Regulation of the Immune Checkpoint Indoleamine 2,3-Dioxygenase Expression by Epstein-Barr Virus

Overview

Journal Biomolecules

Publisher MDPI

Specialties Biochemistry
Molecular Biology

Date 2021 Dec 24

PMID 34944437

Citations 4

Authors

Leila Sawada

Antonio Carlos Rosario Vallinoto

Igor Brasil-Costa

Affiliations

Soon will be listed here.

Abstract

Epstein-Barr virus (EBV) is an oncovirus ubiquitously distributed and associated with different types of cancer. The reason why only a group of infected people develop cancer is still unknown. EBV-associated cancers represent about 1.8% of all cancer deaths worldwide, with more than 150,000 new cases of cancer being reported annually. Since EBV-associated cancers are described as more aggressive and more resistant to the usual treatment compared to EBV-negative ones, the recent introduction of monoclonal antibodies (mAbs) targeting immune checkpoints (ICs) in the treatment of cancer patients represents a possible therapy for EBV-associated diseases. However, the current mAb therapies available still need improvement, since a group of patients do not respond well to treatment. Therefore, the main objective of this review is to summarize the progress made regarding the contribution of EBV infection to the expression of the IC indoleamine 2,3-dioxygenase (IDO) thus far. This IC has the potential to be used as a target in new immune therapies, such as mAbs. We hope that this work helps the development of future immunotherapies, improving the prognosis of EBV-associated cancer patients.

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References

Khan G, Hashim M . Global burden of deaths from Epstein-Barr virus attributable malignancies 1990-2010. Infect Agent Cancer. 2014; 9(1):38. PMC: 4253616. DOI: 10.1186/1750-9378-9-38. View

Choe J, Yun J, Jeon Y, Kim S, Park G, Huh J . Indoleamine 2,3-dioxygenase (IDO) is frequently expressed in stromal cells of Hodgkin lymphoma and is associated with adverse clinical features: a retrospective cohort study. BMC Cancer. 2014; 14:335. PMC: 4026588. DOI: 10.1186/1471-2407-14-335. View

Ben-Haj-Ayed A, Moussa A, Ghedira R, Gabbouj S, Miled S, Bouzid N . Prognostic value of indoleamine 2,3-dioxygenase activity and expression in nasopharyngeal carcinoma. Immunol Lett. 2015; 169:23-32. DOI: 10.1016/j.imlet.2015.11.012. View

Munz C, Moormann A . Immune escape by Epstein-Barr virus associated malignancies. Semin Cancer Biol. 2008; 18(6):381-7. PMC: 2615476. DOI: 10.1016/j.semcancer.2008.10.002. View

Renaud S, Lefebvre A, Mordon S, Morales O, Delhem N . Novel Therapies Boosting T Cell Immunity in Epstein Barr Virus-Associated Nasopharyngeal Carcinoma. Int J Mol Sci. 2020; 21(12). PMC: 7352617. DOI: 10.3390/ijms21124292. View

Okamoto A, Nikaido T, Ochiai K, Takakura S, Saito M, Aoki Y . Indoleamine 2,3-dioxygenase serves as a marker of poor prognosis in gene expression profiles of serous ovarian cancer cells. Clin Cancer Res. 2005; 11(16):6030-9. DOI: 10.1158/1078-0432.CCR-04-2671. View

Gonin J, Larousserie F, Bastard C, Picquenot J, Couturier J, Radford-Weiss I . Epstein-Barr virus-induced gene 3 (EBI3): a novel diagnosis marker in Burkitt lymphoma and diffuse large B-cell lymphoma. PLoS One. 2011; 6(9):e24617. PMC: 3169615. DOI: 10.1371/journal.pone.0024617. View

Liu H, Shen Z, Wang Z, Wang X, Zhang H, Qin J . Increased expression of IDO associates with poor postoperative clinical outcome of patients with gastric adenocarcinoma. Sci Rep. 2016; 6:21319. PMC: 4758033. DOI: 10.1038/srep21319. View

Badawy A . Tryptophan metabolism in alcoholism. Nutr Res Rev. 2008; 15(1):123-52. DOI: 10.1079/NRR200133. View

10.

Nicolae A, Pittaluga S, Abdullah S, Steinberg S, Pham T, Davies-Hill T . EBV-positive large B-cell lymphomas in young patients: a nodal lymphoma with evidence for a tolerogenic immune environment. Blood. 2015; 126(7):863-72. PMC: 4536540. DOI: 10.1182/blood-2015-02-630632. View

11.

Fabian K, Padget M, Fujii R, Schlom J, Hodge J . Differential combination immunotherapy requirements for inflamed (warm) tumors versus T cell excluded (cool) tumors: engage, expand, enable, and evolve. J Immunother Cancer. 2021; 9(2). PMC: 7896589. DOI: 10.1136/jitc-2020-001691. View

12.

Ghoneim H, Fan Y, Moustaki A, Abdelsamed H, Dash P, Dogra P . De Novo Epigenetic Programs Inhibit PD-1 Blockade-Mediated T Cell Rejuvenation. Cell. 2017; 170(1):142-157.e19. PMC: 5568784. DOI: 10.1016/j.cell.2017.06.007. View

13.

Billadeau D, Upshaw J, Schoon R, Dick C, Leibson P . NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol. 2003; 4(6):557-64. DOI: 10.1038/ni929. View

14.

Zhang H, Li Y, Wang H, Zhang A, Chen M, Fang Z . Ephrin receptor A2 is an epithelial cell receptor for Epstein-Barr virus entry. Nat Microbiol. 2018; 3(2):1-8. DOI: 10.1038/s41564-017-0080-8. View

15.

Triplett T, Garrison K, Marshall N, Donkor M, Blazeck J, Lamb C . Reversal of indoleamine 2,3-dioxygenase-mediated cancer immune suppression by systemic kynurenine depletion with a therapeutic enzyme. Nat Biotechnol. 2018; 36(8):758-764. PMC: 6078800. DOI: 10.1038/nbt.4180. View

16.

Matsuura H, Kirschner A, Longnecker R, Jardetzky T . Crystal structure of the Epstein-Barr virus (EBV) glycoprotein H/glycoprotein L (gH/gL) complex. Proc Natl Acad Sci U S A. 2010; 107(52):22641-6. PMC: 3012493. DOI: 10.1073/pnas.1011806108. View

17.

Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, Falorni A . CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol. 2002; 3(11):1097-101. DOI: 10.1038/ni846. View

18.

Ball H, Sanchez-Perez A, Weiser S, Austin C, Astelbauer F, Miu J . Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene. 2007; 396(1):203-13. DOI: 10.1016/j.gene.2007.04.010. View

19.

Munn D, Sharma M, Baban B, Harding H, Zhang Y, Ron D . GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity. 2005; 22(5):633-42. DOI: 10.1016/j.immuni.2005.03.013. View

20.

Pessoa Rodrigues C, Ferreira A, Pinho M, de Moraes C, Bergami-Santos P, Barbuto J . Tolerogenic IDO(+) Dendritic Cells Are Induced by PD-1-Expressing Mast Cells. Front Immunol. 2016; 7:9. PMC: 4724729. DOI: 10.3389/fimmu.2016.00009. View