References
- Vijayan D, Young A, Teng MW, Smyth MJ. Targeting immunosuppressive adenosine in cancer. Nat Rev Cancer. 2017;17:709. doi:https://doi.org/10.1038/nrc.2017.86.
- Zimmermann H, Zebisch M, Sträter N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal. 2012;8:437–16.
- Vaupel P, Multhoff G. Commentary: a metabolic immune checkpoint: adenosine in tumor microenvironment. Front Immunol. 2016;7:332. doi:https://doi.org/10.3389/fimmu.2016.00332.
- Takenaka MC, Robson S, Quintana FJ. Regulation of the T cell response by CD39. Trends Immunol. 2016;37:427–39. doi:https://doi.org/10.1016/j.it.2016.04.009.
- Bours M, Swennen E, Di Virgilio F, Cronstein B, Dagnelie P. Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther. 2006;112:358–404. doi:https://doi.org/10.1016/j.pharmthera.2005.04.013.
- Jacob F, Novo CP, Bachert C, Van Crombruggen K. Purinergic signaling in inflammatory cells: P2 receptor expression, functional effects, and modulation of inflammatory responses. Purinergic Signal. 2013;9:285–306.
- Di Virgilio F, Sarti AC, Falzoni S, De Marchi E, Adinolfi E. Extracellular ATP and P2 purinergic signalling in the tumour microenvironment. Nat Rev Cancer. 2018;18:601–18.
- Yegutkin GG. Enzymes involved in metabolism of extracellular nucleotides and nucleosides: functional implications and measurement of activities. Crit Rev Biochem Mol Biol. 2014;49:473–97.
- Deterre P, Gelman L, Gary-Gouy H, Arrieumerlou C, Berthelier V, Tixier J-M, Ktorza S, Goding J, Schmitt C, Bismuth G. Coordinated regulation in human T cells of nucleotide-hydrolyzing ecto-enzymatic activities, including CD38 and PC-1. Possible role in the recycling of nicotinamide adenine dinucleotide metabolites. J Immunol. 1996;157:1381–88.
- Jackson EK, Ren J, Mi Z. Extracellular 2′, 3′-cAMP is a source of adenosine. J Biol Chem. 2009;284:33097–106. doi:https://doi.org/10.1074/jbc.M109.053876.
- Di Virgilio F, Adinolfi E. Extracellular purines, purinergic receptors and tumor growth. Oncogene. 2017;36:293–303. doi:https://doi.org/10.1038/onc.2016.206.
- Zebisch M, Krauss M, Schäfer P, Sträter N. Crystallographic evidence for a domain motion in rat nucleoside triphosphate diphosphohydrolase (NTPDase) 1. J Mol Biol. 2012;415:288–306. doi:https://doi.org/10.1016/j.jmb.2011.10.050.
- Koziak K, Sévigny J, Robson SC, Siegel JB, Kaczmarek E. Analysis of CD39/ATP diphosphohydrolase (ATPDase) expression in endothelial cells, platelets and leukocytes. Thromb Haemost. 1999;82:1538–44. doi:https://doi.org/10.1055/s-0037-1614868.
- Duhen T, Duhen R, Montler R, Moses J, Moudgil T, de Miranda NF, Goodall CP, Blair TC, Fox BA, McDermott JE, et al. Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors. Nat Commun. 2018;9:1–13. doi:https://doi.org/10.1038/s41467-018-05072-0.
- Gupta PK, Godec J, Wolski D, Adland E, Yates K, Pauken KE, Cosgrove C, Ledderose C, Junger WG, Robson SC, et al. CD39 expression identifies terminally exhausted CD8+ T cells. PLoS Pathog. 2015;11:e1005177. doi:https://doi.org/10.1371/journal.ppat.1005177.
- Whiteside TL. The role of regulatory T cells in cancer immunology. ImmunoTargets Therapy. 2015;4:159. doi:https://doi.org/10.2147/ITT.S55415.
- Li X-Y, Moesta AK, Xiao C, Nakamura K, Casey M, Zhang H, Madore J, Lepletier A, Aguilera AR, Sundarrajan A, et al. Targeting CD39 in cancer reveals an extracellular ATP-and inflammasome-driven tumor immunity. Cancer Discov. 2019;9:1754–73. doi:https://doi.org/10.1158/2159-8290.CD-19-0541.
- Allard B, Longhi MS, Robson SC, Stagg J. The ectonucleotidases CD 39 and CD 73: novel checkpoint inhibitor targets. Immunol Rev. 2017;276:121–44.
- Boison D, Yegutkin GG. Adenosine metabolism: emerging concepts for cancer therapy. Cancer Cell. 2019;36:582–96. doi:https://doi.org/10.1016/j.ccell.2019.10.007.
- Allard D, Allard B, Stagg J. On the mechanism of anti-CD39 immune checkpoint therapy. J ImmunoTher Cancer. 2020;8:e000186. doi:https://doi.org/10.1136/jitc-2019-000186.
- Robson SC, Sévigny J, Zimmermann H. The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal. 2006;2:409.
- Fausther M, Lecka J, Kukulski F, Lévesque SA, Pelletier J, Zimmermann H, Dranoff JA, Sévigny J. Cloning, purification, and identification of the liver canalicular ecto-ATPase as NTPDase8. Am J Physiol Gastrointest Liver Physiol. 2007;292:G785–G95. doi:https://doi.org/10.1152/ajpgi.00293.2006.
- Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol. 2011;187:676–83. doi:https://doi.org/10.4049/jimmunol.1003884.
- Levesque S, Lavoie ÉG, Lecka J, Bigonnesse F, Sévigny J. Specificity of the ecto‐ATPase inhibitor ARL 67156 on human and mouse ectonucleotidases. Br J Pharmacol. 2007;152:141–50. doi:https://doi.org/10.1038/sj.bjp.0707361.
- Munkonda MN, Pelletier J, Ivanenkov VV, Fausther M, Tremblay A, Künzli B, Kirley TL, Sévigny J. Characterization of a monoclonal antibody as the first specific inhibitor of human NTP diphosphohydrolase‐3: partial characterization of the inhibitory epitope and potential applications. Febs J. 2009;276:479–96. doi:https://doi.org/10.1111/j.1742-4658.2008.06797.x.
- Goueli SA, Hsiao K, Beavis PA. Monitoring and characterizing soluble and membrane-bound ectonucleotidases CD73 and CD39. PloS One. 2019;14:e0220094. doi:https://doi.org/10.1371/journal.pone.0220094.
- Iqbal J, Shah SJA. Molecular dynamic simulations reveal structural insights into substrate and inhibitor binding modes and functionality of ecto-nucleoside triphosphate diphosphohydrolases. Sci Rep. 2018;8:1–11. doi:https://doi.org/10.1038/s41598-018-20971-4.
- Kumar M, Lowery R, Kumar V. High-throughput screening assays for cancer immunotherapy targets: ectonucleotidases CD39 and CD73. SLAS DISCOVERY: Advanc Sci Drug Discovery. 2020;25:320–26.
- Lee S-Y, Fiene A, Li W, Hanck T, Brylev KA, Fedorov VE, Lecka J, Haider A, Pietzsch H-J, Zimmermann H, et al. Polyoxometalates—potent and selective ecto-nucleotidase inhibitors. Biochem Pharmacol. 2015;93:171–81. doi:https://doi.org/10.1016/j.bcp.2014.11.002.
- Levy G. Mechanism‐based pharmacodynamic modeling. Clin Pharmacol Ther. 1994;56:356–58. doi:https://doi.org/10.1038/clpt.1994.149.
- Robinson PK. Enzymes: principles and biotechnological applications. Essays Biochem. 2015;59:1–41. doi:https://doi.org/10.1042/bse0590001.
- Geoghegan JC, Diedrich G, Lu X, Rosenthal K, Sachsenmeier KF, Wu H, Dall’Acqua WF, Damschroder MM. Inhibition of CD73 AMP hydrolysis by a therapeutic antibody with a dual, non-competitive mechanism of action. MAbs. 2016;8:454–67. doi:https://doi.org/10.1080/19420862.2016.1143182.
- Allard D, Chrobak P, Allard B, Messaoudi N, Stagg J. Targeting the CD73-adenosine axis in immuno-oncology. Immunol Lett. 2019;205:31–39. doi:https://doi.org/10.1016/j.imlet.2018.05.001.
- Leone RD, Emens LA. Targeting adenosine for cancer immunotherapy. J ImmunoTher Cancer. 2018;6:57.
- Fong L, Hotson A, Powderly JD, Sznol M, Heist RS, Choueiri TK, George S, Hughes BGM, Hellmann MD, Shepard DR, et al. Adenosine 2A receptor blockade as an immunotherapy for treatment-refractory renal cell cancer. Cancer Discov. 2020;10:40–53. doi:https://doi.org/10.1158/2159-8290.CD-19-0980.
- Perrot I, Michaud H-A, Giraudon-Paoli M, Augier S, Docquier A, Gros L, Courtois R, Déjou C, Jecko D, Becquart O, et al. Blocking antibodies targeting the CD39/CD73 immunosuppressive pathway unleash immune responses in combination cancer therapies. Cell Rep. 2019;27:2411–25. e9. doi:https://doi.org/10.1016/j.celrep.2019.04.091.
- Holland P Targeting the adeonsine axis to treat cancer. Brisbane Immunotherapy Conference; Brisbane, Australia; 2019.
- Yan J, Li X-Y, Aguilera AR, Xiao C, Jacoberger-Foisac C, Nowlan B, Robson SC, Beers C, Moesta AK, Geetha N, et al. Control of metastases via myeloid CD39 and NK cell effector function. Cancer Immunol Res. 2020;8:356–67. doi:https://doi.org/10.1158/2326-6066.CIR-19-0749.
- Zimmermann H. Extracellular metabolism of ATP and other nucleotides. Naunyn-Schmiedeberg’s arch pharmacol. 2000;362:299–309. doi:https://doi.org/10.1007/s002100000309.
- Zebisch M, Krauss M, Schäfer P, Lauble P, Sträter N. Crystallographic snapshots along the reaction pathway of nucleoside triphosphate diphosphohydrolases. Structure. 2013;21:1460–75. doi:https://doi.org/10.1016/j.str.2013.05.016.
- Copeland RA. Enzymes: a practical introduction to structure, mechanism, and data analysis. New York (NY): John Wiley & Sons; 2004.
- Tam SH, McCarthy SG, Armstrong AA, Somani S, Wu S-J, Liu X, Gervais A, Ernst R, Saro D, Decker R. Functional, biophysical, and structural characterization of human IgG1 and IgG4 Fc variants with ablated immune functionality. Antibodies. 2017;6:12.
- Losenkova K, Paul M, Irjala H, Jalkanen S, Yegutkin GG. Histochemical approach for simultaneous detection of ectonucleotidase and alkaline phosphatase activities in tissues. In: Purinergic signaling. New York (NY): Springer; 2020. p. 107–16.
- Müller CE, Iqbal J, Baqi Y, Zimmermann H, Röllich A, Stephan H. Polyoxometalates—a new class of potent ecto-nucleoside triphosphate diphosphohydrolase (NTPDase) inhibitors. Bioorg Med Chem Lett. 2006;16:5943–47.
- Köhler D, Eckle T, Faigle M, Grenz A, Mittelbronn M, Laucher S, Hart ML, Robson SC, Müller CE, Eltzschig HK, et al. CD39/Ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation. 2007;116:1784–94. doi:https://doi.org/10.1161/CIRCULATIONAHA.107.690180.
- Drosopoulos JH, Broekman MJ, Islam N, Maliszewski CR, Gayle RB, Marcus AJ. Site-directed mutagenesis of human endothelial cell ecto-ADPase/soluble CD39: requirement of glutamate 174 and serine 218 for enzyme activity and inhibition of platelet recruitment. Biochemistry. 2000;39:6936–43. doi:https://doi.org/10.1021/bi992581e.
- Nath N, Godat B, Zimprich C, Dwight SJ, Corona C, McDougall M, Urh M. Homogeneous plate based antibody internalization assay using pH sensor fluorescent dye. J Immunol Methods. 2016;431:11–21. doi:https://doi.org/10.1016/j.jim.2016.02.001.
- Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L, Séror C, Métivier D, Perfettini J-L, Zitvogel L, et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle. 2009;8:3723–28. doi:https://doi.org/10.4161/cc.8.22.10026.
- Estrella V, Chen T, Lloyd M, Wojtkowiak J, Cornnell HH, Ibrahim-Hashim A, Bailey K, Balagurunathan Y, Rothberg JM, Sloane BF, et al. Acidity generated by the tumor microenvironment drives local invasion. Cancer Res. 2013;73:1524–35. doi:https://doi.org/10.1158/0008-5472.CAN-12-2796.
- Appleby TC, Greenstein AE, Hung M, Liclican A, Velasquez M, Villaseñor AG, Wang R, Wong MH, Liu X, Papalia GA, et al. Biochemical characterization and structure determination of a potent, selective antibody inhibitor of human MMP9. J Biol Chem. 2017;292:6810–20. doi:https://doi.org/10.1074/jbc.M116.760579.
- Rodriguez HM, Vaysberg M, Mikels A, McCauley S, Velayo AC, Garcia C, Smith V. Modulation of lysyl oxidase-like 2 enzymatic activity by an allosteric antibody inhibitor. J Biol Chem. 2010;285:20964–74. doi:https://doi.org/10.1074/jbc.M109.094136.
- Deckert J, Wetzel MC, Bartle LM, Skaletskaya A, Goldmacher VS, Vallee F, Zhou-Liu Q, Ferrari P, Pouzieux S, Lahoute C, et al. SAR650984, a novel humanized CD38-targeting antibody, demonstrates potent antitumor activity in models of multiple myeloma and other CD38+ hematologic malignancies. Clin Cancer Res. 2014;20:4574–83. doi:https://doi.org/10.1158/1078-0432.CCR-14-0695.
- van de Donk NW, Janmaat ML, Mutis T, Lammerts van Bueren JJ, Ahmadi T, Sasser AK, Lokhorst HM, Parren PW. Monoclonal antibodies targeting CD38 in hematological malignancies and beyond. Immunol Rev. 2016;270:95–112. doi:https://doi.org/10.1111/imr.12389.
- Hay CM, Sult E, Huang Q, Mulgrew K, Fuhrmann SR, McGlinchey KA, Hammond SA, Rothstein R, Rios-Doria J, Poon E, et al. Targeting CD73 in the tumor microenvironment with MEDI9447. Oncoimmunology. 2016;5:e1208875. doi:https://doi.org/10.1080/2162402X.2016.1208875.
- Lerner AG, Kovalenko M, Welch M, Cruz T, Jones J, Wong C, Spatola B, Eberhardt M, Wong A, Fung W, et al. Abstract 5012: targeting CD39 with a first-in-class inhibitory antibody prevents ATP processing and increases T-cell activation. Cancer Res. 2019;79:5012.
- Zebisch M, Baqi Y, Schäfer P, Müller CE, Sträter N. Crystal structure of NTPDase2 in complex with the sulfoanthraquinone inhibitor PSB-071. J Struct Biol. 2014;185:336–41. doi:https://doi.org/10.1016/j.jsb.2014.01.005.
- Zebisch M, Strater N Structural insight into signal conversion and inactivation by NTPDase2 in purinergic signaling. Proceedings of the National Academy of Sciences of the United States of America 2008; 105:6882–87.
- Knapp K, Zebisch M, Pippel J, El-Tayeb A, Muller CE, Strater N. Crystal structure of the human ecto-5ʹ-nucleotidase (CD73): insights into the regulation of purinergic signaling. Structure. 2012;20:2161–73. doi:https://doi.org/10.1016/j.str.2012.10.001.
- Rahimova R, Fontanel S, Lionne C, Jordheim LP, Peyrottes S, Chaloin L. Identification of allosteric inhibitors of the ecto-5ʹ-nucleotidase (CD73) targeting the dimer interface. PLoS Comput Biol. 2018;14:e1005943. doi:https://doi.org/10.1371/journal.pcbi.1005943.
- Grinthal A, Guidotti G. Dynamic motions of CD39 transmembrane domains regulate and are regulated by the enzymatic active site. Biochemistry. 2004;43:13849–58. doi:https://doi.org/10.1021/bi048644x.
- Grinthal A, Guidotti G. CD39, NTPDase 1, is attached to the plasma membrane by two transmembrane domains. Why? Purinergic Signal. 2006;2:391–98. doi:https://doi.org/10.1007/s11302-005-5907-8.
- Ivanenkov VV, Crawford PA, Toyama A, Sevigny J, Kirley TL. Epitope mapping in cell surface proteins by site-directed masking: defining the structural elements of NTPDase3 inhibition by a monoclonal antibody. Protein Eng Des Sel. 2010;23:579–88. doi:https://doi.org/10.1093/protein/gzq027.
- Losenkova K, Zuccarini M, Helenius M, Jacquemet G, Gerasimovskaya E, Tallgren C, Jalkanen S, Yegutkin GG. Endothelial cells cope with hypoxia-induced depletion of ATP via activation of cellular purine turnover and phosphotransfer networks. Biochimica Et Biophysica Acta (BBA) Mol Basis Dis. 2018;1864:1804–15. doi:https://doi.org/10.1016/j.bbadis.2018.03.001.
- Liang X, Potter J, Kumar S, Zou Y, Quintanilla R, Sridharan M, Carte J, Chen W, Roark N, Ranganathan S, et al. Rapid and highly efficient mammalian cell engineering via Cas9 protein transfection. J Biotechnol. 2015;208:44–53. doi:https://doi.org/10.1016/j.jbiotec.2015.04.024.
- Pannu KK, Joe ET, Iyer SB. Performance evaluation of QuantiBRITE phycoerythrin beads. Cytometry: J Int Soc Anal Cytol. 2001;45:250–58.
- Gai SA, Wittrup KD. Yeast surface display for protein engineering and characterization. Curr Opin Struct Biol. 2007;17:467–73. doi:https://doi.org/10.1016/j.sbi.2007.08.012.
- Xu Y, Roach W, Sun T, Jain T, Prinz B, Yu T-Y, Torrey J, Thomas J, Bobrowicz P, Vasquez M, et al. Addressing polyspecificity of antibodies selected from an in vitro yeast presentation system: a FACS-based, high-throughput selection and analytical tool. Protein Eng Des Sel. 2013;26:663–70. doi:https://doi.org/10.1093/protein/gzt047.
- Estep P, Reid F, Nauman C, Liu Y, Sun T, Sun J, Xu Y. High throughput solution-based measurement of antibody-antigen affinity and epitope binning; MAbs: Taylor & Francis:2013. 270–78.
- Abdiche YN, Miles A, Eckman J, Foletti D, Van Blarcom TJ, Yeung YA, Pons J, Rajpal A. High-throughput epitope binning assays on label-free array-based biosensors can yield exquisite epitope discrimination that facilitates the selection of monoclonal antibodies with functional activity. PLoS One. 2014;9:e92451. doi:https://doi.org/10.1371/journal.pone.0092451.
- Xie L, Mark Jones R, Glass TR, Navoa R, Wang Y, Grace MJ. Measurement of the functional affinity constant of a monoclonal antibody for cell surface receptors using kinetic exclusion fluorescence immunoassay. J Immunol Methods. 2005;304:1–14. doi:https://doi.org/10.1016/j.jim.2005.04.009.
- Yegutkin GG, Henttinen T, Jalkanen S. Extracellular ATP formation on vascular endothelial cells is mediated by ecto-nucleotide kinase activities via phosphotransfer reactions. Faseb J. 2001;15:251–60. doi:https://doi.org/10.1096/fj.00-0268com.