Enolase in Meyerozyma guilliermondii strain SO: Sequential and structural insights of MgEno4581 as a putative virulence factor and host-fungal interactions through comprehensive in silico approaches

Microbial Pathogenesis - Tập 176 - Trang 106025 - 2023
Alia Iwani Amran1, Si Jie Lim2,3, Noor Dina Muhd Noor1,3, Abu Bakar Salleh3, Siti Nurbaya Oslan1,2,3
1Department of Biochemistry, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, 43400, UPM, Serdang, Selangor, Malaysia
2Enzyme Technology and X-ray Crystallography Laboratory, VacBio 5, Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
3Enzyme and Microbial Technology (EMTech) Research Centre, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia

Tài liệu tham khảo

Pancholi, 2001, Multifunctional α-enolase: its role in diseases, Cell. Mol. Life Sci. C., 587, 902, 10.1007/PL00000910 Valdar, 2001, Protein-protein interfaces: analysis of amino acid conservation in homodimers, Proteins Struct. Funct. Genet., 42, 108, 10.1002/1097-0134(20010101)42:1<108::AID-PROT110>3.0.CO;2-O Reyna-Beltrán, 2018, The Candida albicans ENO1 gene encodes a transglutaminase involved in growth, cell division, morphogenesis, and osmotic protection, J. Biol. Chem., 293, 4304, 10.1074/jbc.M117.810440 Didiasova, 2019, When place matters: shuttling of enolase-1 across cellular compartments, Front. Cell Dev. Biol., 7, 61, 10.3389/fcell.2019.00061 Marangos, 1978, Functional properties of neuronal and glial isoenzymes of brain enolase, J. Neurochem., 31, 727, 10.1111/j.1471-4159.1978.tb07847.x Walsh, 1991, Detection of circulating Candida enolase by immunoassay in patients with cancer and invasive candidiasis, N. Engl. J. Med., 324, 1026, 10.1056/NEJM199104113241504 Gil-Bona, 2015, Proteomics unravels extracellular vesicles as carriers of classical cytoplasmic proteins in Candida albicans, J. Proteome Res., 14, 142, 10.1021/pr5007944 Karkowska-Kuleta, 2021, Proteinous components of neutrophil extracellular traps are arrested by the cell wall proteins of Candida albicans during fungal infection, and can be used in the host invasion, Cells, 10, 10.3390/cells10102736 Turner, 2014, The Candida pathogenic species complex, Cold Spring Harb. Perspect. Med., 4, a019778, 10.1101/cshperspect.a019778 Lim, 2021, Opportunistic yeast pathogen Candida spp.: secreted and membrane-bound virulence factors, Med. Mycol., 10.1093/mmy/myab053 Satala, 2020, Structural insights into the interactions of Candidal enolase with human vitronectin, fibronectin and plasminogen, Int. J. Mol. Sci., 21, 7843, 10.3390/ijms21217843 Chen, 2020, Preventing Candida albicans from subverting host plasminogen for invasive infection treatment, Emerg. Microb. Infect., 9, 2417, 10.1080/22221751.2020.1840927 Vaz, 2021, Mass spectrometry-based proteomic and immunoproteomic analyses of the Candida albicans hyphal secretome reveal diagnostic biomarker candidates for invasive candidiasis, J. Fungi., 7, 10.3390/jof7070501 Fox, 2001, Plasminogen-binding activity of enolase in the opportunistic pathogen Pneumocystis carinii, Med. Mycol., 39, 495, 10.1080/mmy.39.6.495.507 Karkowska-Kuleta, 2021, Als3-mediated attachment of enolase on the surface of Candida albicans cells regulates their interactions with host proteins, Cell Microbiol., 23, 10.1111/cmi.13297 Liping, 2022, Baicalein acts against Candida albicans by targeting Eno1 and inhibiting glycolysis, Microbiol. Spectr., 10 Karkowska-Kuleta, 2020, Characteristics of extracellular vesicles released by the pathogenic yeast-like fungi Candida glabrata, Candida parapsilosis and Candida tropicalis, Cells, 9, 10.3390/cells9071722 Vázquez-Fernández, 2021, A comparative proteomic analysis of Candida species in response to the oxidizing agent cumene hydroperoxide, Arch. Microbiol., 203, 2219, 10.1007/s00203-021-02186-w Kołaczkowska, 2016, Drug resistance mechanisms and their regulation in non-albicans Candida species, J. Antimicrob. Chemother., 71, 1438, 10.1093/jac/dkv445 Taei, 2019, An alarming rise of non-albicans Candida species and uncommon yeasts in the clinical samples; a combination of various molecular techniques for identification of etiologic agents, BMC Res. Notes, 12, 1, 10.1186/s13104-019-4811-1 Kolhe, 2020, Removal of uranium by immobilized biomass of a tropical marine yeast Yarrowia lipolytica, J. Environ. Radioact., 223 Colombo, 2017, Emerging multidrug-resistant Candida species, Curr. Opin. Infect. Dis., 30, 528, 10.1097/QCO.0000000000000411 Yan, 2021, Biotechnological applications of the non-conventional yeast Meyerozyma guilliermondii, Biotechnol. Adv., 46, 10.1016/j.biotechadv.2020.107674 Oslan, 2012, Locally isolated yeasts from Malaysia: identification, phylogenetic study and characterization, Acta Bochimica Pol, 59, 225 Abu, 2017, Optimization of physical conditions for the production of thermostable T1 lipase in Pichia guilliermondii strain SO using response surface methodology, BMC Biotechnol., 17, 78, 10.1186/s12896-017-0397-7 Nasir, 2020, Molecular expression of a recombinant thermostable bacterial amylase from Geobacillus stearothermophilus SR74 using methanol-free Meyerozyma guilliermondii strain SO yeast system, Bioresources, 15, 3161, 10.15376/biores.15.2.3161-3172 Radzi, 2020 Xie, 2021, Hidden Markov Model: a shortest unique representative approach to detect the protein toxins, virulence factors and antibiotic resistance genes, BMC Res. Notes, 14, 1, 10.1186/s13104-021-05531-w Lu, 2020, CDD/SPARCLE: the conserved domain database in 2020, Nucleic Acids Res., 48, D265, 10.1093/nar/gkz991 Teufel, 2022, SignalP 6.0 predicts all five types of signal peptides using protein language models, Nat. Biotechnol., 40, 1023, 10.1038/s41587-021-01156-3 Thumuluri, 2022, DeepLoc 2.0: multi-label subcellular localization prediction using protein language models, Nucleic Acids Res., 50, W228, 10.1093/nar/gkac278 Sievers, 2021, The clustal omega multiple alignment package, Methods Mol. Biol., 2231, 3, 10.1007/978-1-0716-1036-7_1 Robert, 2014, Deciphering key features in protein structures with the new ENDscript server, Nucleic Acids Res., 42, W320, 10.1093/nar/gku316 Waterhouse, 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res., 46, 296, 10.1093/nar/gky427 Kozakov, 2017, The ClusPro web server for protein-protein docking, Nat. Protoc., 12, 255, 10.1038/nprot.2016.169 Laskowski, 2011, LigPlot+: multiple ligand-protein interaction diagrams for drug discovery, J. Chem. Inf. Model., 51, 2778, 10.1021/ci200227u Chandler, 2008, Protein profiling of the dimorphic, pathogenic fungus, Penicillium marneffei, Proteome Sci., 6, 17, 10.1186/1477-5956-6-17 Patel, 2017, Pathogenicity-associated protein domains: the fiercely-conserved evolutionary signatures, Gene Reports, 7, 127, 10.1016/j.genrep.2017.04.004 Gerlt, 2012, Divergent evolution in enolase superfamily: strategies for assigning functions, J. Biol. Chem., 287, 29, 10.1074/jbc.R111.240945 Likic, 2010, Using hidden markov models to discover new protein transport machines, Methods Mol. Biol., 619, 271, 10.1007/978-1-60327-412-8_16 Finn, 2016, The Pfam protein families database: towards a more sustainable future, Nucleic Acids Res., 44, D279—, 10.1093/nar/gkv1344 Liu, 2019, VFDB 2019: a comparative pathogenomic platform with an interactive web interface, Nucleic Acids Res., 47, D687—, 10.1093/nar/gky1080 Chin, 1981, The amino acid sequence of yeast enolase, J. Biol. Chem., 256, 1377, 10.1016/S0021-9258(19)69975-8 Kornblatt, 2013, The Saccharomyces cerevisiae enolase-related regions encode proteins that are active enolases, Yeast, 30, 55, 10.1002/yea.2940 Dasari, 2019, Enolase from Aspergillus fumigatus is a moonlighting protein that binds the human plasma complement proteins factor H, FHL-1, C4BP, and plasminogen, Front. Immunol., 10, 2573, 10.3389/fimmu.2019.02573 Entelis, 2006, A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae, Genes Dev., 20, 1609, 10.1101/gad.385706 Brandina, 2006, Enolase takes part in a macromolecular complex associated to mitochondria in yeast, Biochim. Biophys. Acta Bioenerg., 1757, 1217, 10.1016/j.bbabio.2006.07.001 Bernal, 2004, Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica, FEBS Lett., 563, 203, 10.1016/S0014-5793(04)00306-0 Lonhienne, 2020, Structures of fungal and plant acetohydroxyacid synthases, Nature, 586, 317, 10.1038/s41586-020-2514-3 Fagan, 2010, Flavin-dependent enzymes, Compr. Nat. Prod. II Chem. Biol., 7, 37 Franklyn, 1993, Cloning and nucleotide sequence analysis of the Candida albicans enolase gene, FEMS Microbiol. Lett., 111, 101, 10.1111/j.1574-6968.1993.tb06368.x Butler, 2009, Evolution of pathogenicity and sexual reproduction in eight Candida genomes, Nature, 459, 657, 10.1038/nature08064 Mitsutake, 1994, Detection of Candida enolase antibody in patients with candidiasis, J. Clin. Lab. Anal., 8, 207, 10.1002/jcla.1860080405 V Koonin, 2003, Principles and methods of sequence analysis, 111 Dunn, 2018, Functional diversification accompanies gene family expansion of MED2 homologs in Candida albicans, PLoS Genet., 14, 10.1371/journal.pgen.1007326 Makigaki, 2020, Sequence alignment using machine learning for accurate template-based protein structure prediction, Bioinformatics, 36, 104, 10.1093/bioinformatics/btz483 Nguyen, 2021, Targeting unconventional pathways in pursuit of novel antifungals, Front. Mol. Biosci., 7, 10.3389/fmolb.2020.621366 Funk, 2016, The glycolytic enzyme enolase represents a plasminogen-binding protein on the surface of a wide variety of medically important fungal species, Int. J. Med. Microbiol., 306, 59, 10.1016/j.ijmm.2015.11.005 Miura, 2012, Tracing putative trafficking of the glycolytic enzyme enolase via SNARE-driven unconventional secretion, Eukaryot. Cell, 11, 1075, 10.1128/EC.00075-12 Coe, 1999, A role for Tlg1p in the transport of proteins within the Golgi Apparatus of Saccharomyces cerevisiae, Mol. Biol. Cell, 10, 2407, 10.1091/mbc.10.7.2407 Ballantyne, 2000, Purification of native enolase from medically important Candida species, Biotechnol. Appl. Biochem., 31, 213, 10.1042/BA19990106 Silva, 2014, Extracellular enolase of Candida albicans is involved in colonization of mammalian intestinal epithelium, Front. Cell. Infect. Microbiol., 4, 66, 10.3389/fcimb.2014.00066 Seweryn, 2015, Kinetic and thermodynamic characterization of the interactions between the components of human plasma kinin-forming system and isolated and purified cell wall proteins of Candida albicans, Acta Biochim. Pol., 62, 825, 10.18388/abp.2015_1142 He, 2022, Investigation of the location and secretion features of Candida albicans enolase with monoclonal antibodies, Ann. Microbiol., 72, 25, 10.1186/s13213-022-01682-8 Rollenhagen, 2020, The role of secretory pathways in Candida albicans pathogenesis, J. Fungi, 6, 26, 10.3390/jof6010026 Reed, 1996, Structural and mechanistic studies of enolase, Curr. Opin. Struct. Biol., 6, 736, 10.1016/S0959-440X(96)80002-9 Ucker, 2012, Externalized glycolytic enzymes are novel, conserved, and early biomarkers of apoptosis, J. Biol. Chem., 287, 10325, 10.1074/jbc.M111.314971 Zadvornyy, 2015, Biochemical and structural characterization of enolase from Chloroflexus aurantiacus: evidence for a thermophilic origin, Front. Bioeng. Biotechnol., 3, 74, 10.3389/fbioe.2015.00074 Fiser, 2010, Template-based protein structure modeling, 73 Brewer, 1981, Yeast enolase: mechanism of activation by metal ion, Crit. Rev. Biochem. Mol. Biol., 11, 209 Li, 2019, Substrate-to-product conversion facilitates active site loop opening in yeast enolase: a molecular dynamics study, ACS Catal., 9, 8985, 10.1021/acscatal.9b03249 Larsen, 1996, A carboxylate oxygen of the substrate bridges the magnesium ions at the active site of enolase: structure of the yeast enzyme complexed with the equilibrium mixture of 2-phosphoglycerate and phosphoenolpyruvate at 1.8 Åresolution, Biochemistry, 35, 4349, 10.1021/bi952859c Schreier, 2010, Engineering the enolase magnesium II binding site: implications for its evolution, Biochemistry, 49, 7582, 10.1021/bi100954f Avilán, 2011, A key player in the metabolism and a probable virulence factor of trypanosomatid parasites - perspectives for its use as a therapeutic target, Enzym. Res., 2011, 10.4061/2011/932549 Bergmann, 2005, The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration, Thromb. Haemostasis, 94, 304, 10.1160/TH05-05-0369 Kozik, 2015, Fibronectin-, vitronectin- and laminin-binding proteins at the cell walls of Candida parapsilosis and Candida tropicalis pathogenic yeasts, BMC Microbiol., 15, 197, 10.1186/s12866-015-0531-4