227
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Golgi α-mannosidase: opposing structures of Drosophila melanogaster and novel human model using molecular dynamics simulations and docking at different pHs

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 2714-2725 | Received 02 Feb 2023, Accepted 19 Apr 2023, Published online: 09 May 2023

References

  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of Protein Database Search Programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389
  • Armstrong, Z., Kuo, C.-L., Lahav, D., Liu, B., Johnson, R., Beenakker, T. J. M., de Boer, C., Wong, C.-S., van Rijssel, E. R., Debets, M. F., Florea, B. I., Hissink, C., Boot, R. G., Geurink, P. P., Ovaa, H., van der Stelt, M., van der Marel, G. M., Codée, J. D. C., Aerts, J. M. F. G., … Davies, G. J. (2020). Manno-Epi-Cyclophellitols enable activity-based protein profiling of human α-mannosidases and discovery of new Golgi Mannosidase II inhibitors. Journal of the American Chemical Society, 142(30), 13021–13029. https://doi.org/10.1021/jacs.0c03880
  • Ashida, H., Kato, T., & Yamamoto, K. (2007). 3.09 - Degradation of Glycoproteins. In H. Kamerling (Ed.) Comprehensive glycoscience (pp. 151–170). Elsevier. https://doi.org/10.1016/B978-044451967-2/00042-8
  • Becke, A. D. (1993a). Density-functional thermochemistry. III. The role of exact exchange. Journal of Chemical Physics, 98(7), 5648–5652. https://doi.org/10.1063/1.464913
  • Becke, A. D. (1993b). A New Mixing of Hartree-Fock and Local Density‐functional Theories. Journal of Chemical Physics. 98(2), 1372–1377. https://doi.org/10.1063/1.464304
  • Castro, T. G., Munteanu, F.-D., & Cavaco-Paulo, A. (2019). Electrostatics of Tau Protein by molecular dynamics. Biomolecules, 9(3), 116. https://doi.org/10.3390/biom9030116
  • Chen, W., Sayyad, A., Chen, C., Chen, Y., Cheng, T. R., & Cheng, W. (2019). Divergent synthesis of bicyclic iminosugars: Preparation of (−)‐Swainsonine‐based alkaloids and their inhibition study towards α ‐human mannosidases. Asian Journal of Organic Chemistry, 8(12), 2233–2242. https://doi.org/10.1002/ajoc.201900637
  • Ciccotti, G., Dellago, C., Ferrario, M., Hernández, E. R., & Tuckerman, M. E. (2022). Molecular simulations: Past, present, and future (a Topical Issue in EPJB). The European Physical Journal B, 95(1), 3. https://doi.org/10.1140/epjb/s10051-021-00249-x
  • Deschamps, A., Colinet, A.-S., Zimmermannova, O., Sychrova, H., & Morsomme, P. (2020). A new PH sensor localized in the Golgi apparatus of Saccharomyces cerevisiae reveals unexpected roles of Vph1p and Stv1p isoforms. Scientific Reports, 10(1), 1881. https://doi.org/10.1038/s41598-020-58795-w
  • Ditchfield, R., Hehre, W. J., & Pople, J. A. (1971). Self‐consistent molecular‐orbital methods. IX. An extended Gaussian‐type basis for molecular‐orbital studies of organic molecules. Journal of Chemical Physics. 54(2), 724–728. https://doi.org/10.1063/1.1674902
  • Dube, D. H., & Bertozzi, C. R. (2005). Glycans in cancer and inflammation—Potential for therapeutics and diagnostics. Nature Reviews. Drug Discovery, 4(6), 477–488. https://doi.org/10.1038/nrd1751
  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., et al. (2009). Gaussian09. Gaussian, Inc.
  • Futerman, A. H., Stieger, B., Hubbard, A. L., & Pagano, R. E. (1990). Sphingomyelin synthesis in rat liver occurs predominantly at the Cis and medial cisternae of the Golgi Apparatus. The Journal of Biological Chemistry, 265(15), 8650–8657. https://doi.org/10.1016/S0021-9258(19)38937-9
  • Goss, P. E., Baker, M. A., Carver, J. P., & Dennis, J. W. (1995). Inhibitors of carbohydrate processing: A new class of anticancer agents. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 1(9), 935–944.
  • Goss, P. E., Reid, C. L., Bailey, D., & Dennis, J. W. (1997). Phase IB clinical trial of the oligosaccharide processing inhibitor Swainsonine in patients with advanced malignancies. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 3(7), 1077–1086.
  • Hariharan, P. C., & Pople, J. A. (1974). Accuracy of AH n equilibrium geometries by single determinant molecular orbital theory. Molecular Physics, 27(1), 209–214. https://doi.org/10.1080/00268977400100171
  • Hohenberg, P., & Kohn, W. (1964). Inhomogeneous electron gas. Physical Review, 136(3B), B864–B871. https://doi.org/10.1103/PhysRev.136.B864
  • Jurrus, E., Engel, D., Star, K., Monson, K., Brandi, J., Felberg, L. E., Brookes, D. H., Wilson, L., Chen, J., Liles, K., Chun, M., Li, P., Gohara, D. W., Dolinsky, T., Konecny, R., Koes, D. R., Nielsen, J. E., Head-Gordon, T., Geng, W., … Baker, N. A. (2018). Improvements to the APBS Biomolecular Solvation Software Suite. Protein Science : A Publication of the Protein Society, 27(1), 112–128. https://doi.org/10.1002/pro.3280
  • Kalník, M., Šesták, S., Kóňa, J., Bella, M., & Poláková, M. (2023). Synthesis, α-Mannosidase inhibition studies and molecular modeling of 1,4-imino-d-lyxitols and their C-5-altered N-arylalkyl derivatives. Beilstein Journal of Organic Chemistry, 19(March), 282–293. https://doi.org/10.3762/bjoc.19.24
  • Kang, M. S., & Elbein, A. D. (1983). Mechanism of inhibition of Jack Bean α-mannosidase by swainsonine. Plant Physiology, 71(3), 551–554. https://doi.org/10.1104/pp.71.3.551
  • Kavlekar, L. M., Kuntz, D. A., Wen, X., Johnston, B. D., Svensson, B., Rose, D. R., & Pinto, B. M. (2005). 5-Thio-d-glycopyranosylamines and their amidinium salts as potential transition-state mimics of glycosyl hydrolases: Synthesis, enzyme inhibitory activities, X-ray crystallography, and molecular modeling. Tetrahedron: Asymmetry, 16(5), 1035–1046. https://doi.org/10.1016/j.tetasy.2005.01.021
  • Klunda, T., Hricovíni, M., Šesták, S., Kóňa, J., & Poláková, M. (2021). Selective Golgi α-mannosidase II inhibitors: N-Alkyl substituted pyrrolidines with a basic functional group. New Journal of Chemistry, 45(24), 10940–10951. https://doi.org/10.1039/D1NJ01176F
  • Klunda, T., Šesták, S., Kóňa, J., & Poláková, M. (2019). Synthesis of N-benzyl substituted 1,4-imino-l-lyxitols with a basic functional group as selective inhibitors of Golgi α-Mannosidase IIb. Bioorganic Chemistry, 83(March), 424–431. https://doi.org/10.1016/j.bioorg.2018.10.066
  • Kóňa, J., Šesták, S., Wilson, I. B. H., & Poláková, M. (2022). 1,4-Dideoxy-1,4-imino- d - and l -lyxitol-based inhibitors bind to Golgi α-mannosidase II in different protonation forms. Organic & Biomolecular Chemistry, 20(45), 8932–8943. https://doi.org/10.1039/D2OB01545E
  • Koyama, R., Kano, Y., Kikushima, K., Mizutani, A., Soeda, Y., Miura, K., Hirano, T., Nishio, T., & Hakamata, W. (2020). A novel Golgi mannosidase inhibitor: Molecular design, synthesis, enzyme inhibition, and inhibition of spheroid formation. Bioorganic & Medicinal Chemistry, 28(11), 115492. https://doi.org/10.1016/j.bmc.2020.115492
  • Kuntz, D. A., & Rose, D. R. Crystal structure of Golgi Mannosidase II in complex with swainsonine at 1.3 Angstrom resolution. https://doi.org/10.2210/pdb3blb/pdb
  • Kuntz, D. A., Ghavami, A., Johnston, B. D., Pinto, B. M., & Rose, D. R. (2005). Crystallographic analysis of the interactions of Drosophila Melanogaster Golgi α-Mannosidase II with the naturally occurring Glycomimetic salacinol and its analogues. Tetrahedron: Asymmetry, Carbohydrate Science. Part 1, 16(1), 25–32. https://doi.org/10.1016/j.tetasy.2004.11.057
  • Laskowski, R. A., & Swindells, M. B. (2011). LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. Journal of Chemical Information and Modeling, 51(10), 2778–2786. https://doi.org/10.1021/ci200227u
  • Lee, Z. Y., Loo, J. S. E., Wibowo, A., Mohammat, M. F., & Foo, J. B. (2021). Targeting cancer via Golgi α-Mannosidase II inhibition: How far have we come in developing effective inhibitors? Carbohydrate Research, 508(October), 108395. https://doi.org/10.1016/j.carres.2021.108395
  • Li, B., Kawatkar, S. P., George, S., Strachan, H., Woods, R. J., Siriwardena, A., Moremen, K. W., & Boons, G.-J. (2004). Inhibition of Golgi Mannosidase II with Mannostatin A analogues: Synthesis, biological evaluation, and structure–activity relationship studies. Chembiochem : A European Journal of Chemical Biology, 5(9), 1220–1227. https://doi.org/10.1002/cbic.200300842
  • Li, C., Guo, L., Chen, F., Yu, W., Rao, T., & Ruan, Y. (2020). Golgi Alpha-Mannosidase II as a novel biomarker predicts prognosis in clear cell renal cell carcinoma. Oncology Research and Treatment, 43(6), 264–275. https://doi.org/10.1159/000505931
  • Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., & Henrissat, B. (2014). The Carbohydrate-Active Enzymes Database (CAZy) in 2013. Nucleic Acids Research, 42(Database issue), D490–D495. https://doi.org/10.1093/nar/gkt1178
  • Mahtarin, R., Islam, S., Jahirul Islam, M., Ullah, M. O., Ali, M. A., & Halim, M. A. (2022). Structure and dynamics of membrane protein in SARS-CoV-2. Journal of Biomolecular Structure & Dynamics, 40(10), 4725–4738. https://doi.org/10.1080/07391102.2020.1861983
  • Mane, R. S., Ghosh, S., Singh, S., Chopade, B. A., & Dhavale, D. D. (2011). Synthesis of anomeric 1,5-anhydrosugars as conformationally locked selective α-mannosidase inhibitors. Bioorganic & Medicinal Chemistry, 19(22), 6720–6725. https://doi.org/10.1016/j.bmc.2011.09.046
  • McCarter, J. D., & Withers, S. G. (1994). Mechanisms of enzymatic glycoside hydrolysis. Current Opinion in Structural Biology, 4(6), 885–892. https://doi.org/10.1016/0959-440x(94)90271-2
  • Navyashree, V., Kant, K., & Kumar, A. (2021). Natural chemical entities from Arisaema Genus might be a promising break-through against Japanese encephalitis virus infection: A molecular docking and dynamics approach. Journal of Biomolecular Structure & Dynamics, 39(4), 1404–1416. https://doi.org/10.1080/07391102.2020.1731603
  • O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open babel: An open chemical toolbox. Journal of Cheminformatics, 3(1), 33. https://doi.org/10.1186/1758-2946-3-33
  • Paciotti, S., Codini, M., Tasegian, A., Ceccarini, M. R., Cataldi, S., Arcuri, C., Fioretti, B., Albi, E., & Beccari, T. (2017). Lysosomal alpha-mannosidase and alpha-mannosidosis. Frontiers in Bioscience (Landmark Edition), 22(1), 157–167. https://doi.org/10.2741/4478
  • Pearce, R., & Zhang, Y. (2021). Deep learning techniques have significantly impacted protein structure prediction and protein design. Current Opinion in Structural Biology, 68(June), 194–207. https://doi.org/10.1016/j.sbi.2021.01.007
  • Poláková, M., Horák, R., Šesták, S., & Holková, I. (2016). Synthesis of modified D-mannose core derivatives and their impact on GH38 α-mannosidases. Carbohydrate Research, 428(June), 62–71. https://doi.org/10.1016/j.carres.2016.04.004
  • PyMOL. The PyMOL molecular graphics system, Version 2.0, 2017. Schrödinger, LLC.
  • Rassolov, V. A., Ratner, M. A., Pople, J. A., Redfern, P. C., & Curtiss, L. (2001). 6‐31G* Basis Set for third-row atoms. Journal of Computational Chemistry, 22(9), 976–984. https://doi.org/10.1002/jcc.1058
  • Ravindranath, P. A., Forli, S., Goodsell, D. S., Olson, A. J., & Sanner, M. F. (2015). AutoDockFR: Advances in protein-ligand docking with explicitly specified binding site flexibility. PLoS Computational Biology, 11(12), e1004586. https://doi.org/10.1371/journal.pcbi.1004586
  • Rose, D. R. (2012). Structure, mechanism and inhibition of Golgi α-mannosidase II. Current Opinion in Structural Biology, 22(5), 558–562. https://doi.org/10.1016/j.sbi.2012.06.005
  • Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols, 5(4), 725–738. https://doi.org/10.1038/nprot.2010.5
  • Salimi, A., Lim, J. H., Jang, J. H., & Lee, J. Y. (2022). The use of machine learning modeling, virtual screening, molecular docking, and molecular dynamics simulations to identify potential VEGFR2 kinase inhibitors. Scientific Reports, 12(1), 18825. https://doi.org/10.1038/s41598-022-22992-6
  • Schmid, N., Eichenberger, A. P., Choutko, A., Riniker, S., Winger, M., Mark, A. E., & van Gunsteren, W. F. (2011). Definition and testing of the GROMOS force-field versions 54A7 and 54B7. European Biophysics Journal : EBJ, 40(7), 843–856. https://doi.org/10.1007/s00249-011-0700-9
  • Sethi, A., Joshi, K., Sasikala, K., Alvala, M., Sethi, A., Joshi, K., Sasikala, K., & Alvala, M. (2019). Molecular Docking in Modern Drug Discovery: Principles and Recent Applications. Drug Discovery and Development - New Advances. IntechOpen. https://doi.org/10.5772/intechopen.85991
  • Shah, N., Kuntz, D. A., & Rose, D. R. (2003). Comparison of kifunensine and 1-deoxymannojirimycin binding to class I and II α-mannosidases demonstrates different saccharide distortions in inverting and retaining catalytic mechanisms. Biochemistry, 42(47), 13812–13816. https://doi.org/10.1021/bi034742r
  • Shah, N., Kuntz, D. A., & Rose, D. R. (2008). Golgi α-mannosidase II cleaves two sugars sequentially in the same catalytic site. Proceedings of the National Academy of Sciences of the United States of America, 105(28), 9570–9575. https://doi.org/10.1073/pnas.0802206105
  • Spoel, D., Van Der, E., Lindahl, B., Hess, G., Groenhof, A. E., Mark, H. J., & Berendsen, C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
  • Tirado-Rives, J., & Jorgensen, W. L. (2008). Performance of B3LYP density functional methods for a large set of organic molecules. Journal of Chemical Theory and Computation, 4(2), 297–306. https://doi.org/10.1021/ct700248k
  • Tripathi, A., & Misra, K. (2017). Molecular docking: A structure-based drug designing approach. JSM Chem, 5(2), 1042
  • UniProt Consortium. (2018). UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47(D1), D506–D515. https://doi.org/10.1093/nar/gky1049
  • van den Berg, R. J. B. H. N., Wennekes, T., Ghisaidoobe, A., Donker-Koopman, W. E., Strijland, A., Boot, R. G., van der Marel, G. A., Aerts, J. M. F. G., & Overkleeft, H. S. (2011). Assessment of partially deoxygenated deoxynojirimycin derivatives as glucosylceramide synthase inhibitors. ACS Medicinal Chemistry Letters, 2(7), 519–522. https://doi.org/10.1021/ml200050s
  • van den Elsen, J. M., Kuntz, D. A., & Rose, D. R. (2001). Structure of Golgi α-Mannosidase II: A target for inhibition of growth and metastasis of cancer cells. The EMBO Journal, 20(12), 3008–3017. https://doi.org/10.1093/emboj/20.12.3008
  • Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER suite: Protein structure and function prediction. Nature Methods, 12(1), 7–8. https://doi.org/10.1038/nmeth.3213
  • Yuriev, E., Agostino, M., & Ramsland, P. A. (2011). Challenges and advances in computational docking: 2009 in review. Journal of Molecular Recognition : JMR, 24(2), 149–164. https://doi.org/10.1002/jmr.1077
  • Zhang, C., Mortuza, S. M., He, B., Wang, Y., & Zhang, Y. (2018). Template-based and free modeling of I-TASSER and QUARK pipelines using predicted contact maps in CASP12. Proteins: Structure, Function, and Bioinformatics, 86(S1), 136–151. https://doi.org/10.1002/prot.25414
  • Zhang, X. (2021). Alterations of Golgi structural proteins and glycosylation defects in cancer. Frontiers in Cell and Developmental Biology, 9, 665289. https://doi.org/10.3389/fcell.2021.665289
  • Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. https://doi.org/10.1186/1471-2105-9-40
  • Zhang, Y., Forli, S., Omelchenko, A., & Sanner, M. F. (2019). AutoGridFR: Improvements on AutoDock affinity maps and associated software tools. Journal of Computational Chemistry, 40(32), 2882–2886. https://doi.org/10.1002/jcc.26054
  • Zheng, W., Li, Y., Zhang, C., Zhou, X., Pearce, R., Bell, E. W., Huang, X., & Zhang, Y. (2021). Protein structure prediction using deep learning distance and hydrogen-bonding restraints in CASP14. Proteins, 89(12), 1734–1751. https://doi.org/10.1002/prot.26193
  • Zheng, W., Zhang, C., Li, Y., Pearce, R., Bell, E. W., & Zhang, Y. (2021). Folding non-homologous proteins by coupling deep-learning contact maps with I-TASSER assembly simulations. Cell Reports Methods, 1(3), 100014. https://doi.org/10.1016/j.crmeth.2021.100014

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.