{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T12:55:39Z","timestamp":1783515339830,"version":"3.55.0"},"reference-count":81,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2023,3,17]],"date-time":"2023-03-17T00:00:00Z","timestamp":1679011200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,3,17]],"date-time":"2023-03-17T00:00:00Z","timestamp":1679011200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001773","name":"University of New South Wales","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100001773","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Comput Aided Mol Des"],"published-print":{"date-parts":[[2023,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Carbonic anhydrase is an attractive drug target for the treatment of many diseases. This paper examines the ability of end-state MM\/GBSA methods to rank inhibitors of carbonic anhydrase in terms of their binding affinities. The MM\/GBSA binding energies were evaluated using different atomic charge schemes (Mulliken, ESP and NPA) at different levels of theories, including Hartree\u2013Fock, B3LYP-D3(BJ), and M06-2X with the 6\u201331G(d,p) basis set. For a large test set of 32 diverse inhibitors, the use of B3LYP-D3(BJ) ESP atomic charges yielded the strongest correlation with experiment (R<jats:sup>2<\/jats:sup>\u2009=\u20090.77). The use of the recently enhanced Autodock Vina and zinc optimised AD4<jats:sub>Zn<\/jats:sub> force field also predicted ligand binding affinities with moderately strong correlation (R<jats:sup>2<\/jats:sup>\u2009=\u20090.64) at significantly lower computational cost. However, the docked poses deviate significantly from crystal structures. Overall, this study demonstrates the applicability of docking to estimate ligand binding affinities for a diverse range of CA inhibitors, and indicates that more theoretically robust MM\/GBSA simulations show promise for improving the accuracy of predicted binding affinities, as long as a validated set of parameters is used.<\/jats:p>\n                <jats:p><jats:bold>Graphical abstract<\/jats:bold><\/jats:p>","DOI":"10.1007\/s10822-023-00499-0","type":"journal-article","created":{"date-parts":[[2023,3,17]],"date-time":"2023-03-17T12:02:56Z","timestamp":1679054576000},"page":"167-182","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["MM\/GBSA prediction of relative binding affinities of carbonic anhydrase inhibitors: effect of atomic charges and comparison with Autodock4Zn"],"prefix":"10.1007","volume":"37","author":[{"given":"Mackenzie","family":"Taylor","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junming","family":"Ho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,3,17]]},"reference":[{"key":"499_CR1","doi-asserted-by":"publisher","DOI":"10.1021\/ja061574s","author":"V Alterio","year":"2006","unstructured":"Alterio V, Vitale RM, Monti SM et al (2006) Carbonic anhydrase inhibitors: X-ray and molecular modeling study for the interaction of a fluorescent antitumor sulfonamide with isozyme II and IX. J Am Chem Soc. https:\/\/doi.org\/10.1021\/ja061574s","journal-title":"J Am Chem Soc"},{"key":"499_CR2","doi-asserted-by":"publisher","DOI":"10.1021\/acsmedchemlett.7b00280","author":"A Angeli","year":"2017","unstructured":"Angeli A, Tanini D, Peat TS et al (2017) Discovery of new selenoureido analogues of 4-(4-fluorophenylureido)benzenesulfonamide as carbonic anhydrase inhibitors. ACS Med Chem Lett. https:\/\/doi.org\/10.1021\/acsmedchemlett.7b00280","journal-title":"ACS Med Chem Lett"},{"key":"499_CR3","doi-asserted-by":"publisher","DOI":"10.3390\/catal10091008","author":"A Angeli","year":"2020","unstructured":"Angeli A, Carta F, Supuran CT (2020) Carbonic anhydrases: versatile and useful biocatalysts in chemistry and biochemistry. Catalysts. https:\/\/doi.org\/10.3390\/catal10091008","journal-title":"Catalysts"},{"key":"499_CR4","doi-asserted-by":"publisher","DOI":"10.1016\/j.pain.2009.11.015","author":"M Asiedu","year":"2010","unstructured":"Asiedu M, Ossipov MH, Kaila K et al (2010) Acetazolamide and midazolam act synergistically to inhibit neuropathic pain. Pain. https:\/\/doi.org\/10.1016\/j.pain.2009.11.015","journal-title":"Pain"},{"key":"499_CR5","doi-asserted-by":"publisher","DOI":"10.1107\/S0907444910006554","author":"CA Behnke","year":"2010","unstructured":"Behnke CA, Le Trong I, Godden JW et al (2010) Atomic resolution studies of carbonic anhydrase II. Acta Crystallogr D Biol Crystallogr. https:\/\/doi.org\/10.1107\/S0907444910006554","journal-title":"Acta Crystallogr D Biol Crystallogr"},{"issue":"1","key":"499_CR6","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1093\/nar\/28.1.235","volume":"28","author":"HM Berman","year":"2000","unstructured":"Berman HM, Westbrook J, Feng Z et al (2000) The protein data bank. Nucleic Acids Res 28(1):235\u2013242","journal-title":"Nucleic Acids Res"},{"key":"499_CR7","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jmedchem.0c00733","author":"A Bonardi","year":"2020","unstructured":"Bonardi A, Nocentini A, Bua S et al (2020) Sulfonamide inhibitors of human carbonic anhydrases designed through a three-tails approach: improving ligand\/isoform matching and selectivity of action. J Med Chem. https:\/\/doi.org\/10.1021\/acs.jmedchem.0c00733","journal-title":"J Med Chem"},{"key":"499_CR8","doi-asserted-by":"publisher","DOI":"10.1055\/s-2007-1024597","author":"AR Bradwell","year":"1992","unstructured":"Bradwell AR, Wright AD, Winterborn M et al (1992) Acetazolamide and high altitude diseases. Int J Sports Med. https:\/\/doi.org\/10.1055\/s-2007-1024597","journal-title":"Int J Sports Med"},{"key":"499_CR9","doi-asserted-by":"publisher","DOI":"10.1002\/jcc.21287","author":"BR Brooks","year":"2009","unstructured":"Brooks BR, Brooks CL 3rd, Mackerell AD Jr et al (2009) CHARMM: the biomolecular simulation program. J Comput Chem. https:\/\/doi.org\/10.1002\/jcc.21287","journal-title":"J Comput Chem"},{"key":"499_CR10","doi-asserted-by":"publisher","DOI":"10.3390\/molecules20045667","author":"S Carradori","year":"2015","unstructured":"Carradori S, Mollica A, De Monte C et al (2015) Nitric oxide donors and selective carbonic anhydrase inhibitors: a dual pharmacological approach for the treatment of glaucoma, cancer and osteoporosis. Molecules. https:\/\/doi.org\/10.3390\/molecules20045667","journal-title":"Molecules"},{"key":"499_CR11","doi-asserted-by":"publisher","DOI":"10.1016\/j.bmc.2017.03.027","author":"F Carta","year":"2017","unstructured":"Carta F, Vullo D, Osman SM et al (2017) Synthesis and carbonic anhydrase inhibition of a series of SLC-0111 analogs. Bioorg Med Chem. https:\/\/doi.org\/10.1016\/j.bmc.2017.03.027","journal-title":"Bioorg Med Chem"},{"key":"499_CR12","volume-title":"Amber 2021","author":"DA Case","year":"2021","unstructured":"Case DA, Aktulga HM, Belfon K et al (2021) Amber 2021. University of California, San Francisco"},{"key":"499_CR13","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpc.2020.106439","author":"V Chahal","year":"2020","unstructured":"Chahal V, Nirwan S, Kakkar R (2020) A comparative study of the binding modes of SLC-0111 and its analogues in the hCA II and hCA IX active sites using QM\/MM, molecular docking, MM-GBSA and MD approaches. Biophys Chem. https:\/\/doi.org\/10.1016\/j.bpc.2020.106439","journal-title":"Biophys Chem"},{"key":"499_CR14","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jctc.2c00491","author":"J Chen","year":"2022","unstructured":"Chen J, Harper JB, Ho J (2022) Improving the accuracy of quantum mechanics\/molecular mechanics (QM\/MM) models with polarized fragment charges. J Chem Theory Comput. https:\/\/doi.org\/10.1021\/acs.jctc.2c00491","journal-title":"J Chem Theory Comput"},{"key":"499_CR15","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.Can-08-2470","author":"J Chiche","year":"2009","unstructured":"Chiche J, Ilc K, Laferriere J et al (2009) Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. https:\/\/doi.org\/10.1158\/0008-5472.Can-08-2470","journal-title":"Cancer Res"},{"key":"499_CR16","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jcim.9b00346","author":"SS Cinaroglu","year":"2019","unstructured":"Cinaroglu SS, Timucin E (2019) Comparative assessment of seven docking programs on a nonredundant metalloprotein subset of the PDBbind refined. J Chem Inf Model. https:\/\/doi.org\/10.1021\/acs.jcim.9b00346","journal-title":"J Chem Inf Model"},{"key":"499_CR17","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejmech.2013.10.071","author":"L De Luca","year":"2014","unstructured":"De Luca L, Ferro S, Damiano FM et al (2014) Structure-based screening for the discovery of new carbonic anhydrase VII inhibitors. Eur J Med Chem. https:\/\/doi.org\/10.1016\/j.ejmech.2013.10.071","journal-title":"Eur J Med Chem"},{"key":"499_CR18","doi-asserted-by":"publisher","DOI":"10.1152\/jappl.1987.63.5.2134","author":"SJ Dodgson","year":"1987","unstructured":"Dodgson SJ (1987) Inhibition of mitochondrial carbonic anhydrase and ureagenesis: a discrepancy examined. J Appl Physiol. https:\/\/doi.org\/10.1152\/jappl.1987.63.5.2134","journal-title":"J Appl Physiol"},{"key":"499_CR19","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejmech.2017.01.017","author":"WM Eldehna","year":"2017","unstructured":"Eldehna WM, Al-Ansary GH, Bua S et al (2017) Novel indolin-2-one-based sulfonamides as carbonic anhydrase inhibitors: synthesis, in vitro biological evaluation against carbonic anhydrases isoforms I, II, IV and VII and molecular docking studies. Eur J Med Chem. https:\/\/doi.org\/10.1016\/j.ejmech.2017.01.017","journal-title":"Eur J Med Chem"},{"key":"499_CR20","doi-asserted-by":"publisher","DOI":"10.1016\/j.bmc.2015.10.009","author":"I Fidan","year":"2015","unstructured":"Fidan I, Salmas RE, Arslan M et al (2015) Carbonic anhydrase inhibitors: Design, synthesis, kinetic, docking and molecular dynamics analysis of novel glycine and phenylalanine sulfonamide derivatives. Bioorg Med Chem. https:\/\/doi.org\/10.1016\/j.bmc.2015.10.009","journal-title":"Bioorg Med Chem"},{"key":"499_CR21","doi-asserted-by":"publisher","DOI":"10.1080\/00268976.2013.813594","author":"G Fiorin","year":"2013","unstructured":"Fiorin G, Klein ML, Henin J (2013) Using collective variables to drive molecular dynamics simulations. Mol Phys. https:\/\/doi.org\/10.1080\/00268976.2013.813594","journal-title":"Mol Phys"},{"key":"499_CR22","unstructured":"Frisch MJ, Trucks GW, Schlegel HB et al (2016) Gaussian 16 Rev. C.01 Wallingford, CT. https:\/\/gaussian.com\/"},{"key":"499_CR23","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jcim.2c00910","author":"ME Gantner","year":"2022","unstructured":"Gantner ME, Prada Gori DN, Llanos MA et al (2022) Identification of new carbonic anhydrase VII inhibitors by structure-based virtual screening. J Chem Inf Model. https:\/\/doi.org\/10.1021\/acs.jcim.2c00910","journal-title":"J Chem Inf Model"},{"key":"499_CR24","doi-asserted-by":"publisher","DOI":"10.1002\/prot.24029","author":"S Genheden","year":"2012","unstructured":"Genheden S, Ryde U (2012) Comparison of end-point continuum-solvation methods for the calculation of protein-ligand binding free energies. Proteins. https:\/\/doi.org\/10.1002\/prot.24029","journal-title":"Proteins"},{"key":"499_CR25","unstructured":"Gilbert A (2012) IQmol molecular viewer. http:\/\/iqmol.org\/"},{"key":"499_CR26","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gki464","author":"JC Gordon","year":"2005","unstructured":"Gordon JC, Myers JB, Folta T et al (2005) H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res. https:\/\/doi.org\/10.1093\/nar\/gki464","journal-title":"Nucleic Acids Res"},{"key":"499_CR27","doi-asserted-by":"publisher","DOI":"10.1021\/jm011112j","author":"S Gruneberg","year":"2002","unstructured":"Gruneberg S, Stubbs MT, Klebe G (2002) Successful virtual screening for novel inhibitors of human carbonic anhydrase: strategy and experimental confirmation. J Med Chem. https:\/\/doi.org\/10.1021\/jm011112j","journal-title":"J Med Chem"},{"key":"499_CR28","doi-asserted-by":"publisher","DOI":"10.1021\/ct200244p","author":"CR Guimaraes","year":"2011","unstructured":"Guimaraes CR (2011) A direct comparison of the MM-GB\/SA scoring procedure and free-energy perturbation calculations using carbonic anhydrase as a test case: strengths and pitfalls of each approach. J Chem Theory Comput. https:\/\/doi.org\/10.1021\/ct200244p","journal-title":"J Chem Theory Comput"},{"key":"499_CR29","doi-asserted-by":"publisher","DOI":"10.1016\/0898-5529(88)90015-2","author":"W Hasel","year":"1988","unstructured":"Hasel W, Hendrickson TF, Still WC (1988) A rapid approximation to the solvent accessible surface areas of atoms. Tetrahedron Comput Methodol. https:\/\/doi.org\/10.1016\/0898-5529(88)90015-2","journal-title":"Tetrahedron Comput Methodol"},{"key":"499_CR30","doi-asserted-by":"publisher","DOI":"10.1007\/s11426-008-0133-1","author":"H Huang","year":"2009","unstructured":"Huang H, Pan X, Ji C et al (2009) Screening and docking studies of natural phenolic inhibitors of carbonic anhydrase II. Sci Ch Ser B. https:\/\/doi.org\/10.1007\/s11426-008-0133-1","journal-title":"Sci Ch Ser B"},{"issue":"24","key":"499_CR31","doi-asserted-by":"publisher","first-page":"8692","DOI":"10.1021\/ja00180a009","volume":"112","author":"O Jacob","year":"1990","unstructured":"Jacob O, Cardenas R, Tapia O (1990) An ab initio study of transition structures and associated products in [ZnOHCO2]+,[ZnHCO3H2O]+, and [Zn(NH3)3HCO3]+ hypersurfaces. On the role of zinc in the catalytic mechanism of carbonic anhydrase. J Am Chem Soc 112(24):8692\u20138705","journal-title":"J Am Chem Soc"},{"key":"499_CR32","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jpca.2c06358","author":"Y Jiang","year":"2022","unstructured":"Jiang Y, Supuran CT, Ho J (2022) Quantum chemical prediction of the acidities of sulfonamide inhibitors of carbonic anhydrase. J Phys Chem A. https:\/\/doi.org\/10.1021\/acs.jpca.2c06358","journal-title":"J Phys Chem A"},{"issue":"1063\/1","key":"499_CR33","first-page":"445869","volume":"10","author":"WL Jorgensen","year":"1983","unstructured":"Jorgensen WL, Chandrasekhar J, Madura JD et al (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys doi 10(1063\/1):445869","journal-title":"J Chem Phys doi"},{"key":"499_CR34","doi-asserted-by":"publisher","DOI":"10.1080\/07391102.2017.1360208","author":"DS Karlov","year":"2018","unstructured":"Karlov DS, Lavrov MI, Palyulin VA et al (2018) MM-GBSA and MM-PBSA performance in activity evaluation of AMPA receptor positive allosteric modulators. J Biomol Struct Dyn. https:\/\/doi.org\/10.1080\/07391102.2017.1360208","journal-title":"J Biomol Struct Dyn"},{"key":"499_CR35","doi-asserted-by":"publisher","DOI":"10.1016\/s0378-5173(02)00438-6","author":"IP Kaur","year":"2002","unstructured":"Kaur IP, Smitha R, Aggarwal D et al (2002) Acetazolamide: future perspective in topical glaucoma therapeutics. Int J Pharm. https:\/\/doi.org\/10.1016\/s0378-5173(02)00438-6","journal-title":"Int J Pharm"},{"key":"499_CR36","doi-asserted-by":"publisher","DOI":"10.1021\/ja00017a011","author":"M Krauss","year":"1991","unstructured":"Krauss M, Garmer D (1991) Active site ionicity and the mechanism of carbonic anhydrase. J Am Chem Soc. https:\/\/doi.org\/10.1021\/ja00017a011","journal-title":"J Am Chem Soc"},{"key":"499_CR37","doi-asserted-by":"publisher","DOI":"10.1021\/cr050262p","author":"VM Krishnamurthy","year":"2008","unstructured":"Krishnamurthy VM, Kaufman GK, Urbach AR et al (2008) Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev. https:\/\/doi.org\/10.1021\/cr050262p","journal-title":"Chem Rev"},{"key":"499_CR38","doi-asserted-by":"publisher","DOI":"10.1080\/07391102.2019.1626285","author":"A Kumar","year":"2020","unstructured":"Kumar A, Rathi E, Kini SG (2020) Identification of potential tumour-associated carbonic anhydrase isozyme IX inhibitors: atom-based 3D-QSAR modelling, pharmacophore-based virtual screening and molecular docking studies. J Biomol Struct Dyn. https:\/\/doi.org\/10.1080\/07391102.2019.1626285","journal-title":"J Biomol Struct Dyn"},{"key":"499_CR39","doi-asserted-by":"publisher","DOI":"10.1021\/jp972682r","author":"JB Li","year":"1998","unstructured":"Li JB, Zhu TH, Cramer CJ et al (1998) New class IV charge model for extracting accurate partial charges from wave functions. J Phys Chem A. https:\/\/doi.org\/10.1021\/jp972682r","journal-title":"J Phys Chem A"},{"key":"499_CR40","doi-asserted-by":"publisher","DOI":"10.1021\/ct900454q","author":"F Lin","year":"2010","unstructured":"Lin F, Wang R (2010) Systematic derivation of AMBER force field parameters applicable to zinc-containing systems. J Chem Theory Comput. https:\/\/doi.org\/10.1021\/ct900454q","journal-title":"J Chem Theory Comput"},{"key":"499_CR41","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/354594","author":"C Liu","year":"2012","unstructured":"Liu C, Wei Y, Wang J et al (2012) Carbonic anhydrases III and IV autoantibodies in rheumatoid arthritis, systemic lupus erythematosus, diabetes, hypertensive renal disease, and heart failure. Clin Dev Immunol. https:\/\/doi.org\/10.1155\/2012\/354594","journal-title":"Clin Dev Immunol"},{"key":"499_CR42","doi-asserted-by":"publisher","DOI":"10.1016\/j.bmc.2016.01.019","author":"CL Lomelino","year":"2016","unstructured":"Lomelino CL, Mahon BP, McKenna R et al (2016) Kinetic and X-ray crystallographic investigations on carbonic anhydrase isoforms I, II, IX and XII of a thioureido analog of SLC-0111. Bioorg Med Chem. https:\/\/doi.org\/10.1016\/j.bmc.2016.01.019","journal-title":"Bioorg Med Chem"},{"key":"499_CR43","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-0134(19981001)33:1<119::AID-PROT11>3.0.CO;2-O","author":"DS Lu","year":"1998","unstructured":"Lu DS, Voth GA (1998) Molecular dynamics simulations of human carbonic anhydrase II: Insight into experimental results and the role of solvation. Proteins-Str Funct Genet. https:\/\/doi.org\/10.1002\/(SICI)1097-0134(19981001)33:1%3c119::AID-PROT11%3e3.0.CO;2-O","journal-title":"Proteins-Str Funct Genet"},{"key":"499_CR44","doi-asserted-by":"publisher","DOI":"10.1021\/ct300418h","author":"BR Miller 3rd","year":"2012","unstructured":"Miller BR 3rd, McGee TD Jr, Swails JM et al (2012) MMPBSA.py: an efficient program for end-state free energy calculations. J Chem Theory Comput. https:\/\/doi.org\/10.1021\/ct300418h","journal-title":"J Chem Theory Comput"},{"key":"499_CR45","doi-asserted-by":"publisher","DOI":"10.1002\/med.21713","author":"CB Mishra","year":"2020","unstructured":"Mishra CB, Tiwari M, Supuran CT (2020) Progress in the development of human carbonic anhydrase inhibitors and their pharmacological applications: Where are we today? Med Res Rev. https:\/\/doi.org\/10.1002\/med.21713","journal-title":"Med Res Rev"},{"key":"499_CR46","doi-asserted-by":"publisher","DOI":"10.1097\/COC.0000000000000691","author":"PC McDonald","year":"2020","unstructured":"McDonald PC, Chia S, Bedard PL et al (2020) A phase 1 study of SLC-0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. Am J Clin Oncol. https:\/\/doi.org\/10.1097\/COC.0000000000000691","journal-title":"Am J Clin Oncol"},{"key":"499_CR47","unstructured":"Meeko. https:\/\/github.com\/forlilab\/Meeko. Accessed 31 Jan 2022"},{"key":"499_CR48","doi-asserted-by":"publisher","DOI":"10.1002\/jcc.27052","author":"O Melse","year":"2022","unstructured":"Melse O, Antes I, Kaila VRI et al (2022) Benchmarking biomolecular force field-based Zn(2+) for mono- and bimetallic ligand binding sites. J Comput Chem. https:\/\/doi.org\/10.1002\/jcc.27052","journal-title":"J Comput Chem"},{"key":"499_CR49","doi-asserted-by":"publisher","DOI":"10.3109\/14756369909030336","author":"L Menabuoni","year":"1999","unstructured":"Menabuoni L, Scozzafava A, Mincione F et al (1999) Carbonic anhydrase inhibitors. Water-soluble, topically effective intraocular pressure lowering agents derived from isonicotinic acid and aromatic\/heterocyclic sulphonamides: is the tail more important than the ring. J Enzyme Inhib. https:\/\/doi.org\/10.3109\/14756369909030336","journal-title":"J Enzyme Inhib"},{"key":"499_CR50","doi-asserted-by":"publisher","DOI":"10.1021\/ct600085e","author":"J Mongan","year":"2007","unstructured":"Mongan J, Simmerling C, McCammon JA et al (2007) Generalized born model with a simple, robust molecular volume correction. J Chem Theory Comput. https:\/\/doi.org\/10.1021\/ct600085e","journal-title":"J Chem Theory Comput"},{"key":"499_CR51","doi-asserted-by":"publisher","DOI":"10.1002\/jcc.21256","author":"GM Morris","year":"2009","unstructured":"Morris GM, Huey R, Lindstrom W et al (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem. https:\/\/doi.org\/10.1002\/jcc.21256","journal-title":"J Comput Chem"},{"issue":"1063\/1","key":"499_CR52","first-page":"1740588","volume":"10","author":"RS Mulliken","year":"1955","unstructured":"Mulliken RS (1955) Electronic population analysis on LCAO\u2013MO molecular wave functions. I J Chem Phys doi 10(1063\/1):1740588","journal-title":"I J Chem Phys doi"},{"key":"499_CR53","doi-asserted-by":"publisher","DOI":"10.1039\/c0cc02707c","author":"F Pacchiano","year":"2010","unstructured":"Pacchiano F, Aggarwal M, Avvaru BS et al (2010) Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Chem Commun (Camb). https:\/\/doi.org\/10.1039\/c0cc02707c","journal-title":"Chem Commun (Camb)"},{"key":"499_CR54","doi-asserted-by":"publisher","DOI":"10.1021\/jm101541x","author":"F Pacchiano","year":"2011","unstructured":"Pacchiano F, Carta F, McDonald PC et al (2011) Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem. https:\/\/doi.org\/10.1021\/jm101541x","journal-title":"J Med Chem"},{"key":"499_CR55","doi-asserted-by":"publisher","DOI":"10.1002\/jcc.20289","author":"JC Phillips","year":"2005","unstructured":"Phillips JC, Braun R, Wang W et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem. https:\/\/doi.org\/10.1002\/jcc.20289","journal-title":"J Comput Chem"},{"issue":"1063\/5","key":"499_CR56","first-page":"0014475","volume":"10","author":"JC Phillips","year":"2020","unstructured":"Phillips JC, Hardy DJ, Maia JDC et al (2020) Scalable molecular dynamics on CPU and GPU architectures with NAMD. J Chem Phys doi 10(1063\/5):0014475","journal-title":"J Chem Phys doi"},{"key":"499_CR57","doi-asserted-by":"publisher","DOI":"10.1016\/j.bmc.2013.08.033","author":"MA Pinard","year":"2013","unstructured":"Pinard MA, Boone CD, Rife BD et al (2013) Structural study of interaction between brinzolamide and dorzolamide inhibition of human carbonic anhydrases. Bioorg Med Chem. https:\/\/doi.org\/10.1016\/j.bmc.2013.08.033","journal-title":"Bioorg Med Chem"},{"key":"499_CR58","doi-asserted-by":"publisher","DOI":"10.1155\/2015\/453543","author":"MA Pinard","year":"2015","unstructured":"Pinard MA, Mahon B, McKenna R (2015) Probing the surface of human carbonic anhydrase for clues towards the design of isoform specific inhibitors. Biomed Res Int. https:\/\/doi.org\/10.1155\/2015\/453543","journal-title":"Biomed Res Int"},{"key":"499_CR59","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jctc.1c00071","author":"A Plazinska","year":"2021","unstructured":"Plazinska A, Plazinski W (2021) Comparison of carbohydrate force fields in molecular dynamics simulations of protein-carbohydrate complexes. J Chem Theory Comput. https:\/\/doi.org\/10.1021\/acs.jctc.1c00071","journal-title":"J Chem Theory Comput"},{"issue":"1063\/1","key":"499_CR60","first-page":"449486","volume":"10","author":"AE Reed","year":"1985","unstructured":"Reed AE, Weinstock RB, Weinhold F (1985) Natural population analysis. J Chem Phys doi 10(1063\/1):449486","journal-title":"J Chem Phys doi"},{"key":"499_CR61","doi-asserted-by":"publisher","DOI":"10.1177\/106002809603000515","author":"WG Reiss","year":"1996","unstructured":"Reiss WG, Oles KS (1996) Acetazolamide in the treatment of seizures. Ann Pharmacother. https:\/\/doi.org\/10.1177\/106002809603000515","journal-title":"Ann Pharmacother"},{"key":"499_CR62","doi-asserted-by":"publisher","DOI":"10.1021\/jm00012a005","author":"KA Rossi","year":"1995","unstructured":"Rossi KA, Merz KM Jr, Smith GM et al (1995) Application of the free energy perturbation method to human carbonic anhydrase II inhibitors. J Med Chem. https:\/\/doi.org\/10.1021\/jm00012a005","journal-title":"J Med Chem"},{"key":"499_CR63","doi-asserted-by":"publisher","DOI":"10.1016\/j.bioorg.2019.103153","author":"BN Saglik","year":"2019","unstructured":"Saglik BN, Cevik UA, Osmaniye D et al (2019) Synthesis, molecular docking analysis and carbonic anhydrase I-II inhibitory evaluation of new sulfonamide derivatives. Bioorg Chem. https:\/\/doi.org\/10.1016\/j.bioorg.2019.103153","journal-title":"Bioorg Chem"},{"key":"499_CR64","doi-asserted-by":"publisher","DOI":"10.1021\/ci500209e","author":"D Santos-Martins","year":"2014","unstructured":"Santos-Martins D, Forli S, Ramos MJ et al (2014) AutoDock4(Zn): an improved AutoDock force field for small-molecule docking to zinc metalloproteins. J Chem Inf Model. https:\/\/doi.org\/10.1021\/ci500209e","journal-title":"J Chem Inf Model"},{"key":"499_CR65","doi-asserted-by":"publisher","DOI":"10.1039\/c1sc00628b","author":"M Schmid","year":"2012","unstructured":"Schmid M, Nogueira ES, Monnard FW et al (2012) Arylsulfonamides as inhibitors for carbonic anhydrase: prediction & validation. Chem Sci. https:\/\/doi.org\/10.1039\/c1sc00628b","journal-title":"Chem Sci"},{"key":"499_CR66","doi-asserted-by":"publisher","DOI":"10.1002\/jcc.540050204","author":"UC Singh","year":"1984","unstructured":"Singh UC, Kollman PA (1984) An approach to computing electrostatic charges for molecules. J Comput Chem. https:\/\/doi.org\/10.1002\/jcc.540050204","journal-title":"J Comput Chem"},{"key":"499_CR67","doi-asserted-by":"publisher","DOI":"10.1002\/prot.340230104","author":"RH Stote","year":"1995","unstructured":"Stote RH, Karplus M (1995) Zinc binding in proteins and solution: a simple but accurate nonbonded representation. Proteins. https:\/\/doi.org\/10.1002\/prot.340230104","journal-title":"Proteins"},{"key":"499_CR68","doi-asserted-by":"publisher","DOI":"10.2174\/138161208783877884","author":"CT Supuran","year":"2008","unstructured":"Supuran CT (2008) Carbonic anhydrases - an overview. Curr Pharm Des. https:\/\/doi.org\/10.2174\/138161208783877884","journal-title":"Curr Pharm Des"},{"key":"499_CR69","doi-asserted-by":"publisher","DOI":"10.1517\/14728214.2012.664132","author":"CT Supuran","year":"2012","unstructured":"Supuran CT (2012) Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin Emerg Drugs. https:\/\/doi.org\/10.1517\/14728214.2012.664132","journal-title":"Expert Opin Emerg Drugs"},{"key":"499_CR70","doi-asserted-by":"publisher","DOI":"10.3109\/14756366.2015.1122001","author":"CT Supuran","year":"2016","unstructured":"Supuran CT (2016) How many carbonic anhydrase inhibition mechanisms exist\u202f? J Enzyme Inhib Med Chem. https:\/\/doi.org\/10.3109\/14756366.2015.1122001","journal-title":"J Enzyme Inhib Med Chem"},{"key":"499_CR71","doi-asserted-by":"publisher","DOI":"10.1021\/jm501798g","author":"RP Tanpure","year":"2015","unstructured":"Tanpure RP, Ren B, Peat TS et al (2015) Carbonic anhydrase inhibitors with dual-tail moieties to match the hydrophobic and hydrophilic halves of the carbonic anhydrase active site. J Med Chem. https:\/\/doi.org\/10.1021\/jm501798g","journal-title":"J Med Chem"},{"key":"499_CR72","doi-asserted-by":"publisher","DOI":"10.1016\/j.bioorg.2019.02.013","author":"F Turkan","year":"2019","unstructured":"Turkan F, Cetin A, Taslimi P et al (2019) Synthesis, biological evaluation and molecular docking of novel pyrazole derivatives as potent carbonic anhydrase and acetylcholinesterase inhibitors. Bioorg Chem. https:\/\/doi.org\/10.1016\/j.bioorg.2019.02.013","journal-title":"Bioorg Chem"},{"key":"499_CR73","doi-asserted-by":"publisher","DOI":"10.1002\/jcc.21367","author":"K Vanommeslaeghe","year":"2010","unstructured":"Vanommeslaeghe K, Hatcher E, Acharya C et al (2010) CHARMM general force field: a force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem. https:\/\/doi.org\/10.1002\/jcc.21367","journal-title":"J Comput Chem"},{"key":"499_CR74","doi-asserted-by":"publisher","DOI":"10.1021\/ci300363c","author":"K Vanommeslaeghe","year":"2012","unstructured":"Vanommeslaeghe K, MacKerell AD Jr (2012) Automation of the CHARMM General Force Field (CGenFF) I: bond perception and atom typing. J Chem Inf Model. https:\/\/doi.org\/10.1021\/ci300363c","journal-title":"J Chem Inf Model"},{"key":"499_CR75","doi-asserted-by":"publisher","DOI":"10.1021\/ci3003649","author":"K Vanommeslaeghe","year":"2012","unstructured":"Vanommeslaeghe K, Raman EP, MacKerell AD Jr (2012) Automation of the CHARMM General Force Field (CGenFF) II: assignment of bonded parameters and partial atomic charges. J Chem Inf Model. https:\/\/doi.org\/10.1021\/ci3003649","journal-title":"J Chem Inf Model"},{"key":"499_CR76","doi-asserted-by":"publisher","DOI":"10.1016\/0141-8130(90)90040-h","author":"J Vidgren","year":"1990","unstructured":"Vidgren J, Liljas A, Walker NP (1990) Refined structure of the acetazolamide complex of human carbonic anhydrase II at 1.9 A. Int J Biol Macromol. https:\/\/doi.org\/10.1016\/0141-8130(90)90040-h","journal-title":"Int J Biol Macromol"},{"key":"499_CR77","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpc.2016.05.006","author":"TO Wambo","year":"2016","unstructured":"Wambo TO, Chen LY, McHardy SF et al (2016) Molecular dynamics study of human carbonic anhydrase II in complex with Zn(2+) and acetazolamide on the basis of all-atom force field simulations. Biophys Chem. https:\/\/doi.org\/10.1016\/j.bpc.2016.05.006","journal-title":"Biophys Chem"},{"key":"499_CR78","doi-asserted-by":"publisher","DOI":"10.1021\/acs.chemrev.9b00055","author":"E Wang","year":"2019","unstructured":"Wang E, Sun H, Wang J et al (2019) end-point binding free energy calculation with MM\/PBSA and MM\/GBSA: strategies and applications in drug design. Chem Rev. https:\/\/doi.org\/10.1021\/acs.chemrev.9b00055","journal-title":"Chem Rev"},{"key":"499_CR79","doi-asserted-by":"publisher","DOI":"10.1021\/jp404160y","author":"L Xu","year":"2013","unstructured":"Xu L, Sun H, Li Y et al (2013) Assessing the performance of MM\/PBSA and MM\/GBSA methods. 3. The impact of force fields and ligand charge models. J Phys Chem B. https:\/\/doi.org\/10.1021\/jp404160y","journal-title":"J Phys Chem B"},{"issue":"1063\/1","key":"499_CR80","first-page":"465608","volume":"10","author":"DM York","year":"1993","unstructured":"York DM, Darden TA, Pedersen LG (1993) The effect of long-range electrostatic interactions in simulations of macromolecular crystals: a comparison of the Ewald and truncated list methods. J Chem Phys doi 10(1063\/1):465608","journal-title":"J Chem Phys doi"},{"key":"499_CR81","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21207562","author":"S Zhao","year":"2020","unstructured":"Zhao S, Ni F, Qiu T et al (2020) Molecular basis for polyketide ketoreductase\u2013substrate interactions. Int J Mol Sci. https:\/\/doi.org\/10.3390\/ijms21207562","journal-title":"Int J Mol Sci"}],"container-title":["Journal of Computer-Aided Molecular Design"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10822-023-00499-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10822-023-00499-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10822-023-00499-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,28]],"date-time":"2023-03-28T06:07:58Z","timestamp":1679983678000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10822-023-00499-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,17]]},"references-count":81,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2023,4]]}},"alternative-id":["499"],"URL":"https:\/\/doi.org\/10.1007\/s10822-023-00499-0","relation":{},"ISSN":["0920-654X","1573-4951"],"issn-type":[{"value":"0920-654X","type":"print"},{"value":"1573-4951","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,17]]},"assertion":[{"value":"10 January 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 February 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 March 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interest"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"All authors have reviewed the paper and consent to its publication.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"Not applicable.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}}]}}