References
- Muenst S, Laubli H, Soysal SD, Zippelius A, Tzankov A, Hoeller S. The immune system and cancer evasion strategies: therapeutic concepts. J Intern Med. 2016;279:541–17. doi:https://doi.org/10.1111/joim.12470.
- Munn DH, Bronte V. Immune suppressive mechanisms in the tumor microenvironment. Curr Opin Immunol. 2016;39:1–6. doi:https://doi.org/10.1016/j.coi.2015.10.009.
- Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol. 2007;25:267–96. doi:https://doi.org/10.1146/annurev.immunol.25.022106.141609.
- Timosenko E, Hadjinicolaou AV, Cerundolo V. Modulation of cancer-specific immune responses by amino acid degrading enzymes. Immunotherapy. 2017;9:83–97. doi:https://doi.org/10.2217/imt-2016-0118.
- Umansky V, Adema GJ, Baran J, Brandau S, Van Ginderachter JA, Hu X, Jablonska J, Mojsilovic S, Papadaki HA, De Coaña YP, et al. Interactions among myeloid regulatory cells in cancer. Cancer Immunol Immunother. 2019;68:645–60. doi:https://doi.org/10.1007/s00262-018-2200-6.
- Bronte V, Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol. 2005;5:641–54. doi:https://doi.org/10.1038/nri1668.
- Martí I Líndez -A-A, Dunand-Sauthier I, Conti M, Gobet F, Núñez N, Hannich JT, Riezman H, Geiger R, Piersigilli A, Hahn K, et al. Mitochondrial arginase-2 is a cell‑autonomous regulator of CD8+ T cell function and antitumor efficacy. JCI Insight. 2019;4:e132975. doi:https://doi.org/10.1172/jci.insight.132975.
- Wu G, Morris SM Jr. Arginine metabolism: nitric oxide and beyond. Biochem J. 1998;336(Pt 1):1–17. doi:https://doi.org/10.1042/bj3360001.
- Mussai F, Egan S, Hunter S, Webber H, Fisher J, Wheat R, McConville C, Sbirkov Y, Wheeler K, Bendle G, et al. Neuroblastoma arginase activity creates an immunosuppressive microenvironment that impairs autologous and engineered immunity. Cancer Res. 2015;75:3043–53. doi:https://doi.org/10.1158/0008-5472.CAN-14-3443.
- Zaytouni T, Tsai PY, Hitchcock DS, DuBois CD, Freinkman E, Lin L, Morales-Oyarvide V, Lenehan PJ, Wolpin BM, Mino-Kenudson M, et al. Critical role for arginase 2 in obesity-associated pancreatic cancer. Nat Commun. 2017;8:242. doi:https://doi.org/10.1038/s41467-017-00331-y.
- Ino Y, Yamazaki-Itoh R, Oguro S, Shimada K, Kosuge T, Zavada J, Kanai Y, Hiraoka N. Arginase II expressed in cancer-associated fibroblasts indicates tissue hypoxia and predicts poor outcome in patients with pancreatic cancer. PLoS One. 2013;8:e55146–e. doi:https://doi.org/10.1371/journal.pone.0055146.
- Mussai F, De Santo C, Abu-Dayyeh I, Booth S, Quek L, McEwen-Smith RM, Qureshi A, Dazzi F, Vyas P, Cerundolo V, et al. Acute myeloid leukemia creates an arginase-dependent immunosuppressive microenvironment. Blood. 2013;122:749–58. doi:https://doi.org/10.1182/blood-2013-01-480129.
- Miraki-Moud F, Ghazaly E, Ariza-McNaughton L, Hodby KA, Clear A, Anjos-Afonso F, Liapis K, Grantham M, Sohrabi F, Cavenagh J, et al. Arginine deprivation using pegylated arginine deiminase has activity against primary acute myeloid leukemia cells in vivo. Blood. 2015;125:4060–68. doi:https://doi.org/10.1182/blood-2014-10-608133.
- Tate DJ Jr., Vonderhaar DJ, Caldas YA, Metoyer T, Patterson J, Aviles DH, Zea AH. Effect of arginase II on L-arginine depletion and cell growth in murine cell lines of renal cell carcinoma. J Hematol Oncol. 2008;1:14. doi:https://doi.org/10.1186/1756-8722-1-14.
- Pudlo M, Demougeot C, Girard-Thernier C. Arginase inhibitors: a rational approach over one century. Med Res Rev. 2017;37:475–513. doi:https://doi.org/10.1002/med.21419.
- Wang Y, Zhao P, Qian D, Hu M, Zhang L, Shi H, Wang B. MicroRNA-613 is downregulated in HCMV-positive glioblastoma and inhibits tumour progression by targeting arginase-2. Tumour Biol. 2017;39:1010428317712512. doi:https://doi.org/10.1177/1010428317712512.
- Rodriguez PC, Quiceno DG, Zabaleta J, Ortiz B, Zea AH, Piazuelo MB, Delgado A, Correa P, Brayer J, Sotomayor EM, et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res. 2004;64:5839–49. doi:https://doi.org/10.1158/0008-5472.CAN-04-0465.
- Steggerda SM, Bennett MK, Chen J, Emberley E, Huang T, Janes JR, Li W, MacKinnon AL, Makkouk A, Marguier G, et al. Inhibition of arginase by CB-1158 blocks myeloid cell-mediated immune suppression in the tumor microenvironment. J Immunother Cancer. 2017;5:101. doi:https://doi.org/10.1186/s40425-017-0308-4.
- Imai K, Takaoka A. Comparing antibody and small-molecule therapies for cancer. Nat Rev Cancer. 2006;6:714–27. doi:https://doi.org/10.1038/nrc1913.
- Vaughan TJ, Williams AJ, Pritchard K, Osbourn JK, Pope AR, Earnshaw JC, McCafferty J, Hodits RA, Wilton J, Johnson KS, et al. Human antibodies with sub-nanomolar affinities isolated from a large non-immunized phage display library. Nat Biotechnol. 1996;14:309–14. doi:https://doi.org/10.1038/nbt0396-309.
- 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. doi:https://doi.org/10.1016/j.jim.2006.04.002.
- Lloyd C, Lowe D, Edwards B, Welsh F, Dilks T, Hardman C, Vaughan T. Modelling the human immune response: performance of a 1011 human antibody repertoire against a broad panel of therapeutically relevant antigens. Protein Eng Des Sel. 2009;22:159–68. doi:https://doi.org/10.1093/protein/gzn058.
- Einhorn L, Krapfenbauer K. HTRF: a technology tailored for biomarker determination-novel analytical detection system suitable for detection of specific autoimmune antibodies as biomarkers in nanogram level in different body fluids. Epma J. 2015;6:23. doi:https://doi.org/10.1186/s13167-015-0046-y.
- Zhou Y, Goenaga AL, Harms BD, Zou H, Lou J, Conrad F, Adams GP, Schoeberl B, Nielsen UB, Marks JD, et al. Impact of intrinsic affinity on functional binding and biological activity of EGFR antibodies. Mol Cancer Ther. 2012;11:1467–76. doi:https://doi.org/10.1158/1535-7163.MCT-11-1038.
- Chan DTY, Jenkinson L, Haynes SW, Austin M, Diamandakis A, Burschowsky D, Seewooruthun C, Addyman A, Fiedler S, Ryman S, et al. Extensive sequence and structural evolution of Arginase 2 inhibitory antibodies enabled by an unbiased approach to affinity maturation. Proc Natl Acad Sci USA. 2020;117:16949–60. doi:https://doi.org/10.1073/pnas.1919565117.
- Kabat EA, Wu TT. Identical V region amino acid sequences and segments of sequences in antibodies of different specificities. Relative contributions of VH and VL genes, minigenes, and complementarity-determining regions to binding of antibody-combining sites. J Immunol. 1991;147:1709–19.
- Strelow J, Dewe W, Iversen PW, Brooks HB, Radding JA, McGee J, Weidner J. Mechanism of action assays for enzymes. In: Sittampalam GS, Grossman A, Brimacombe K, Arkin M, Auld D, Austin C, Baell J, Bejcek B, Caaveiro JMM, Chung TDY, et al. editors. Assay guidance manual. Bethesda (MD): Eli Lilly & Company and the National Center for Advancing Translational Sciences; 2004;65–86.
- Van Zandt MC, Whitehouse DL, Golebiowski A, Ji MK, Zhang M, Beckett RP, Jagdmann GE, Ryder TR, Sheeler R, Andreoli M, et al. Discovery of (R)-2-amino-6-borono-2-(2-(piperidin-1-yl)ethyl)hexanoic acid and congeners as highly potent inhibitors of human arginases I and II for treatment of myocardial reperfusion injury. J Med Chem. 2013;56:2568–80. doi:https://doi.org/10.1021/jm400014c.
- Cox JD, Kim NN, Traish AM, Christianson DW. Arginase-boronic acid complex highlights a physiological role in erectile function. Nat Struct Biol. 1999;6:1043–47. doi:https://doi.org/10.1038/14929.
- Cavalli RC, Burke CJ, Kawamoto S, Soprano DR, Ash DE. Mutagenesis of rat liver arginase expressed in Escherichia coli: role of conserved histidines. Biochemistry. 1994;33:10652–57. doi:https://doi.org/10.1021/bi00201a012.
- Kanyo ZF, Scolnick LR, Ash DE, Christianson DW. Structure of a unique binuclear manganese cluster in arginase. Nature. 1996;383:554–57. doi:https://doi.org/10.1038/383554a0.
- Cama E, Colleluori DM, Emig FA, Shin H, Kim SW, Kim NN, Traish AM, Ash DE, Christianson DW. Human Arginase II: crystal structure and physiological role in male and female sexual arousal†,‡. Biochemistry. 2003;42:8445–51. doi:https://doi.org/10.1021/bi034340j.
- Zhang J, Valianou M, Simmons H, Robinson MK, Lee HO, Mullins SR, Marasco WA, Adams GP, Weiner LM, Cheng JD, et al. Identification of inhibitory scFv antibodies targeting fibroblast activation protein utilizing phage display functional screens. FASEB J. 2013;27:581–89. doi:https://doi.org/10.1096/fj.12-210377.
- Fischer T, Riedl R. Inhibitory antibodies designed for matrix metalloproteinase modulation. Molecules. 2019;24:2265. doi:https://doi.org/10.3390/molecules24122265.
- Santamaria S, de Groot R. Monoclonal antibodies against metzincin targets. Br J Pharmacol. 2019;176:52–66. doi:https://doi.org/10.1111/bph.14186.
- Sela-Passwell N, Kikkeri R, Dym O, Rozenberg H, Margalit R, Arad-Yellin R, Eisenstein M, Brenner O, Shoham T, Danon T, et al. Antibodies targeting the catalytic zinc complex of activated matrix metalloproteinases show therapeutic potential. Nat Med. 2011;18:143–47. doi:https://doi.org/10.1038/nm.2582.
- Lauwereys M, Ghahroudi MA, Desmyter A, Kinne J, Holzer W, De Genst E, Wyns L, Muyldermans S. Potent enzyme inhibitors derived from dromedary heavy-chain antibodies. Embo J. 1998;17:3512–20. doi:https://doi.org/10.1093/emboj/17.13.3512.
- Matz H, Dooley H. Shark IgNAR-derived binding domains as potential diagnostic and therapeutic agents. Dev Comp Immunol. 2019;90:100–07. doi:https://doi.org/10.1016/j.dci.2018.09.007.
- Stanfield RL, Dooley H, Flajnik MF, Wilson IA. Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science. 2004;305:1770–73. doi:https://doi.org/10.1126/science.1101148.
- Nam DH, Rodriguez C, Remacle AG, Strongin AY, Ge X. Active-site MMP-selective antibody inhibitors discovered from convex paratope synthetic libraries. Proc Natl Acad Sci USA. 2016;113:14970–75. doi:https://doi.org/10.1073/pnas.1609375114.
- McCafferty J, Fitzgerald KJ, Earnshaw J, Chiswell DJ, Link J, Smith R, Kenten J. Selection and rapid purification of murine antibody fragments that bind a transition-state analog by phage display. Appl Biochem Biotechnol. 1994;47:157–71. discussion 71-3. doi:https://doi.org/10.1007/BF02787932.
- Hawkins RE, Russell SJ, Winter G. Selection of phage antibodies by binding affinity. Mimicking affinity maturation. J Mol Biol. 1992;226:889–96. doi:https://doi.org/10.1016/0022-2836(92)90639-2.
- Dobson CL, Main S, Newton P, Chodorge M, Cadwallader K, Humphreys R, Albert V, Vaughan TJ, Minter RR, Edwards BM, et al. Human monomeric antibody fragments to TRAIL-R1 and TRAIL-R2 that display potent in vitro agonism. mAbs. 2009;1:552–62. doi:https://doi.org/10.4161/mabs.1.6.10057.
- Osbourn JK, McCafferty J, Derbyshire EJ, Waibel R, Chester KA, Boxer G, Allen D. Isolation of a panel of human anti-CEA single chain Fv from a large phage display library. Tumor Target. 1999;4:150–57.
- Daghigh F, Fukuto JM, Ash DE. Inhibition of rat liver arginase by an intermediate in NO biosynthesis, NG-hydroxy-L-arginine: implications for the regulation of nitric oxide biosynthesis by arginase. Biochem Biophys Res Commun. 1994;202:174–80. doi:https://doi.org/10.1006/bbrc.1994.1909.
- Persic L, Roberts A, Wilton J, Cattaneo A, Bradbury A, Hoogenboom HR. An integrated vector system for the eukaryotic expression of antibodies or their fragments after selection from phage display libraries. Gene. 1997;187:9–18. doi:https://doi.org/10.1016/S0378-1119(96)00628-2.
- Kabsch W. Xds. Acta Crystallogr D Biol Crystallogr. 2010;66:125–32. doi:https://doi.org/10.1107/S0907444909047337.
- Evans PR, Murshudov GN. How good are my data and what is the resolution? Acta Crystallogr D. 2013;69:1204–14. doi:https://doi.org/10.1107/S0907444913000061.
- McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40:658–74. doi:https://doi.org/10.1107/S0021889807021206.
- Marcatili P, Rosi A, Tramontano A. PIGS: automatic prediction of antibody structures. Bioinformatics. 2008;24:1953–54. doi:https://doi.org/10.1093/bioinformatics/btn341.
- Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr. 2011;67:355–67. doi:https://doi.org/10.1107/S0907444911001314.
- Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66:486–501. doi:https://doi.org/10.1107/S0907444910007493.
- Nurizzo D, Mairs T, Guijarro M, Rey V, Meyer J, Fajardo P, Chavanne J, Biasci J-C, McSweeney S, Mitchell E, et al. The ID23-1 structural biology beamline at the ESRF. J Synchrotron Radiat. 2006;13:227–38. doi:https://doi.org/10.1107/S0909049506004341.
- Mueller U, Förster R, Hellmig M, Huschmann FU, Kastner A, Malecki P, Pühringer S, Röwer M, Sparta K, Steffien M, et al. The macromolecular crystallography beamlines at BESSY II of the Helmholtz-Zentrum Berlin: current status and perspectives. Eur Phys J Plus. 2015;130:141. doi:https://doi.org/10.1140/epjp/i2015-15141-2.
- Newman J. Novel buffer systems for macromolecular crystallization. Acta Crystallogr D Biol Crystallogr. 2004;60:610–12. doi:https://doi.org/10.1107/S0907444903029640.
- Lebedev AA, Isupov MN. Space-group and origin ambiguity in macromolecular structures with pseudo-symmetry and its treatment with the program Zanuda. Acta Crystallogr D Biol Crystallogr. 2014;70:2430–43. doi:https://doi.org/10.1107/S1399004714014795.
- Schrödinger release 2017–2. New York (NY): Schrödinger, LLC; 2019. p. 2017. https://www.schrodinger.com/platform.
- Sondergaard CR, Olsson MH, Rostkowski M, Jensen JH. Improved treatment of ligands and coupling effects in empirical calculation and rationalization of pKa values. J Chem Theory Comput. 2011;7:2284–95. doi:https://doi.org/10.1021/ct200133y.
- Farid R, Day T, Friesner RA, Pearlstein RA. New insights about HERG blockade obtained from protein modeling, potential energy mapping, and docking studies. Bioorg Med Chem. 2006;14:3160–73. doi:https://doi.org/10.1016/j.bmc.2005.12.032.
- Sherman W, Beard HS, Farid R. Use of an induced fit receptor structure in virtual screening. Chem Biol Drug Des. 2006;67:83–84. doi:https://doi.org/10.1111/j.1747-0285.2005.00327.x.
- Sherman W, Day T, Jacobson MP, Friesner RA, Farid R. Novel procedure for modeling ligand/receptor induced fit effects. J Med Chem. 2006;49:534–53. doi:https://doi.org/10.1021/jm050540c.