017 May 13; 19(6). PMID: 28494868    Free PMC article.
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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.
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Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer.
Julie Brahmer, Karen L Reckamp, +22 authors, David R Spigel.
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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.
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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.
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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.
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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).
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Cell, 2015 Sep 12; 162(6). PMID: 26359984    Free PMC article.
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Highly Cited. Review.
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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.
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