Inhibition of CD73 AMP hydrolysis by a therapeutic antibody with a dual, non-competitive mechanism of action

References

• Zimmermann H. 5′-nucleotidase: Molecular structure and functional aspects. Biochem J 1992; 285 (Pt 2):345–65; PMID:1637327; http://dx.doi.org/10.1042/bj2850345
   PubMed Web of Science ®Google Scholar
• Sullivan JM, Alpers JB. In vitro regulation of rat heart 5′-nucleotidase by adenine nucleotides and magnesium. J Biol Chem 1971; 246:3057–63; PMID:4324346
   PubMed Web of Science ®Google Scholar
• Kumar V. Adenosine as an endogenous immunoregulator in cancer pathogenesis: Where to go? Purinergic Signal 2013; 9:145–65; PMID:23271562; http://dx.doi.org/10.1007/s11302-012-9349-9
   PubMed Web of Science ®Google Scholar
• Spychala J. Tumor-promoting functions of adenosine. Pharmacol Ther 2000; 87:161–73; PMID:11007998; http://dx.doi.org/10.1016/S0163-7258(00)00053-X
   PubMed Web of Science ®Google Scholar
• Xu S, Shao QQ, Sun JT, Yang N, Xie Q, Wang DH, Huang QB, Huang B, Wang XY, Li XG, et al. Synergy between the ectoenzymes CD39 and CD73 contributes to adenosinergic immunosuppression in human malignant gliomas. Neuro Oncol 2013; 15:1160–72; PMID:23737488; http://dx.doi.org/10.1093/neuonc/not067
   PubMed Web of Science ®Google Scholar
• Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, Chen JF, Enjyoji K, Linden J, Oukka M, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204:1257–65; PMID:17502665; http://dx.doi.org/10.1084/jem.20062512
   PubMed Web of Science ®Google Scholar
• Huang S, Apasov S, Koshiba M, Sitkovsky M. Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood 1997; 90:1600–10; PMID:9269779
   PubMed Web of Science ®Google Scholar
• Eppell BA, Newell AM, Brown EJ. Adenosine receptors are expressed during differentiation of monocytes to macrophages in vitro. implications for regulation of phagocytosis. J Immunol 1989; 143:4141–5; PMID:2556476
   PubMed Web of Science ®Google Scholar
• Leibovich SJ, Chen JF, Pinhal-Enfield G, Belem PC, Elson G, Rosania A, Ramanathan M, Montesinos C, Jacobson M, Schwarzschild MA, et al. Synergistic up-regulation of vascular endothelial growth factor expression in murine macrophages by adenosine A(2A) receptor agonists and endotoxin. Am J Pathol 2002; 160:2231–44; PMID:12057925; http://dx.doi.org/10.1016/S0002-9440(10)61170-4
   PubMed Web of Science ®Google Scholar
• Ramanathan M, Pinhal-Enfield G, Hao I, Leibovich SJ. Synergistic up-regulation of vascular endothelial growth factor (VEGF) expression in macrophages by adenosine A2A receptor agonists and endotoxin involves transcriptional regulation via the hypoxia response element in the VEGF promoter. Mol Biol Cell 2007; 18:14–23; PMID:17065555; http://dx.doi.org/10.1091/mbc.E06-07-0596
   PubMed Web of Science ®Google Scholar
• Novitskiy SV, Ryzhov S, Zaynagetdinov R, Goldstein AE, Huang Y, Tikhomirov OY, Blackburn MR, Biaggioni I, Carbone DP, Feoktistov I, et al. Adenosine receptors in regulation of dendritic cell differentiation and function. Blood 2008; 112:1822–31; PMID:18559975; http://dx.doi.org/10.1182/blood-2008-02-136325
   PubMed Web of Science ®Google Scholar
• Beavis PA, Stagg J, Darcy PK, Smyth MJ. CD73: A potent suppressor of antitumor immune responses. Trends Immunol 2012; 33:231–7; PMID:22487321; http://dx.doi.org/10.1016/j.it.2012.02.009
   PubMed Web of Science ®Google Scholar
• Blay J, White TD, Hoskin DW. The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res 1997; 57:2602–5; PMID:9205063
   PubMed Web of Science ®Google Scholar
• Stagg J, Beavis PA, Divisekera U, Liu MC, Moller A, Darcy PK, Smyth MJ. CD73-deficient mice are resistant to carcinogenesis. Cancer Res 2012; 72:2190–6; PMID:22396496; http://dx.doi.org/10.1158/0008-5472.CAN-12-0420
   PubMed Web of Science ®Google Scholar
• Zhi X, Chen S, Zhou P, Shao Z, Wang L, Ou Z, Yin L. RNA interference of ecto-5′-nucleotidase (CD73) inhibits human breast cancer cell growth and invasion. Clin Exp Metastasis 2007; 24:439–48; PMID:17587186; http://dx.doi.org/10.1007/s10585-007-9081-y
   PubMed Web of Science ®Google Scholar
• Zhi X, Wang Y, Zhou X, Yu J, Jian R, Tang S, Yin L, Zhou P. RNAi-mediated CD73 suppression induces apoptosis and cell-cycle arrest in human breast cancer cells. Cancer Sci 2010; 101:2561–9; PMID:20874842; http://dx.doi.org/10.1111/j.1349-7006.2010.01733.x
   PubMed Web of Science ®Google Scholar
• Bavaresco L, Bernardi A, Braganhol E, Cappellari AR, Rockenbach L, Farias PF, Wink MR, Delgado-Canedo A, Battastini AM. The role of ecto-5′-nucleotidase/CD73 in glioma cell line proliferation. Mol Cell Biochem 2008; 319:61–8; PMID:18636315; http://dx.doi.org/10.1007/s11010-008-9877-3
   PubMed Web of Science ®Google Scholar
• Wang L, Zhou X, Zhou T, Ma D, Chen S, Zhi X, Yin L, Shao Z, Ou Z, Zhou P. Ecto-5′-nucleotidase promotes invasion, migration and adhesion of human breast cancer cells. J Cancer Res Clin Oncol 2008; 134:365–72; PMID:17671792; http://dx.doi.org/10.1007/s00432-007-0292-z
   PubMed Web of Science ®Google Scholar
• Naito Y, Lowenstein JM. 5′-nucleotidase from rat heart. Biochemistry 1981; 20:5188–94; PMID:6271180; http://dx.doi.org/10.1021/bi00521a014
   PubMed Web of Science ®Google Scholar
• Airas L, Niemela J, Salmi M, Puurunen T, Smith DJ, Jalkanen S. Differential regulation and function of CD73, a glycosyl-phosphatidylinositol-linked 70-kD adhesion molecule, on lymphocytes and endothelial cells. J Cell Biol 1997; 136:421–31; PMID:9015312; http://dx.doi.org/10.1083/jcb.136.2.421
   PubMed Web of Science ®Google Scholar
• Knapp K, Zebisch M, Pippel J, El-Tayeb A, Muller CE, Strater N. Crystal structure of the human ecto-5′-nucleotidase (CD73): Insights into the regulation of purinergic signaling. Structure 2012; 20:2161–73; PMID:23142347; http://dx.doi.org/10.1016/j.str.2012.10.001
   PubMed Web of Science ®Google Scholar
• Knofel T, Strater N. Mechanism of hydrolysis of phosphate esters by the dimetal center of 5′-nucleotidase based on crystal structures. J Mol Biol 2001; 309:239–54; PMID:11491293; http://dx.doi.org/10.1006/jmbi.2001.4656
   PubMed Web of Science ®Google Scholar
• Schultz-Heienbrok R, Maier T, Strater N. A large hinge bending domain rotation is necessary for the catalytic function of escherichia coli 5′-nucleotidase. Biochemistry 2005; 44:2244–52; PMID:15709736; http://dx.doi.org/10.1021/bi047989c
   PubMed Web of Science ®Google Scholar
• Knofel T, Strater N. E. coli 5′-nucleotidase undergoes a hinge-bending domain rotation resembling a ball-and-socket motion. J Mol Biol 2001; 309:255–66; PMID:11491294; http://dx.doi.org/10.1006/jmbi.2001.4657
   PubMed Web of Science ®Google Scholar
• Ipata PL. Studies on the inhibition by nucleoside-triphosphates of sheep brain 5-nucleotidase. Biochem Biophys Res Commun 1967; 27:337–43; PMID:6035114; http://dx.doi.org/10.1016/S0006-291X(67)80103-7
   PubMed Web of Science ®Google Scholar
• Burger RM, Lowenstein JM. Preparation and properties of 5′-nucleotidase from smooth muscle of small intestine. J Biol Chem 1970; 245:6274–80; PMID:4320834
   PubMed Web of Science ®Google Scholar
• Iqbal J, Saeed A, Raza R, Matin A, Hameed A, Furtmann N, Lecka J, Sevigny J, Bajorath J. Identification of sulfonic acids as efficient ecto-5′-nucleotidase inhibitors. Eur J Med Chem 2013; 70:685–91; PMID:24215819; http://dx.doi.org/10.1016/j.ejmech.2013.10.053
   PubMed Web of Science ®Google Scholar
• Raza R, Saeed A, Lecka J, Sevigny J, Iqbal J. Identification of small molecule sulfonic acids as ecto-5′-nucleotidase inhibitors. Med Chem 2012; 8:1133–9; PMID:22741787; http://dx.doi.org/10.2174/1573406411208061133
   PubMed Web of Science ®Google Scholar
• Braganhol E, Tamajusuku AS, Bernardi A, Wink MR, Battastini AM. Ecto-5′-nucleotidase/CD73 inhibition by quercetin in the human U138MG glioma cell line. Biochim Biophys Acta 2007; 1770:1352–9; PMID:17643826; http://dx.doi.org/10.1016/j.bbagen.2007.06.003
   PubMed Web of Science ®Google Scholar
• Gagliardi AR, Kassack M, Kreimeyer A, Muller G, Nickel P, Collins DC. Antiangiogenic and antiproliferative activity of suramin analogues. Cancer Chemother Pharmacol 1998; 41:117–24; PMID:9443624; http://dx.doi.org/10.1007/s002800050717
   PubMed Web of Science ®Google Scholar
• Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, Denoyer D, Dwyer KM, Smyth MJ. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A 2010; 107:1547–52; PMID:20080644; http://dx.doi.org/10.1073/pnas.0908801107
   PubMed Web of Science ®Google Scholar
• Rust S, Guillard S, Sachsenmeier K, Hay C, Davidson M, Karlsson A, Karlsson R, Brand E, Lowne D, Elvin J, et al. Combining phenotypic and proteomic approaches to identify membrane targets in a ‘triple negative’ breast cancer cell type. Mol Cancer 2013; 12:11:4598-12-11; PMID:23406016; http;//dx.doi.org/10.1186/1476-4598-12-11
   PubMed Web of Science ®Google Scholar
• Terp MG, Olesen KA, Arnspang EC, Lund RR, Lagerholm BC, Ditzel HJ, Leth-Larsen R. Anti-human CD73 monoclonal antibody inhibits metastasis formation in human breast cancer by inducing clustering and internalization of CD73 expressed on the surface of cancer cells. J Immunol 2013; 191:4165–73; PMID:24043904; http://dx.doi.org/10.4049/jimmunol.1301274
   PubMed Web of Science ®Google Scholar
• Allard B, Turcotte M, Stagg J. Targeting CD73 and downstream adenosine receptor signaling in triple-negative breast cancer. Expert Opin Ther Targets 2014; 18:863–81; PMID:24798880; http://dx.doi.org/10.1517/14728222.2014.915315
   PubMed Web of Science ®Google Scholar
• Sachsenmeier KF, Hay C, Brand E, Clarke L, Rosenthal K, Guillard S, Rust S, Minter R, Hollingsworth R. Development of a novel ectonucleotidase assay suitable for high-throughput screening. J Biomol Screen 2012; 17:993–8; PMID:22522649; http://dx.doi.org/10.1177/1087057112443987
   PubMed Web of Science ®Google Scholar
• Hay C, Sult E, Huang Q, Hammond S, Mulgrew K, McGlinchey K, Fuhrmann S, Rothstein R, Poon E, Stewart R, Hollingsworth R, Sachsenmeier K. MEDI9447: enhancing anti-tumor immunity by targeting CD73 In the tumor microenvironment. [abstract]. In: Proceedings of the 106th Annual Meeting of the American Association for Cancer Research; 2015 Apr 18–22; Philadelphia, PA. Philadelphia (PA): AACR; Cancer Res 2015;75(15 Suppl): Abstract nr 285.
   Google Scholar
• Burger RM, Lowenstein JM. 5′-nucleotidase from smooth muscle of small intestine and from brain. inhibition of nucleotides. Biochemistry 1975; 14:2362–6; PMID:1169962; http://dx.doi.org/10.1021/bi00682a014
   PubMed Web of Science ®Google Scholar
• Parker CH, Morgan CR, Rand KD, Engen JR, Jorgenson JW, Stafford DW. A conformational investigation of propeptide binding to the integral membrane protein gamma-glutamyl carboxylase using nanodisc hydrogen exchange mass spectrometry. Biochemistry 2014; 53:1511–20; PMID:24512177; http://dx.doi.org/10.1021/bi401536m
   PubMed Web of Science ®Google Scholar
• Wei H, Mo J, Tao L, Russell RJ, Tymiak AA, Chen G, Iacob RE, Engen JR. Hydrogen/deuterium exchange mass spectrometry for probing higher order structure of protein therapeutics: Methodology and applications. Drug Discov Today 2014; 19:95–102; PMID:23928097; http://dx.doi.org/10.1016/j.drudis.2013.07.019
   PubMed Web of Science ®Google Scholar
• Marcsisin SR, Narute PS, Emert-Sedlak LA, Kloczewiak M, Smithgall TE, Engen JR. On the solution conformation and dynamics of the HIV-1 viral infectivity factor. J Mol Biol 2011; 410:1008–22; PMID:21763503; http://dx.doi.org/10.1016/j.jmb.2011.04.053
   PubMed Web of Science ®Google Scholar
• Oganesyan V, Peng L, Damschroder MM, Cheng L, Sadowska A, Tkaczyk C, Sellman BR, Wu H, Dall'Acqua WF. Mechanisms of neutralization of a human anti-alpha-toxin antibody. J Biol Chem 2014; 289:29874–80; PMID:25210036; http://dx.doi.org/10.1074/jbc.M114.601328
   PubMed Web of Science ®Google Scholar
• Peng L, Oganesyan V, Wu H, Dall'Acqua WF, Damschroder MM. Molecular basis for antagonistic activity of anifrolumab, an anti-interferon-alpha receptor 1 antibody. MAbs 2015; 7:428–39; PMID:25606664; http://dx.doi.org/10.1080/19420862.2015.1007810
   PubMed Web of Science ®Google Scholar
• Charrie A, Charriere G, Guerrier A. Hook effect in immunometric assays for prostate-specific antigen. Clin Chem 1995; 41:480–1; PMID:7533675
   PubMed Web of Science ®Google Scholar
• Klemens MR, Sherman WR, Holmberg NJ, Ruedi JM, Low MG, Thompson LF. Characterization of soluble vs membrane-bound human placental 5′-nucleotidase. Biochem Biophys Res Commun 1990; 172:1371–7; PMID:2173922; http://dx.doi.org/10.1016/0006-291X(90)91601-N
   PubMed Web of Science ®Google Scholar
• Piec G, Le Hir M. The soluble ‘low-km’ 5′-nucleotidase of rat kidney represents solubilized ecto-5′-nucleotidase. Biochem J 1991; 273(Pt 2):409–13; PMID:1846740; http://dx.doi.org/10.1042/bj2730409
   PubMed Web of Science ®Google Scholar
• Brinkley BR, Beall PT, Wible LJ, Mace ML, Turner DS, Cailleau RM. Variations in cell form and cytoskeleton in human breast carcinoma cells in vitro. Cancer Res 1980; 40:3118–29; PMID:7000337
   PubMed Web of Science ®Google Scholar
• Lamba V, Ghosh I. New directions in targeting protein kinases: Focusing upon true allosteric and bivalent inhibitors. Curr Pharm Des 2012; 18:2936–45; PMID:22571662; http://dx.doi.org/10.2174/138161212800672813
   PubMed Web of Science ®Google Scholar
• Grover AK. Use of allosteric targets in the discovery of safer drugs. Med Princ Pract 2013; 22:418–26; PMID:23711993; http://dx.doi.org/10.1159/000350417
   PubMed Web of Science ®Google Scholar
• Baqi Y, Weyler S, Iqbal J, Zimmermann H, Muller CE. Structure-activity relationships of anthraquinone derivatives derived from bromaminic acid as inhibitors of ectonucleoside triphosphate diphosphohydrolases (E-NTPDases). Purinergic Signal 2009; 5:91–106; PMID:18528783; http://dx.doi.org/10.1007/s11302-008-9103-5
   PubMed Web of Science ®Google Scholar
• Evans WH, Gurd JW. Properties of a 5′-nucleotidase purified from mouse liver plasma membranes. Biochem J 1973; 133:189–99; PMID:4721620; http://dx.doi.org/10.1042/bj1330189
   PubMed Web of Science ®Google Scholar
• Goding JW. Ecto-enzymes: Physiology meets pathology. J Leukoc Biol 2000; 67:285–311; PMID:10733089
   PubMed Web of Science ®Google Scholar
• Salmi M, Jalkanen S. Cell-surface enzymes in control of leukocyte trafficking. Nat Rev Immunol 2005; 5:760–71; PMID:16200079; http://dx.doi.org/10.1038/nri1705
   PubMed Web of Science ®Google Scholar
• Groves M, Lane S, Douthwaite J, Lowne D, Rees DG, Edwards B, Jackson RH. Affinity maturation of phage display antibody populations using ribosome display. J Immunol Methods 2006; 313:129–39; PMID:16730741; http://dx.doi.org/10.1016/j.jim.2006.04.002
   PubMed Web of Science ®Google Scholar
• Xiao X, Chen Y, Mugabe S, Gao C, Tkaczyk C, Mazor Y, Pavlik P, Wu H, Dall'Acqua W, Chowdhury PS. A novel dual expression platform for high throughput functional screening of phage libraries in product like format. PLoS One 2015; 10:e0140691; PMID:26468955; http://dx.doi.org/10.1371/journal.pone.0140691
   PubMed Web of Science ®Google Scholar
• Oganesyan V, Gao C, Shirinian L, Wu H, Dall'Acqua WF. Structural characterization of a human fc fragment engineered for lack of effector functions. Acta Crystallogr D Biol Crystallogr 2008; 64:700–4; PMID:18560159; http://dx.doi.org/10.1107/S0907444908007877
   PubMed Web of Science ®Google Scholar
• Houde D, Berkowitz SA, Engen JR. The utility of hydrogen/deuterium exchange mass spectrometry in biopharmaceutical comparability studies. J Pharm Sci 2011; 100:2071–86; PMID:21491437; http://dx.doi.org/10.1002/jps.22432
   PubMed Web of Science ®Google Scholar
• Henikoff S, Henikoff JG. Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci U S A 1992; 89:10915–9; PMID:1438297; http://dx.doi.org/10.1073/pnas.89.22.10915
   PubMed Web of Science ®Google Scholar