Structural Insights into the Interactions of Candidal Enolase with Human Vitronectin, Fibronectin and Plasminogen
Abstract
:1. Introduction
2. Results
2.1. Soluble Purified Candidal Enolases and Anti-Enolase Antibodies Inhibit the Adsorption of Human VTR, FN and HPG to Fungal Cells
2.2. The Equivalent Human Protein-Binding Abilities of C. albicans Cell Surface-Exposed and Cytosolic Enolases
2.3. C. tropicalis Enolase Binds VTR, FN and HPG with Kinetic and Equilibrium Parameters that Are Comparable to Those of C. albicans Enolase, but Much Stronger than the S. cerevisiae Enolase
2.4. The Binding of VTR, FN and HPG to the Candidal Enolases is Partially Competitive and Does Not Affect Their Catalytic Activity
2.5. Chemical Cross-Linking to Map the Candidal Enolase Sequence Fragments Involved in the Interactions with Human Host Proteins
2.6. Molecular Modeling of the C. albicans Enolase Interactions with VTR, HPG and Fragments of FN
2.7. The Sequence Fragment 235DKAGYKGKVGIAMDVASSEFY255 of C. albicans Enolase is a Major Determinant of Its Interactions with Human Proteins
3. Discussion
4. Materials and Methods
4.1. Yeast Strains and Culture Conditions
4.2. Commercial Proteins
4.3. Purification of C. albicans Surface-Exposed Enolase
4.4. Purification of the Cytosolic Enolases from C. albicans and C. tropicalis
4.5. Expression and Purification of Recombinant C. albicans Enolase (R-Eno)
4.6. DNA Construct for R-Enosc Expression
4.7. Enolase Activity
4.8. Labeling of Human Proteins and Purified Enolases
4.9. Competition of Human VTR, FN and HPG with Soluble Enolase or Anti-Fungal Enolase Antibody for the Binding to C. albicans or C. tropicalis Cells
4.10. Semi-Quantitative Analysis of Enolase Binding to Microplate-Immobilized VTR, FN, and HPG
4.11. SPR Characterization of Fungal Enolase Binding to VTR, FN and HPG
4.12. Mapping of the Fungal Enolase Fragments Involved in the Interactions with VTR, FN and HPG by Chemical Cross-Linking
4.12.1. Chemical Cross-Linking
4.12.2. Mass Spectrometric Analysis
4.13. Competition between Human VTR and HPG for the Binding to C. albicans Enolase
4.14. Alignment of the Amino-Acid Sequences of C. albicans, C. tropicalis, and S. cerevisiae Enolases
4.15. Model of the Interaction between C. albicans Enolase and HPG, VTR and FN
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
ECM | extracellular matrix |
FN | fibronectin |
FN-Bt | biotin-labeled fibronectin |
HPG | human plasminogen |
HPG-Bt | biotin-labeled human plasminogen |
LC-MS/MS | liquid chromatography-coupled tandem mass spectrometry |
R-Eno | recombinant enolase of C. albicans |
R-Enosc | recombinant enolase of C. albicans with a sequence of S. cerevisiae |
SA-HRP/TMB | streptavidin-horseradish peroxidase/tetramethylbenzidine |
SDS-PAGE | sodium dodecyl sulphate polyacrylamide gel electrophoresis |
sulfo-SDAD | sulfosuccinimidyl 2-([4,4′-azipentanamido]ethyl)-1,3′-dithiopropionate |
SPR | surface plasmon resonance |
VTR | vitronectin |
VTR-Bt | biotin-labeled vitronectin |
References
- Díaz-Ramos, A.; Roig-Borrellas, A.; García-Melero, A.; López-Alemany, R. α-Enolase, a multifunctional protein: Its role on pathophysiological situations. J. Biomed. Biotechnol. 2012, 2012, 156795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ji, H.; Wang, J.; Guo, J.; Li, Y.; Lian, S.; Guo, W.; Yang, H.; Kong, F.; Zhen, L.; Guo, L.; et al. Progress in the biological function of alpha-enolase. Anim. Nutr. 2016, 2, 12–17. [Google Scholar] [CrossRef]
- Didiasova, M.; Schaefer, L.; Wygrecka, M. When place matters: Shuttling of enolase-1 across cellular compartments. Front. Cell Dev. Biol. 2019, 7, 61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wistow, G.; Piatigorsky, J. Recruitment of enzymes as lens structural proteins. Science 1987, 236, 1554–1556. [Google Scholar] [CrossRef] [PubMed]
- Wistow, G.J.; Lietman, T.; Williams, L.A.; Stapel, S.O.; de Jong, W.W.; Horwitz, J.; Piatigorsky, J. τ-Crystallin/α-enolase: One gene encodes both an enzyme and a lens structural protein. J. Cell Biol. 1988, 107, 2729–2736. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeffery, C.J. Moonlighting proteins. Trends Biochem. Sci. 1999, 24, 8–11. [Google Scholar] [CrossRef]
- Satala, D.; Karkowska-Kuleta, J.; Zelazna, A.; Rapala-Kozik, M.; Kozik, A. Moonlighting proteins at the candidal cell surface. Microorganisms 2020, 8, 1046. [Google Scholar] [CrossRef]
- Chandran, V.; Luisi, B.F. Recognition of enolase in the Escherichia coli RNA degradosome. J. Mol. Biol. 2006, 358, 8–15. [Google Scholar] [CrossRef]
- Morita, T.; Kawamoto, H.; Mizota, T.; Inada, T.; Aiba, H. Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli. Mol. Microbiol. 2004, 54, 1063–1075. [Google Scholar] [CrossRef]
- Iida, H.; Yahara, I. Yeast heat-shock protein of Mr 48,000 is an isoprotein of enolase. Nature 1985, 314, 688–690. [Google Scholar] [CrossRef]
- Brandina, I.; Graham, J.; Lemaitre-Guillier, C.; Entelis, N.; Krasheninnikov, I.; Sweetlove, L.; Tarassov, I.; Martin, R.P. Enolase takes part in a macromolecular complex associated to mitochondria in yeast. Biochim. Biophys. Acta 2006, 1757, 1217–1228. [Google Scholar] [CrossRef] [PubMed]
- Entelis, N.; Brandina, I.; Kamenski, P.; Krasheninnikov, I.A.; Martin, R.P.; Tarassov, I. A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev. 2006, 20, 1609–1620. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Keller, A.; Peltzer, J.; Carpentier, G.; Horváth, I.; Oláh, J.; Duchesnay, A.; Orosz, F.; Ovádi, J. Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim. Biophys. Acta 2007, 1770, 919–926. [Google Scholar] [CrossRef] [PubMed]
- Bottalico, L.A.; Kendrick, N.C.; Keller, A.; Li, Y.; Tabas, I. Cholesteryl ester loading of mouse peritoneal macrophages is associated with changes in the expression or modification of specific cellular proteins, including increase in an α-enolase isoform. Arterioscler. Thromb. 1993, 13, 264–275. [Google Scholar] [CrossRef] [Green Version]
- Shand, J.H.; West, D.W. Inhibition of neutral cholesteryl ester hydrolase by the glycolytic enzyme enolase. Is this a secondary function of enolase? Lipids 1995, 30, 763–770. [Google Scholar] [CrossRef]
- Graven, K.K.; Zimmerman, L.H.; Dickson, E.W.; Weinhouse, G.L.; Farber, H.W. Endothelial cell hypoxia associated proteins are cell and stress specific. J. Cell. Physiol. 1993, 157, 544–554. [Google Scholar] [CrossRef]
- Aaronson, R.M.; Graven, K.K.; Tucci, M.; McDonald, R.J.; Farber, H.W. Non-Neuronal enolase is an endothelial hypoxic stress protein. J. Biol. Chem. 1995, 270, 27752–27757. [Google Scholar] [CrossRef] [Green Version]
- Feo, S.; Arcuri, D.; Piddini, E.; Passantino, R.; Giallongo, A. ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: Relationship with Myc promoter-binding protein 1 (MBP-1). FEBS Lett. 2000, 473, 47–52. [Google Scholar] [CrossRef] [Green Version]
- Lung, J.; Liu, K.J.; Chang, J.Y.; Leu, S.J.; Shih, N.Y. MBP-1 is efficiently encoded by an alternative transcript of the ENO1 gene but post-translationally regulated by proteasome-dependent protein turnover. FEBS J. 2010, 277, 4308–4321. [Google Scholar] [CrossRef]
- Cappello, P.; Principe, M.; Bulfamante, S.; Novelli, F. α-Enolase (ENO1), a potential target in novel immunotherapies. Front. Biosci. 2017, 22, 944–959. [Google Scholar] [CrossRef]
- Wang, G.; Xia, Y.; Cui, J.; Gu, Z.; Song, Y.; Chen, Y.Q.; Chen, H.; Zhang, H.; Chen, W. The roles of moonlighting proteins in bacteria. Curr. Issues Mol. Biol. 2014, 16, 15–22. [Google Scholar] [PubMed]
- Jeffery, C.J. Intracellular proteins moonlighting as bacterial adhesion factors. AIMS Microbiol. 2018, 4, 362–376. [Google Scholar] [CrossRef] [PubMed]
- Karkowska-Kuleta, J.; Kozik, A. Moonlighting proteins as virulence factors of pathogenic fungi, parasitic protozoa and multicellular parasites. Mol. Oral Microbiol. 2014, 29, 270–283. [Google Scholar] [CrossRef]
- Gómez-Arreaza, A.; Acosta, H.; Quiñones, W.; Concepción, J.L.; Michels, P.A.M.; Avilán, L. Extracellular functions of glycolytic enzymes of parasites: Unpredicted use of ancient proteins. Mol. Biochem. Parasitol. 2014, 193, 75–81. [Google Scholar] [CrossRef] [PubMed]
- López-Villar, E.; Monteoliva, L.; Larsen, M.R.; Sachon, E.; Shabaz, M.; Pardo, M.; Pla, J.; Gil, C.; Roepstorff, P.; Nombela, C. Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 2006, 6 (Suppl. 1), S107–S118. [Google Scholar] [CrossRef]
- Castillo, L.; Calvo, E.; Martínez, A.I.; Ruiz-Herrera, J.; Valentín, E.; Lopez, J.A.; Sentandreu, R. A study of the Candida albicans cell wall proteome. Proteomics 2008, 8, 3871–3881. [Google Scholar] [CrossRef]
- Karkowska-Kuleta, J.; Zajac, D.; Bochenska, O.; Kozik, A. Surfaceome of pathogenic yeasts, Candida parapsilosis and Candida tropicalis, revealed with the use of cell surface shaving method and shotgun proteomic approach. Acta Biochim. Pol. 2015, 62, 807–819. [Google Scholar] [CrossRef]
- Karkowska-Kuleta, J.; Satala, D.; Bochenska, O.; Rapala-Kozik, M.; Kozik, A. Moonlighting proteins are variably exposed at the cell surfaces of Candida glabrata, Candida parapsilosis and Candida tropicalis under certain growth conditions. BMC Microbiol. 2019, 19, 149. [Google Scholar] [CrossRef]
- Mohamed, A.A.; Lu, X.L.; Mounmin, F.A. Diagnosis and treatment of esophageal candidiasis: Current updates. Can. J. Gastroenterol. Hepatol. 2019, 2019, 3585136. [Google Scholar] [CrossRef] [Green Version]
- Tadec, L.; Talarmin, J.P.; Gastinne, T.; Bretonnière, C.; Miegeville, M.; Le Pape, P.; Morio, F. Epidemiology, risk factor, species distribution, antifungal resistance and outcome of candidemia at a single French hospital: A 7 year study. Mycoses 2016, 2016, 296–303. [Google Scholar] [CrossRef]
- Enoch, D.A.; Yang, H.; Aliyu, S.H.; Micallef, C. The changing epidemiology of invasive fungal infections. Methods Mol. Biol. 2017, 1508, 17–65. [Google Scholar] [CrossRef]
- Lamoth, F.; Lockhart, S.R.; Berkow, E.L.; Calandra, T. Changes in the epidemiological landscape of invasive candidiasis. J. Antimicrob. Chemother. 2018, 73, i4–i13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giri, S.; Kindo, A.J. A review of Candida species causing blood stream infection. Indian J. Med. Microbiol. 2012, 30, 270–278. [Google Scholar] [CrossRef] [PubMed]
- Wu, P.F.; Liu, W.L.; Hsieh, M.H.; Hii, I.M.; Lee, Y.L.; Lin, Y.T.; Ho, M.-W.; Liu, C.-E.; Chen, Y.-H.; Wang, F.-D. Epidemiology and antifungal susceptibility of candidemia isolates of non-albicans Candida species from cancer patients. Emerg. Microbes Infect. 2017, 6, e87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sundstrom, P.; Aliaga, G.R. Molecular cloning of cDNA and analysis of protein secondary structure of Candida albicans enolase, an abundant, immunodominant glycolytic enzyme. J. Bacteriol. 1992, 174, 6789–6799. [Google Scholar] [CrossRef] [Green Version]
- Ko, H.C.; Hsiao, T.Y.; Chen, C.T.; Yang, Y.L. Candida albicans ENO1 null mutants exhibit altered drug susceptibility, hyphal formation, and virulence. J. Microbiol. 2013, 51, 345–351. [Google Scholar] [CrossRef]
- Reyna-Beltrán, E.; Iranzo, M.; Calderón-González, K.G.; Mondragón-Flores, R.; Labra-Barrios, M.L.; Mormeneo, S.; Luna-Arias, J.P. The Candida albicans ENO1 gene encodes a transglutaminase involved in growth, cell division, morphogenesis, and osmotic protection. J. Biol. Chem. 2018, 293, 4304–4323. [Google Scholar] [CrossRef] [Green Version]
- Núñez-Beltrán, A.; López-Romero, E.; Cuéllar-Cruz, M. Identification of proteins involved in the adhesion of Candida species to different medical devices. Microb. Pathog. 2017, 107, 293–303. [Google Scholar] [CrossRef]
- Silva, S.; Negri, M.; Henriques, M.; Oliveira, R.; Williams, D.W.; Azeredo, J. Adherence and biofilm formation of non-Candida albicans Candida species. Trends Microbiol. 2011, 19, 241–247. [Google Scholar] [CrossRef] [Green Version]
- Silva, R.C.; Padovan, A.C.; Pimenta, D.C.; Ferreira, R.C.; da Silva, C.V.; Briones, M.R. Extracellular enolase of Candida albicans is involved in colonization of mammalian intestinal epithelium. Front. Cell. Infect. Microbiol. 2014, 4, 66. [Google Scholar] [CrossRef] [Green Version]
- Ramírez-Quijas, M.D.; López-Romero, E.; Cuéllar-Cruz, M. Proteomic analysis of cell wall in four pathogenic species of Candida exposed to oxidative stress. Microb. Pathog. 2015, 87, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Gil-Bona, A.; Amador-García, A.; Gil, C.; Monteoliva, L. The external face of Candida albicans: A proteomic view of the cell surface and the extracellular environment. J. Proteom. 2018, 180, 70–79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wächtler, B.; Citiulo, F.; Jablonowski, N.; Förster, S.; Dalle, F.; Schaller, M.; Wilson, D.; Hube, B. Candida albicans-epithelial interactions: Dissecting the roles of active penetration, induced endocytosis and host factors on the infection process. PLoS ONE 2012, 7, e36952. [Google Scholar] [CrossRef] [Green Version]
- Felk, A.; Kretschmar, M.; Albrecht, A.; Schaller, M.; Beinhauer, S.; Nichterlein, T.; Sanglard, D.; Korting, H.C.; Schäfer, W.; Hube, B. Candida albicans hyphal formation and the expression of the Efg1-regulated proteinases Sap4 to Sap6 are required for the invasion of parenchymal organs. Infect. Immun. 2002, 70, 3689–3700. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kozik, A.; Karkowska-Kuleta, J.; Zajac, D.; Bochenska, O.; Kedracka-Krok, S.; Jankowska, U.; Rapala-Kozik, M. Fibronectin-, vitronectin- and laminin-binding proteins at the cell walls of Candida parapsilosis and Candida tropicalis pathogenic yeasts. BMC Microbiol. 2015, 15, 197. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kinloch, A.; Tatzer, V.; Wait, R.; Peston, D.; Lundberg, K.; Donatien, P.; Moyes, D.L.; Taylor, P.C.; Venables, P.J. Identification of citrullinated alpha-enolase as a candidate autoantigen in rheumatoid arthritis. Arthritis Res. Ther. 2005, 7, R1421–R1429. [Google Scholar] [CrossRef] [Green Version]
- Agarwal, A.K.; Xu, T.; Jacob, M.R.; Feng, Q.; Li, X.C.; Walker, L.A.; Clark, A.M. Genomic and genetic approaches for the identification of antifungal drug targets. Infect. Disord. Drug Targets 2008, 8, 2–15. [Google Scholar] [CrossRef]
- Poltermann, S.; Kunert, A.; von der Heide, M.; Eck, R.; Hartmann, A.; Zipfel, P.F. Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem. 2007, 282, 37537–37544. [Google Scholar] [CrossRef] [Green Version]
- Karkowska-Kuleta, J.; Zajac, D.; Bras, G.; Bochenska, O.; Rapala-Kozik, M.; Kozik, A. Binding of human plasminogen and high-molecular-mass kininogen by cell surface-exposed proteins of Candida parapsilosis. Acta Biochim. Pol. 2017, 64, 391–400. [Google Scholar] [CrossRef]
- Crowe, J.D.; Sievwright, I.K.; Auld, G.C.; Moore, N.R.; Gow, N.A.; Booth, N.A. Candida albicans binds human plasminogen: Identification of eight plasminogen-binding proteins. Mol. Microbiol. 2003, 47, 1637–1651. [Google Scholar] [CrossRef]
- Funk, J.; Schaarschmidt, B.; Slesiona, S.; Hallström, T.; Horn, U.; Brock, M. 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. 2016, 306, 59–68. [Google Scholar] [CrossRef] [PubMed]
- Jeffery, C.J. Mass spectrometry and the search for moonlighting proteins. Mass Spectrom. Rev. 2005, 24, 772–782. [Google Scholar] [CrossRef] [PubMed]
- Jeffery, C.J. Protein species and moonlighting proteins: Very small changes in a protein’s covalent structure can change its biochemical function. J. Proteom. 2016, 134, 19–24. [Google Scholar] [CrossRef] [PubMed]
- Hernández, S.; Franco, L.; Calvo, A.; Ferragut, C.; Hermoso, A.; Amela, I.; Gómez, A.; Querol, E.; Cedano, J. Bioinformatics and moonlighting proteins. Front. Bioeng. Biotechnol. 2015, 3, 90. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ehinger, S.; Schubert, W.D.; Bergmann, S.; Hammerschmidt, S.; Heinz, D.W. Plasmin(ogen)-binding a-enolase from Streptococcus pneumoniae: Crystal structure and evaluation of plasmin(ogen)-binding sites. J. Mol. Biol. 2004, 343, 997–1005. [Google Scholar] [CrossRef] [PubMed]
- Kang, H.J.; Jung, S.K.; Kim, S.J.; Chung, S.J. Structure of human α-enolase (hENO1), a multifunctional glycolytic enzyme. Acta Crystallogr. 2008, 6, 651–657. [Google Scholar] [CrossRef] [Green Version]
- Godier, A.; Hunt, B.J. Plasminogen receptors and their role in the pathogenesis of inflammatory, autoimmune and malignant disease. J. Thromb. Haemost. 2013, 11, 26–34. [Google Scholar] [CrossRef] [PubMed]
- Wedekind, J.E.; Reed, G.H.; Rayment, I. Octahedral coordination at the high-affinity metal site in enolase: Crystallographic analysis of the MgII-enzyme complex from yeast at 1.9 A resolution. Biochemistry 1995, 34, 4325–4330. [Google Scholar] [CrossRef]
- Law, R.H.; Caradoc-Davies, T.; Cowieson, N.; Horvath, A.J.; Quek, A.J.; Encarnacao, J.A.; Steer, D.; Cowan, A.; Zhang, Q.; Lu, B.G.; et al. The X-ray crystal structure of full-length human plasminogen. Cell Rep. 2012, 1, 185–190. [Google Scholar] [CrossRef] [Green Version]
- Graille, M.; Pagano, M.; Rose, T.; Ravaux, M.R.; van Tilbeurgh, H. Zinc induces structural reorganization of gelatin binding domain from human fibronectin and affects collagen binding. Structure 2010, 18, 710–718. [Google Scholar] [CrossRef] [Green Version]
- Tochowicz, A.; Goettig, P.; Evans, R.; Visse, R.; Shitomi, Y.; Palmisano, R.G.; Ito, N.; Richter, K.; Maskos, K.; Franke, D.; et al. The dimer interface of the membrane type 1 matrix metalloproteinase hemopexin domain: Crystal structure and biological functions. J. Biol. Chem. 2011, 286, 7587–7600. [Google Scholar] [CrossRef] [Green Version]
- Zhou, A.; Huntington, J.A.; Pannu, N.S.; Carrell, R.W.; Read, R.J. How vitronectin binds PAI-1 to modulate fibrinolysis and cell migration. Nat. Struct. Biol. 2003, 10, 541–544. [Google Scholar] [CrossRef] [PubMed]
- Kjaergaard, M.; Gårdsvoll, H.; Hirschberg, D.; Nielbo, S.; Mayasundari, A.; Peterson, C.B.; Jansson, A.; Jørgensen, T.J.; Poulsen, F.M.; Ploug, M. Solution structure of recombinant somatomedin B domain from vitronectin produced in Pichia pastoris. Protein Sci. 2007, 16, 1934–1945. [Google Scholar] [CrossRef] [Green Version]
- Huai, Q.; Zhou, A.; Lin, L.; Mazar, A.P.; Parry, G.C.; Callahan, J.; Shaw, D.E.; Furie, B.; Furie, B.C.; Huang, M. Crystal structures of two human vitronectin, urokinase and urokinase receptor complexes. Nat. Struct. Mol. Biol. 2008, 15, 422–423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeffery, C.J. Multitalented actors inside and outside the cell: Recent discoveries add to the number of moonlighting proteins. Biochem. Soc. Trans. 2019, 47, 1941–1948. [Google Scholar] [CrossRef]
- Lee, P.Y.; Gam, L.H.; Yong, V.C.; Rosli, R.; Ng, K.P.; Chong, P.P. Identification of immunogenic proteins of Candida parapsilosis by serological proteome analysis. J. Appl. Microbiol. 2014, 116, 999–1009. [Google Scholar] [CrossRef] [PubMed]
- Lee, P.Y.; Gam, L.H.; Yong, V.C.; Rosli, R.; Ng, K.P.; Chong, P.P. Immunoproteomic analysis of antibody response to cell wall-associated proteins of Candida tropicalis. J. Appl. Microbiol. 2014, 117, 854–865. [Google Scholar] [CrossRef]
- Karkowska-Kuleta, J.; Zajac, D.; Bras, G.; Bochenska, O.; Seweryn, K.; Kędracka-Krok, S.; Jankowska, U.; Rapala-Kozik, M.; Kozik, A. Characterization of the interactions between human high-molecular-mass kininogen and cell wall proteins of pathogenic yeasts Candida tropicalis. Acta Biochim. Pol. 2016, 63, 427–436. [Google Scholar] [CrossRef] [Green Version]
- Karkowska-Kuleta, J.; Kulig, K.; Karnas, E.; Zuba-Surma, E.; Woznicka, O.; Pyza, E.; Kuleta, P.; Osyczka, A.; Rapala-Kozik, M.; Kozik, A. Characteristics of extracellular vesicles released by the pathogenic yeast-like fungi Candida glabrata, Candida parapsilosis and Candida tropicalis. Cells 2020, 9, 1722. [Google Scholar] [CrossRef]
- Dallo, S.F.; Kannan, T.R.; Blaylock, M.W.; Baseman, J.B. Elongation factor Tu and E1 βsubunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol. Microbiol. 2002, 46, 1041–1051. [Google Scholar] [CrossRef]
- Heilmann, C.; Hartleib, J.; Hussain, M.S.; Peters, G. The multifunctional Staphylococcus aureus autolysin aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect. Immun. 2005, 73, 4793–4802. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kinhikar, A.G.; Vargas, D.; Li, H.; Mahaffey, S.B.; Hinds, L.; Belisle, J.T.; Laal, S. Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol. Microbiol. 2006, 60, 999–1013. [Google Scholar] [CrossRef] [PubMed]
- Esgleas, M.; Li, Y.Y.; Hancock, M.A.; Hare, J.; Dubreui, J.D.; Gottschalk, M. Isolation and characterization of α-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 2008, 154, 2668–2679. [Google Scholar] [CrossRef] [Green Version]
- Dasari, P.; Koleci, N.; Shopova, I.A.; Wartenberg, D.; Beyersdorf, N.; Dietrich, S.; Sahagún-Ruiz, A.; Figge, M.T.; Skerka, C.; Brakhage, A.A.; et al. Enolase from Aspergillus fumigatus is a moonlighting protein that binds the human plasma complement proteins factor H, FHL-1, C4BP, and plasminogen. Front. Immunol. 2019, 10, 2573. [Google Scholar] [CrossRef] [Green Version]
- Seweryn, K.; Karkowska-Kuleta, J.; Wolak, N.; Bochenska, O.; Kedracka-Krok, S.; Kozik, A.; Rapala-Kozik, M. 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. 2015, 62, 825–835. [Google Scholar] [CrossRef]
- Donohue, D.S.; Ielasi, F.S.; Goossens, K.V.; Willaert, R.G. The N-terminal part of Als1 protein from Candida albicans specifically binds fucose-containing glycans. Mol. Microbiol. 2011, 80, 1667–1679. [Google Scholar] [CrossRef]
- Ielasi, F.S.; Verhaeghe, T.; Desmet, T.; Willaert, R.G. Engineering the carbohydrate-binding site of Epa1p from Candida glabrata: Generation of adhesin mutants with different carbohydrate specificity. Glycobiology 2014, 24, 1312–1322. [Google Scholar] [CrossRef] [Green Version]
- Zajac, D.; Karkowska-Kuleta, J.; Bochenska, O.; Rapala-Kozik, M.; Kozik, A. Interaction of human fibronectin with Candida glabrata epithelial adhesin 6 (Epa6). Acta Biochim. Pol. 2016, 63, 417–426. [Google Scholar] [CrossRef]
- Butterfield, D.A.; Lange, M.L. Multifunctional roles of enolase in Alzheimer’s disease brain: Beyond altered glucose metabolism. J. Neurochem. 2009, 111, 915–933. [Google Scholar] [CrossRef] [Green Version]
- Zakrzewicz, D.; Didiasova, M.; Krüger, M.; Giaimo, B.D.; Borggrefe, T.; Mieth, M.; Hocke, A.C.; Zakrzewicz, A.; Schaefer, L.; Preissner, K.T.; et al. Protein arginine methyltransferase 5 mediates enolase-1 cell surface trafficking in human lung adenocarcinoma cells. Biochim. Biophys. Acta Mol. Basis Dis. 2018, 1864, 1816–1827. [Google Scholar] [CrossRef]
- Shevade, S.; Jindal, N.; Dutta, S.; Jarori, G.K. Food vacuole associated enolase in plasmodium undergoes multiple post-translational modifications: Evidence for atypical ubiquitination. PLoS ONE 2013, 8, e72687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, E.; Brewer, J.M.; Minor, W.; Carreira, L.A.; Lebioda, L. Mechanism of enolase: The crystal structure of asymmetric dimer enolase-2-phospho-D-glycerate/enolase-phosphoenolpyruvate at 2.0 Å resolution. Biochemistry 1997, 36, 2526–12534. [Google Scholar] [CrossRef]
- Piccard, H.; Van den Steen, P.E.; Opdenakker, G. Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins. J. Leukoc. Biol. 2007, 81, 870–892. [Google Scholar] [CrossRef] [PubMed]
- Fox, D.; Smulian, A.G. Plasminogen-binding activity of enolase in the opportunistic pathogen Pneumocystis carinii. Med. Mycol. 2001, 39, 495–507. [Google Scholar] [CrossRef] [Green Version]
- Marcos, C.M.; Silva, J.F.; Oliveira, H.C.; Silva, R.A.M.; Mendes-Giannini, M.J.S.; Fusco-Almeida, A.M. Surface-Expressed enolase contributes to the adhesion of Paracoccidioides brasiliensis to host cells. FEMS Yeast Res. 2012, 12, 557–570. [Google Scholar] [CrossRef] [Green Version]
- Ceremuga, I.; Seweryn, E.; Bednarz-Misa, I.; Pietkiewicz, J.; Jermakow, K.; Banas, T.; Gamian, A. Enolase-like protein present on the outer membrane of Pseudomonas aeruginosa binds plasminogen. Folia Microbiol. 2014, 59, 391–397. [Google Scholar] [CrossRef] [Green Version]
- Bao, S.; Guo, X.; Yu, S.; Ding, J.; Tan, L.; Zhang, F.; Sun, Y.; Qiu, X.; Chen, G.; Ding, C. Mycoplasma synoviae enolase is a plasminogen/fibronectin binding protein. BMC Vet. Res. 2014, 10, 223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Derbise, A.; Song, Y.P.; Parikh, S.; Fischetti, V.A.; Pancholi, V. Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect. Immun. 2004, 72, 94–105. [Google Scholar] [CrossRef] [Green Version]
- Sha, J.; Erova, T.E.; Alyea, R.A.; Wang, S.; Olano, J.P.; Pancholi, V.; Chopra, A.K. Surface-Expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. J. Bacteriol. 2009, 191, 3095–3107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rahi, A.; Dhiman, A.; Singh, D.; Lynn, A.M.; Rehan, M.; Bhatnagar, R. Exploring the interaction between Mycobacterium tuberculosis enolase and human plasminogen using computational methods and experimental techniques. J. Cell. Biochem. 2017, 119, 2408–2417. [Google Scholar] [CrossRef]
- Bergmann, S.; Wild, D.; Diekmann, O.; Frank, R.; Bracht, D.; Chhatwal, G.S.; Hammerschmidt, S. Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumoniae. Mol. Microbiol. 2003, 49, 411–423. [Google Scholar] [CrossRef] [PubMed]
- Vanegas, G.; Quiñones, W.; Carrasco-López, C.; Concepción, J.L.; Albericio, F.; Avilán, L. Enolase as a plasminogen binding protein in Leishmania mexicana. Parasitol. Res. 2007, 101, 1511–1516. [Google Scholar] [CrossRef] [PubMed]
- Nogueira, S.V.; Fonseca, F.L.; Rodrigues, M.L.; Mundodi, V.; Abi-Chacra, E.A.; Winters, M.S.; Alderete, J.F.; de Almeida Soares, C.M. Paracoccidioides brasiliensis enolase is a surface protein that binds plasminogen and mediates interaction of yeast forms with host cells. Infect. Immun. 2010, 78, 4040–4050. [Google Scholar] [CrossRef] [Green Version]
- Ghosh, A.K.; Jacobs-Lorena, M. Surface-expressed enolases of Plasmodium and other pathogens. Mem. Inst. Oswaldo Cruz 2011, 106 (Suppl. 1), 85–90. [Google Scholar] [CrossRef] [Green Version]
- López-López, M.J.; Rodríguez-Luna, I.C.; Lara-Ramírez, E.E.; López-Hidalgo, M.; Benítez-Cardoza, C.G.; Guo, X. Biochemical and biophysical characterization of the enolase from Helicobacter pylori. Biomed. Res. Int. 2018, 17, 9538193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rios-Steiner, J.L.; Schenone, M.; Mochalkin, I.; Tulinsky, A.; Castellino, F.J. Structure and binding determinants of the recombinant kringle-2 domain of human plasminogen to an internal peptide from a group A Streptococcal surface protein. J. Mol. Biol. 2001, 308, 705–719. [Google Scholar] [CrossRef]
- Bhattacharya, S.; Ploplis, V.A.; Castellino, F.J. Bacterial plasminogen receptors utilize host plasminogen system for effective invasion and dissemination. J. Biomed. Biotechnol. 2012, 2012, 482096. [Google Scholar] [CrossRef] [Green Version]
- Vieira, M.L.; Vasconcellos, S.A.; Goncales, A.P.; de Morais, Z.M.; Nascimento, A.L. Plasminogen acquisition and activation at the surface of Leptospira species lead to fibronectin degradation. Infect. Immun. 2009, 77, 4092–4101. [Google Scholar] [CrossRef] [Green Version]
- Ballantyne, D.S.; Warmington, J.R. Purification of native enolase from medically important Candida species. Biotechnol. Appl. Biochem. 2000, 31, 213–218. [Google Scholar] [CrossRef] [PubMed]
- Rapala-Kozik, M.; Karkowska, J.; Jacher, A.; Golda, A.; Barbasz, A.; Guevara-Lora, I.; Kozik, A. Kininogen adsorption to the cell surface of Candida spp. Int. Immunopharmacol. 2008, 8, 237–241. [Google Scholar] [CrossRef]
- Xu, H.; Freitas, M.A. MassMatrix: A database search program for rapid characterization of proteins and peptides from tandem mass spectrometry data. Proteomics 2009, 9, 1548–1555. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Madeira, F.; Park, Y.M.; Lee, J.; Buso, N.; Gur, T.; Madhusoodanan, N.; Basutkar, P.; Tivey, A.R.N.; Potter, S.C.; Finn, R.D.; et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019, 47, W636–W641. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sali, A.; Blundell, T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234, 779–815. [Google Scholar] [CrossRef] [PubMed]
- Vajda, S.; Yueh, C.; Beglov, D.; Bohnuud, T.; Mottarella, S.E.; Xia, B.; Hall, D.R.; Kozakov, D. New additions to the ClusPro server motivated by CAPRI. Proteins 2017, 85, 435–444. [Google Scholar] [CrossRef] [Green Version]
- Kozakov, D.; Hall, D.R.; Xia, B.; Porter, K.A.; Padhorny, D.; Yueh, C.; Beglov, D.; Vajda, S. The ClusPro web server for protein-protein docking. Nat. Protoc. 2017, 12, 255–278. [Google Scholar] [CrossRef]
Human Protein | Enolase Origin | KD [M] | ka [1/Ms] | kd [1/s] |
---|---|---|---|---|
VTR | C. albicans, cell wall | 3.11 × 10−8 ± 4.58 × 10−10 | 1.34 × 105 ± 2.52 × 103 | 4.17 × 10−3 ± 7.63 × 10−5 |
VTR | C. albicans, cytosol | 5.53 × 10−8 ± 2.43 × 10−9 | 8.91 × 104 ± 5.06 × 103 | 4.93 × 10−3 ± 9.12 × 10−5 |
VTR | C. tropicalis, cytosol | 6.83 × 10−7 ± 4.39 × 10−8 | 1.34 × 104 ± 1.11 × 103 | 9.15 × 10−3 ± 5.96 × 10−4 |
FN | C. albicans, cell wall | 3.68 × 10−8 ± 3.26 × 10−9 | 6.03 × 104 ± 1.45 × 103 | 2.22 × 10−3 ± 6.74 × 10−5 |
FN | C. albicans, cytosol | 4.28 × 10−8 ± 3.74 × 10−9 | 6.47 × 105 ± 9.84 × 103 | 2.77 × 10−2 ± 3.58 × 10−3 |
FN | C. tropicalis, cytosol | 5.18 × 10−8 ± 8.54 × 10−10 | 5.48 × 104 ± 8.41 × 102 | 2.84 × 10−3 ± 6.04 × 10−5 |
HPG | C. albicans, cell wall | 1.20 × 10−7 ± 4.25 × 10−6 | 5.22 × 105 ± 4.84 × 104 | 6.26 × 10−2 ± 2.26 × 10−3 |
HPG | C. albicans, cytosol | 2.57 × 10−7 ± 4.17 × 10−6 | 2.70 × 105 ± 1.92 × 104 | 6.93 × 10−2 ± 1.30 × 10−3 |
HPG | C. tropicalis, cytosol | 2.53 × 10−7 ± 2.06 × 10−6 | 5.77 × 104 ± 6.84 × 103 | 1.46 × 10−2 ± 2.18 × 10−1 |
Peptides of C. albicans Enolase | Peptides of C. tropicalis Enolase |
---|---|
VTR-Bnding | |
236KAGYKGKVGIAMD248 243VGIAMDVASSEFYKDGKYDLDFK265 330NPTRIKTAIEK340 419IEEELGSEAIYAGK432 | 236QAGHTGKVKIAMDPASSE253 245IAMDPASSEFFKDGKYDLDFK265 334IKKAIEKK341 |
FN-Binding | |
52DGDKSK57 107LGANAILGVSLAAANAAAAAQGIPLYKHIANISNAKK143 187IGSEVYHNLK196 240KGKVGIAMDVASSEFYKDGK259 | 245IAMDPASSEFFKDGKYDLDFK265 334IKKAIEKK341 |
HPG-Binding | |
30GLFRSIVPSGASTGVHEALELRDGDK55 56SKWLGKGVLK65 107LGANAILGVSLAAANAAAAAQGIPLYK133 237AGYKGKVGIAMDVASSEFYKDGK259 | 106KLGANAILGVSLAAA120 222TPEEALDLIVESIEQAGHTGK242 245IAMDPASSEFFKDGK259 |
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Satala, D.; Satala, G.; Karkowska-Kuleta, J.; Bukowski, M.; Kluza, A.; Rapala-Kozik, M.; Kozik, A. Structural Insights into the Interactions of Candidal Enolase with Human Vitronectin, Fibronectin and Plasminogen. Int. J. Mol. Sci. 2020, 21, 7843. https://doi.org/10.3390/ijms21217843
Satala D, Satala G, Karkowska-Kuleta J, Bukowski M, Kluza A, Rapala-Kozik M, Kozik A. Structural Insights into the Interactions of Candidal Enolase with Human Vitronectin, Fibronectin and Plasminogen. International Journal of Molecular Sciences. 2020; 21(21):7843. https://doi.org/10.3390/ijms21217843
Chicago/Turabian StyleSatala, Dorota, Grzegorz Satala, Justyna Karkowska-Kuleta, Michal Bukowski, Anna Kluza, Maria Rapala-Kozik, and Andrzej Kozik. 2020. "Structural Insights into the Interactions of Candidal Enolase with Human Vitronectin, Fibronectin and Plasminogen" International Journal of Molecular Sciences 21, no. 21: 7843. https://doi.org/10.3390/ijms21217843