Impact of l-arginine metabolism on immune response and anticancer immunotherapy

Frontiers in Oncology

Volumn 8, Issue MAR, 2018, Pages

  Kim, Sun Hee ^a   Roszik, Jason ^a   Grimm, Elizabeth A ^a   Ekmekcioglu, Suhendan ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Arginase 1; Arginine; Cyclooxygenase 2; Immune response; Immunotherapy; Metabolism; Microsomal prostaglandin E synthase 1; NO synthase

Indexed keywords

EID: 85044376103     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2018.00067     Document Type: Short Survey

References (33)

1. Ekmekcioglu S, Davies MA, Tanese K, Roszik J, Shin-Sim M, Bassett RL Jr, et al. Inflammatory marker testing identifies CD74 expression in melanoma tumor cells, and its expression associates with favorable survival for stage III melanoma. Clin Cancer Res (2016) 22:3016-24. doi:10.1158/1078-0432.CCR-15-2226
2. Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell (2010) 140:771-6. doi:10.1016/j.cell.2010.03.006
3. Reuben A, Spencer CN, Prieto PA, Gopalakrishnan V, Reddy SM, Miller JP, et al. Genomic and immune heterogeneity are associated with differential responses to therapy in melanoma. NPJ Genom Med (2017) 2:10. doi:10.1038/s41525-017-0013-8
4. Veglia F, Gabrilovich DI. Dendritic cells in cancer: the role revisited. Curr Opin Immunol (2017) 45:43-51. doi:10.1016/j.coi.2017.01.002
5. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature (2008) 454:436-44. doi:10.1038/nature07205
6. Popolo A, Adesso S, Pinto A, Autore G, Marzocco S. l-arginine and its metabolites in kidney and cardiovascular disease. Amino Acids (2014) 46:2271-86. doi:10.1007/s00726-014-1825-9
7. Hatzoglou M, Fernandez J, Yaman I, Closs E, Regulation of cationic amino acid transport: the story of the CAT-1 transporter. Annu Rev Nutr (2004) 24:377-99. doi:10.1146/annurev.nutr.23.011702.073120
8. Simmons WW, Closs EI, Cunningham JM, Smith TW, Kelly RA. Cytokines and insulin induce cationic amino acid transporter (CAT) expression in cardiac myocytes. Regulation of l-arginine transport and no production by CAT-1, CAT-2A, and CAT-2B. J Biol Chem (1996) 271:11694-702. doi:10.1074/jbc.271.20.11694
9. Forstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J (2012) 33:829-37. doi:10.1093/eurheartj/ehr304
10. Wang Y, Hu S, Gabisi AM Jr, Er JA, Pope A, Burstein G, et al. Developing an irreversible inhibitor of human DDAH-1, an enzyme upregulated in melanoma. ChemMedChem (2014) 9:792-7. doi:10.1002/cmdc.201300557
11. Yoon JK, Frankel AE, Feun LG, Ekmekcioglu S, Kim KB. Arginine deprivation therapy for malignant melanoma. Clin Pharmacol (2013) 5:11-9. doi:10.2147/CPAA.S37350
12. Geiger R, Rieckmann JC, Wolf T, Basso C, Feng Y, Fuhrer T, et al. l-arginine modulates T cell metabolism and enhances survival and anti-tumor activity. Cell (2016) 167:829-842e813. doi:10.1016/j.cell.2016.09.031
13. Fletcher M, Ramirez ME, Sierra RA, Raber P, Thevenot P, Al-Khami AA, et al. l-Arginine depletion blunts antitumor T-cell responses by inducing myeloid-derived suppressor cells. Cancer Res (2015) 75:275-83. doi:10.1158/0008-5472.CAN-14-1491
14. Norian LA, Rodriguez PC, O'Mara LA, Zabaleta J, Ochoa AC, Cella M, et al. Tumor-infiltrating regulatory dendritic cells inhibit CD8+ T cell function via l-arginine metabolism. Cancer Res (2009) 69:3086-94. doi:10.1158/0008-5472.CAN-08-2826
15. Habib S, Ali A. Biochemistry of nitric oxide. Indian J Clin Biochem (2011) 26:3-17. doi:10.1007/s12291-011-0108-4
16. Kovacs I, Lindermayr C. Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Front Plant Sci (2013) 4:137. doi:10.3389/fpls.2013.00137
17. Yakovlev VA, Mikkelsen RB. Protein tyrosine nitration in cellular signal transduction pathways. J Recept Signal Transduct Res (2010) 30:420-9. doi:10.3109/10799893.2010.513991
18. Ekmekcioglu S, Ellerhorst JA, Prieto VG, Johnson MM, Broemeling LD, Grimm EA. Tumor iNOS predicts poor survival for stage III melanoma patients. Int J Cancer (2006) 119:861-6. doi:10.1002/ijc.21767
19. Johansson CC, Egyhazi S, Masucci G, Harlin H, Mougiakakos D, Poschke I, et al. Prognostic significance of tumor iNOS and COX-2 in stage III malignant cutaneous melanoma. Cancer Immunol Immunother (2009) 58:1085-94. doi:10.1007/s00262-008-0631-1
20. Grimm EA, Sikora AG, Ekmekcioglu S. Molecular pathways: inflammation-associated nitric-oxide production as a cancer-supporting redox mechanism and a potential therapeutic target. Clin Cancer Res (2013) 19:5557-63. doi:10.1158/1078-0432.CCR-12-1554
21. Heinecke JL, Ridnour LA, Cheng RY, Switzer CH, Lizardo MM, Khanna C, et al. Tumor microenvironment-based feed-forward regulation of NOS2 in breast cancer progression. Proc Natl Acad Sci U S A (2014) 111:6323-8. doi:10.1073/pnas.1401799111
22. Tanese K, Grimm EA, Ekmekcioglu S. The role of melanoma tumor-derived nitric oxide in the tumor inflammatory microenvironment: its impact on the chemokine expression profile, including suppression of CXCL10. Int J Cancer (2012) 131:891-901. doi:10.1002/ijc.26451
23. Ekmekcioglu S, Grimm EA, Roszik J. Targeting iNOS to increase efficacy of immunotherapies. Hum Vaccin Immunother (2017) 13:1105-8. doi:10.1080/21645515.2016.1276682
24. Hugo W, Zaretsky JM, Sun L, Song C, Moreno BH, Hu-Lieskovan S, et al. Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma. Cell (2016) 165:35-44. doi:10.1016/j.cell.2016.02.065
25. Tham M, Tan KW, Keeble J, Wang X, Hubert S, Barron L, et al. Melanoma-initiating cells exploit M2 macrophage TGFbeta and arginase pathway for survival and proliferation. Oncotarget (2014) 5:12027-42. doi:10.18632/oncotarget.2482
26. Lind DS. Arginine and cancer. J Nutr (2004) 134:2837S-41S. doi:10.1093/jn/134.10.2837S
27. Feun L, You M, Wu CJ, Kuo MT, Wangpaichitr M, Spector S, et al. Arginine deprivation as a targeted therapy for cancer. Curr Pharm Des (2008) 14:1049-57. doi:10.2174/138161208784246199
28. Rodriguez PC, Quiceno DG, Ochoa AC. l-arginine availability regulates T-lymphocyte cell-cycle progression. Blood (2007) 109:1568-73. doi:10.1182/blood-2006-06-031856
29. Lamas B, Vergnaud-Gauduchon J, Goncalves-Mendes N, Perche O, Rossary A, Vasson MP, et al. Altered functions of natural killer cells in response to l-arginine availability. Cell Immunol (2012) 280:182-90. doi:10.1016/j.cellimm.2012.11.018
30. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol (2009) 9:162-74. doi:10.1038/nri2506
31. Tang CH, Grimm EA. Depletion of endogenous nitric oxide enhances cisplatin-induced apoptosis in a p53-dependent manner in melanoma cell lines. J Biol Chem (2004) 279:288-98. doi:10.1074/jbc. M310821200
32. Visigalli R, Bussolati O, Sala R, Barilli A, Rotoli BM, Parolari A, et al. The stimulation of arginine transport by TNFalpha in human endothelial cells depends on NF-kappaB activation. Biochim Biophys Acta (2004) 1664:45-52. doi:10.1016/j.bbamem.2004.04.001
33. Prima V, Kaliberova LN, Kaliberov S, Curiel DT, Kusmartsev S. COX2/mPGES1/PGE2 pathway regulates PD-L1 expression in tumor-associated macrophages and myeloid-derived suppressor cells. Proc Natl Acad Sci U S A (2017) 114:1117-22. doi:10.1073/pnas.1612920114