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Research Articles

Identification of dual active sites in Caenorhabditis elegans GANA-1 protein: an ortholog of the human α-GAL a and α-NAGA enzymes

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Pages 5261-5276 | Received 27 Jan 2022, Accepted 24 May 2022, Published online: 11 Jun 2022

References

  • Asfaw, B., Ledvinová, J., Dobrovolńy, R., Bakker, H.D., Desnick, R.J., Van Diggelen, O.P., De Jong, J.G., Kanzaki, T., Chabas, A., Maire, I. and Conzelmann, E. (2002). Defects in degradation of blood group A and B glycosphingolipids in Schindler and Fabry diseases. Journal of lipid research, 43(7), 1096–1104. https://doi.org/10.1194/jlr.m100423-jlr200
  • Azevedo, O.,Gal, A.,Faria, R.,Gaspar, P.,Miltenberger-Miltenyi, G.,Gago, M. F.,Dias, F.,Martins, A.,Rodrigues, J.,Reimão, P.,Pereira, O.,Simões, S.,Lopes, E.,Guimarães, M. J.,Sousa, N., &Cunha, D. (2020). Founder effect of Fabry disease due to p.F113L mutation: Clinical profile of a late-onset phenotype. Molecular Genetics and Metabolism, 129(2), 150–160. https://doi.org/10.1016/j.ymgme.2019.07.012
  • Bateman, A. (2004). The Pfam protein families database. Nucleic Acids Research, 32(90001), 138D–1141. https://doi.org/10.1093/nar/gkh121
  • Benkert, P.,Tosatto, S. C. E., &Schomburg, D. (2008). QMEAN: A comprehensive scoring function for model quality assessment. Proteins, 71(1), 261–277. https://doi.org/10.1002/prot.21715 17932912
  • Benkert, P.,Biasini, M., &Schwede, T. (2011). Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics (Oxford, England), 27(3), 343–350. https://doi.org/10.1093/bioinformatics/btq662 21134891
  • Bhaskaran, S., Butler, J. A., Becerra, S., Fassio, V., Girotti, M., & Rea, S. L. (2011). Breaking Caenorhabditis elegans the easy way using the Balch homogenizer: An old tool for a new application. Analytical Biochemistry, 413(2), 123–132. https://doi.org/10.1016/j.ab.2011.02.029
  • Binkowski, T.,Adamian, L., &Liang, J. (2003). Inferring Functional Relationships of Proteins from Local Sequence and Spatial Surface Patterns. Journal of Molecular Biology, 332(2), 505–526. https://doi.org/10.1016/S0022-2836(03)00882-9
  • Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics Society of America, 77(1), 71–94. Retrieved 11 July 11, 2019, from http://www.ncbi.nlm.nih.gov/pubmed/4366476. https://doi.org/10.1093/genetics/77.1.71
  • Clark, N. E., &Garman, S. C. (2009). The 1.9 a structure of human alpha-N-acetylgalactosaminidase: The molecular basis of Schindler and Kanzaki diseases. Journal of Molecular Biology, 393(2), 435–447. https://doi.org/10.1016/j.jmb.2009.08.021 19683538
  • Clark, N. E., Metcalf, M. C., Best, D., Fleet, G. W. J., & Garman, S. C. (2012). Pharmacological chaperones for human α-N-acetylgalactosaminidase. Proceedings of the National Academy of Sciences of the United States of America, 109(43), 17400–17405. https://doi.org/10.1073/pnas.1203924109
  • Clifford, A., &Donald, R. Understanding HIV/AIDS Management and Care- Pandemic Approaches in the 21st Century. InTech (2011). Glycosphingolipids in HIV/AIDS: The Potential Therapeutic Application.
  • De Voer, G.,Peters, D., &Taschner, P. E. M. (2008). Caenorhabditis elegans as a model for lysosomal storage disorders. Biochimica Et Biophysica Acta, 1782(7-8), 433–446. https://doi.org/10.1016/j.bbadis.2008.04.003 18501720
  • Delahaye, J. L.,Foster, O. K.,Vine, A.,Saxton, D. S.,Curtin, T. P.,Somhegyi, H.,Salesky, R., &Hermann, G. J. (2014). Caenorhabditis elegans HOPS and CCZ-1 mediate trafficking to lysosome-related organelles independently of RAB-7 and SAND-1. Molecular Biology of the Cell, 25(7), 1073–1096. https://doi.org/10.1091/mbc.E13-09-0521 24501423
  • Do, H.-S.,Park, S.-W.,Im, I.,Seo, D.,Yoo, H.-W.,Go, H.,Kim, Y. H.,Koh, G. Y.,Lee, B.-H., &Han, Y.-M. (2020). Enhanced thrombospondin-1 causes dysfunction of vascular endothelial cells derived from Fabry disease-induced pluripotent stem cells. EBioMedicine, 52, 102633https://doi.org/10.1016/j.ebiom.2020.102633 31981984
  • Eisenberg, D.,Lüthy, R., &Bowie, J. U. (1997). VERIFY3D: Assessment of protein models with three-dimensional profiles. Methods in Enzymology, 277, 396–404.
  • Ferri, L.,Malesci, D.,Fioravanti, A.,Bagordo, G.,Filippini, A.,Ficcadenti, A.,Manna, R.,Antuzzi, D.,Verrecchia, E.,Donati, I.,Mignani, R.,Cavicchi, C.,Guerrini, R., &Morrone, A. (2018). Functional and pharmacological evaluation of novel GLA variants in Fabry disease identifies six (two de novo ) causative mutations and two amenable variants to the chaperone DGJ. Clinica Chimica Acta, 481, 25–33. https://doi.org/10.1016/j.cca.2018.02.021
  • Garman, S. C., &Garboczi, D. N. (2004). The molecular defect leading to Fabry disease: structure of human alpha-galactosidase. Journal of Molecular Biology, 337(2), 319–335. https://doi.org/10.1016/j.jmb.2004.01.035 15003450
  • Godlewska, M., & Banga, P. J. (2019). Thyroid peroxidase as a dual active site enzyme: Focus on biosynthesis, hormonogenesis and thyroid disorders of autoimmunity and cancer. Biochimie, 160, 34–45. https://doi.org/10.1016/j.biochi.2019.02.003
  • Grasso, G., Di Gregorio, A., Mavkov, B., Piga, D., Labate, G. F. D., Danani, A., & Deriu, M. A. (2021). Fragmented blind docking: A novel protein–ligand binding prediction protocol. Journal of Biomolecular Structure and Dynamics, 1–10. https://doi.org/10.1080/07391102.2021.1988709
  • Guce, A. I.,Clark, N. E.,Salgado, E. N.,Ivanen, D. R.,Kulminskaya, A. A.,Brumer, H., &Garman, S. C. (2010). Catalytic Mechanism of Human α-Galactosidase. Journal of Biological Chemistry, 285(6), 3625–3632. https://doi.org/10.1074/jbc.M109.060145
  • Guérard, N.,Morand, O., &Dingemanse, J. (2017). Lucerastat, an iminosugar with potential as substrate reduction therapy for glycolipid storage disorders: safety, tolerability, and pharmacokinetics in healthy subjects. Orphanet Journal of Rare Diseases, 12(1), 9https://doi.org/10.1186/s13023-017-0565-9 28088251
  • Guérard, N.,Oder, D.,Nordbeck, P.,Zwingelstein, C.,Morand, O.,Welford, R. W. D.,Dingemanse, J., &Wanner, C. (2018). Lucerastat, an Iminosugar for Substrate Reduction Therapy: Tolerability, Pharmacodynamics, and Pharmacokinetics in Patients With Fabry Disease on Enzyme Replacement. Clinical Pharmacology and Therapeutics, 103(4), 703–711. https://doi.org/10.1002/cpt.790 28699267
  • Guex, N., &Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis, 18(15), 2714–2723. https://doi.org/10.1002/elps.1150181505 9504803
  • Gutternigg, M.,Kretschmer-Lubich, D.,Paschinger, K.,Rendić, D.,Hader, J.,Geier, P.,Ranftl, R.,Jantsch, V.,Lochnit, G., &Wilson, I. B. H. (2007). Biosynthesis of truncated N-linked oligosaccharides results from non-orthologous hexosaminidase-mediated mechanisms in nematodes, plants, and insects. The Journal of Biological Chemistry, 282(38), 27825–27840. https://doi.org/10.1074/jbc.M704235200 17636254
  • Hibshman, J. D., Webster, A. K., & Baugh, L. R. (2021). Liquid-culture protocols for synchronous starvation, growth, dauer formation, and dietary restriction of Caenorhabditis elegans. STAR Protocols, 2(1), 100276. https://doi.org/10.1016/j.xpro.2020.100276
  • Hughes, D. A.,Nicholls, K.,Shankar, S. P.,Sunder-Plassmann, G.,Koeller, D.,Nedd, K.,Vockley, G.,Hamazaki, T.,Lachmann, R.,Ohashi, T.,Olivotto, I.,Sakai, N.,Deegan, P.,Dimmock, D.,Eyskens, F.,Germain, D. P.,Goker-Alpan, O.,Hachulla, E.,Jovanovic, A.,…Feldt-Rasmussen, U. (2017). Oral pharmacological chaperone migalastat compared with enzyme replacement therapy in Fabry disease: 18-month results from the randomised phase III ATTRACT study. Journal of Medical Genetics, 54(4), 288–296. doi: 10.1136/jmedgenet-2016-104178.
  • Hujová, J., Sikora, J., Dobrovolný, R., Poupetová, H., Ledvinová, J., Kostrouchová, M., & Hrebícek, M. (2005). Characterization of gana-1, a Caenorhabditis elegans gene encoding a single ortholog of vertebrate alpha-galactosidase and alpha-N-acetylgalactosaminidase. BMC Cell Biology, 6(1), 5. https://doi.org/10.1186/1471-2121-6-5
  • Ishii, S.,Chang, H.-H.,Kawasaki, K.,Yasuda, K.,Wu, H.-L.,Garman, S., &Fan, J.-Q. (2007). Mutant α-galactosidase A enzymes identified in Fabry disease patients with residual enzyme activity: biochemical characterization and restoration of normal intracellular processing by 1-deoxygalactonojirimycin. Biochemical Journal, 406(2), 285–295. https://doi.org/10.1042/BJ20070479
  • Jeong, J., Kim, H., & Choi, J. (2019). In silico molecular docking and in vivo validation with Caenorhabditis elegans to discover molecular initiating events in adverse outcome pathway framework: Case study on endocrine-disrupting chemicals with estrogen and androgen receptors. International Journal of Molecular Sciences, 20(5), 1209. https://doi.org/10.3390/ijms20051209
  • Kanda, A.,Nakao, S.,Tsuyama, S.,Murata, F., &Kanzaki, T. (2000). Fabry disease: ultrastructural lectin histochemical analyses of lysosomal deposits. Virchows Archiv : An International Journal of Pathology, 436(1), 36–42. https://doi.org/10.1007/pl00008196 10664160
  • Khan, S. U., Ahemad, N., Chuah, L.-H., Naidu, R., & Htar, T. T. (2022). Natural bioactive compounds as a new source of promising G protein-coupled estrogen receptor (GPER) modulators: Comprehensive in silico approach. Journal of Biomolecular Structure & Dynamics, 40(4), 1617–1628. doi:https://doi.org/10.1080/07391102.2020.1830853.
  • Krieger, E., & Vriend, G. (2014). YASARA view - molecular graphics for all devices - from smartphones to workstations. Bioinformatics (Oxford, England), 30(20), 2981–2982. https://doi.org/10.1093/bioinformatics/btu426
  • Kufareva, I., & Abagyan, R. (2012). Methods of protein structure comparison. Methods in Molecular Biology (Clifton, NJ), 857, 231–257. https://doi.org/10.1007/978-1-61779-588-6_10
  • Land, H., &Humble, M. S. (2018). YASARA: A Tool to Obtain Structural Guidance in Biocatalytic Investigations. Methods in Molecular Biology (Clifton, N.J.), 1685, 43–67. https://doi.org/10.1007/978-1-4939-7366-8_4 29086303
  • Laskowski, R. A. (2001). PDBsum: summaries and analyses of PDB structures. Nucleic Acids Research, 29(1), 221–222. https://doi.org/10.1093/nar/29.1.221 11125097
  • Laskowski, R. A.,Watson, J. D., &Thornton, J. M. (2005). ProFunc: a server for predicting protein function from 3D structure. Nucleic Acids Research, 33(Web Server), W89–W93. https://doi.org/10.1093/nar/gki414
  • Lenders, M., &Brand, E. (2018). Effects of Enzyme Replacement Therapy and Antidrug Antibodies in Patients with Fabry Disease. Journal of the American Society of Nephrology : JASN, 29(9), 2265–2278. https://doi.org/10.1681/ASN.2018030329 30093456
  • Lenders, M., &Brand, E. (2021). Fabry Disease: The Current Treatment Landscape. Drugs, 81(6), 635–645. https://doi.org/10.1007/s40265-021-01486-1
  • Lovell, S. C.,Davis, I. W.,Arendall, W. B.,De Bakker, P. I. W.,Word, J. M.,Prisant, M. G.,Richardson, J. S., &Richardson, D. C. (2003). Structure validation by Cα geometry: ϕ,ψ and Cβ deviation. Proteins: Structure, Function, and Bioinformatics, 50(3), 437–450. https://doi.org/10.1002/prot.10286
  • Malikanti, R., Vadija, R., Veeravarapu, H., Mustyala, K. K., Malkhed, V., & Vuruputuri, U. (2017). Identification of small molecular ligands as potent inhibitors of fatty acid metabolism in Mycobacterium tuberculosis. Journal of Molecular Structure, 1150, 227–241. https://doi.org/10.1016/j.molstruc.2017.08.090
  • Moise, A., Maeser, S., Rawer, S., Eggers, F., Murphy, M., Bornheim, J., & Przybylski, M. (2016). Substrate and substrate-mimetic chaperone binding sites in human α-galactosidase a revealed by affinity-mass spectrometry. Journal of the American Society for Mass Spectrometry, 27(6), 1071–1078. https://doi.org/10.1007/s13361-016-1386-0
  • Morris, A. L.,MacArthur, M. W.,Hutchinson, E. G., &Thornton, J. M. (1992). Stereochemical quality of protein structure coordinates. Proteins, 12(4), 345–364. https://doi.org/10.1002/prot.340120407 1579569
  • Mosca, R., Brannetti, B., & Schneider, T. R. (2008). Alignment of protein structures in the presence of domain motions. BMC Bioinformatics, 9, 352. https://doi.org/10.1186/1471-2105-9-352
  • Oduselu, G. O., Ajani, O. O., Ajamma, Y. U., Brors, B., & Adebiyi, E. (2019). Homology modelling and molecular docking studies of selected substituted benzo[d]imidazol-1-yl)methyl)benzimidamide scaffolds on Plasmodium falciparum adenylosuccinate lyase receptor. Bioinformatics and Biology Insights, 13, 117793221986553. https://doi.org/10.1177/1177932219865533
  • Pintos-Morell, G., &Beck, M. (2009). Fabry disease in children and the effects of enzyme replacement treatment. European Journal of Pediatrics, 168(11), 1355–1363. https://doi.org/10.1007/s00431-009-0937-9 19242721
  • Qu, W.,Ren, C.,Li, Y.,Shi, J.,Zhang, J.,Wang, X.,Hang, X.,Lu, Y.,Zhao, D., &Zhang, C. (2011). Reliability analysis of the Ahringer Caenorhabditis elegans RNAi feeding library: a guide for genome-wide screens. BMC Genomics, 12, 170 https://doi.org/10.1186/1471-2164-12-170 21453524
  • Ray, A.,Lindahl, E., &Wallner, B. (2012). Improved model quality assessment using ProQ2. BMC Bioinformatics, 13, 224 https://doi.org/10.1186/1471-2105-13-224 22963006
  • Rombach, S. M.,Dekker, N.,Bouwman, M. G.,Linthorst, G. E.,Zwinderman, A. H.,Wijburg, F. A.,Kuiper, S.,Vd Bergh Weerman, M. A.,Groener, J.,Poorthuis, B. J.,Hollak, C., &Aerts, J. (2010). Plasma globotriaosylsphingosine: Diagnostic value and relation to clinical manifestations of Fabry disease. Biochimica Et Biophysica Acta (BBA)- Molecular Basis of Disease, 1802(9), 741–748. https://doi.org/10.1016/j.bbadis.2010.05.003
  • Rombach, S. M.,Hollak, C. E. M.,Linthorst, G. E., &Dijkgraaf, M. G. W. (2013). Cost-effectiveness of enzyme replacement therapy for Fabry disease. Orphanet Journal of Rare Diseases, 8, 29 https://doi.org/10.1186/1750-1172-8-29 23421808
  • Schaheen, L.,Dang, H., &Fares, H. (2006). Basis of lethality in C. elegans lacking CUP-5, the Mucolipidosis Type IV orthologue. Developmental Biology, 293(2), 382–391. https://doi.org/10.1016/j.ydbio.2006.02.008 16530747
  • Selvam, K.,Senbagam, D.,Selvankumar, T.,Sudhakar, C.,Kamala-Kannan, S.,Senthilkumar, B., &Govarthanan, M. (2017). Cellulase enzyme: Homology modeling, binding site identification and molecular docking. Journal of Molecular Structure, 1150, 61–67. https://doi.org/10.1016/j.molstruc.2017.08.067
  • Sharma, O. P., Agrawal, S., & Kumar, M. S. (2013). Physicochemical properties of the modeled structure of astacin metalloprotease moulting enzyme NAS-36 and mapping the druggable allosteric space of Heamonchus contortus, Brugia malayi and Ceanorhabditis elegans via molecular dynamics simulation. Interdisciplinary Sciences, Computational Life Sciences, 5(4), 312–323. https://doi.org/10.1007/s12539-013-0182-9
  • Tian, W., Chen, C., Lei, X., Zhao, J., & Liang, J. (2018). CASTp 3.0: Computed atlas of surface topography of proteins. Nucleic Acids Research, 46(W1), W363–W367. https://doi.org/10.1093/nar/gky473
  • Tsai, G.,Tsai, C.-J.,Ma, B., &Nussinov, R. (2004). In silico protein design by combinatorial assembly of protein building blocks. Protein Science : a Publication of the Protein Society, 13(10), 2753–2765. https://doi.org/10.1110/ps.04774004 15388863
  • Volkamer, A.,Kuhn, D.,Grombacher, T.,Rippmann, F., &Rarey, M. (2012). Combining global and local measures for structure-based druggability predictions. Journal of Chemical Information and Modeling, 52(2), 360–372. https://doi.org/10.1021/ci200454v 22148551
  • Welford, R. W.,Mühlemann, A.,Priestman, D.,Garzotti, M.,Deymier, C.,Ertel, E. A.,Iglarz, M.,Baldoni, D.,Platt, F. M., &Probst, M. R. (2017). Lucerastat, an iminosugar for substrate reduction therapy in Fabry disease: preclinical evidence. Molecular Genetics and Metabolism, 120(1-2), S139–S140. https://doi.org/10.1016/j.ymgme.2016.11.369
  • Wiltgen, M. (2018). Algorithms for structure comparison and analysis: Homology modelling of proteins. In Encyclopedia of bioinformatics and computational biology: ABC of bioinformatics, 1, 38–61. Academic Press. https://doi.org/10.1016/B978-0-12-809633-8.20484-6
  • Xu, D., & Zhang, Y. (2011). Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophysical Journal, 101(10), 2525–2534. https://doi.org/10.1016/j.bpj.2011.10.024
  • Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2014). The I-TASSER suite: Protein structure and function prediction. Nature Methods, 12(1), 7–8. https://doi.org/10.1038/nmeth.3213
  • Yuasa, T., Takenaka, T., Higuchi, K., Uchiyama, N., Horizoe, Y., Cyaen, H., Mizukami, N., Takasaki, K., Kisanuki, A., Miyata, M., & Ohishi, M. (2017). Fabry disease. Journal of Echocardiography, 15(4), 151–157. https://doi.org/10.1007/s12574-017-0340-x
  • Zhang, C., Freddolino, P. L., & Zhang, Y. (2017). COFACTOR: Improved protein function prediction by combining structure, sequence and protein-protein interaction information. Nucleic Acids Research, 45(W1), W291–W299. https://doi.org/10.1093/nar/gkx366

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