Characterization of novel bangle lectin from Photorhabdus asymbiotica with dual sugar-binding specificity and its effect on host immunity
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28806750
PubMed Central
PMC5584973
DOI
10.1371/journal.ppat.1006564
PII: PPATHOGENS-D-17-00229
Knihovny.cz E-zdroje
- MeSH
- bakteriální proteiny genetika imunologie MeSH
- interakce hostitele a patogenu imunologie MeSH
- konformace proteinů MeSH
- krystalografie rentgenová MeSH
- lektiny chemie genetika imunologie MeSH
- lidé MeSH
- molekulární sekvence - údaje MeSH
- Photorhabdus genetika imunologie MeSH
- povrchová plasmonová rezonance MeSH
- sekvence nukleotidů MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
- fucose-binding lectin MeSH Prohlížeč
- lektiny MeSH
Photorhabdus asymbiotica is one of the three recognized species of the Photorhabdus genus, which consists of gram-negative bioluminescent bacteria belonging to the family Morganellaceae. These bacteria live in a symbiotic relationship with nematodes from the genus Heterorhabditis, together forming a complex that is highly pathogenic for insects. Unlike other Photorhabdus species, which are strictly entomopathogenic, P. asymbiotica is unique in its ability to act as an emerging human pathogen. Analysis of the P. asymbiotica genome identified a novel fucose-binding lectin designated PHL with a strong sequence similarity to the recently described P. luminescens lectin PLL. Recombinant PHL exhibited high affinity for fucosylated carbohydrates and the unusual disaccharide 3,6-O-Me2-Glcβ1-4(2,3-O-Me2)Rhaα-O-(p-C6H4)-OCH2CH2NH2 from Mycobacterium leprae. Based on its crystal structure, PHL forms a seven-bladed β-propeller assembling into a homo-dimer with an inter-subunit disulfide bridge. Investigating complexes with different ligands revealed the existence of two sets of binding sites per monomer-the first type prefers l-fucose and its derivatives, whereas the second type can bind d-galactose. Based on the sequence analysis, PHL could contain up to twelve binding sites per monomer. PHL was shown to interact with all types of red blood cells and insect haemocytes. Interestingly, PHL inhibited the production of reactive oxygen species induced by zymosan A in human blood and antimicrobial activity both in human blood, serum and insect haemolymph. Concurrently, PHL increased the constitutive level of oxidants in the blood and induced melanisation in haemolymph. Our results suggest that PHL might play a crucial role in the interaction of P. asymbiotica with both human and insect hosts.
Central European Institute of Technology Masaryk University Brno Czech Republic
Department of Biochemistry Faculty of Science Masaryk University Brno Czech Republic
National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czech Republic
Zobrazit více v PubMed
Gerrard J, Waterfield N, Vohra R, ffrench-Constant R. Human infection with Photorhabdus asymbiotica: an emerging bacterial pathogen. Microbes Infect. 2004. February;6(2):229–37. PubMed
Waterfield NR, Ciche T, Clarke D. Photorhabdus and a host of hosts. Annu Rev Microbiol. 2009. June;63:557–74. doi: 10.1146/annurev.micro.091208.073507 PubMed DOI
Costa SCP, Girard PA, Brehélin M, Zumbihl R. The emerging human pathogen Photorhabdus asymbiotica is a facultative intracellular bacterium and induces apoptosis of macrophage-like cells. Infect Immun. 2009. March;77(3):1022–30. doi: 10.1128/IAI.01064-08 PubMed DOI PMC
Gerrard JG, Waterfield NR, Sanchez-Contreeras M. Photorhabdus asymbiotica: Shedding light on a human pathogenic bioluminescent bacterium. Clin Microbiol Newsl. 2011. July;33(14):103–9.
Mulley G, Beeton ML, Wilkinson P, Vlisidou I, Ockendon-Powell N, Hapeshi A, et al. From insect to man: Photorhabdus sheds light on the emergence of human pathogenicity. PloS One. 2015. December;10(12):e0144937 doi: 10.1371/journal.pone.0144937 PubMed DOI PMC
Costa SCP, Chavez CV, Jubelin G, Givaudan A, Escoubas J-M, Brehélin M, et al. Recent insight into the pathogenicity mechanisms of the emergent pathogen Photorhabdus asymbiotica. Microbes Infect. 2010. March;12(3):182–9. doi: 10.1016/j.micinf.2009.12.003 PubMed DOI
Wilkinson P, Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, Vlisidou I, et al. Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics. 2009. July;10(1):302. PubMed PMC
Wilkinson P, Paszkiewicz K, Moorhouse A, Szubert JM, Beatson S, Gerrard J, et al. New plasmids and putative virulence factors from the draft genome of an Australian clinical isolate of Photorhabdus asymbiotica: New plasmids and virulence factors in P. asymbiotica genome. FEMS Microbiol Lett. 2010. June;309:136–143. doi: 10.1111/j.1574-6968.2010.02030.x PubMed DOI
Eleftherianos I, ffrench-Constant RH, Clarke DJ, Dowling AJ, Reynolds SE. Dissecting the immune response to the entomopathogen Photorhabdus. Trends Microbiol. 2010. December;18(12):552–60. doi: 10.1016/j.tim.2010.09.006 PubMed DOI
Forst S, Dowds B, Boemare N, Stackebrandt E. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol. 1996. March;51:47–72. PubMed
Waterfield NR, Sanchez-Contreras M, Eleftherianos I, Dowling A, Yang G, Wilkinson P, et al. Rapid Virulence Annotation (RVA): identification of virulence factors using a bacterial genome library and multiple invertebrate hosts. Proc Natl Acad Sci U S A. 2008. October;105(41):15967–72. doi: 10.1073/pnas.0711114105 PubMed DOI PMC
Saint André Av, Blackwell NM, Hall LR, Hoerauf A, Brattig NW, Volkmann L, et al. The role of endosymbiotic Wolbachia bacteria in the pathogenesis of river blindness. Science. 2002. March;295(5561):1892–5. doi: 10.1126/science.1068732 PubMed DOI
Cross HF, Haarbrink M, Egerton G, Yazdanbakhsh M, Taylor MJ. Severe reactions to filarial chemotherapy and release of Wolbachia endosymbionts into blood. Lancet Lond Engl. 2001. December;358(9296):1873–5. PubMed
Brattig NW, Bazzocchi C, Kirschning CJ, Reiling N, Buttner DW, Ceciliani F, et al. The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune responses through TLR2 and TLR4. J Immunol. 2004. July;173(1):437–45. PubMed
Gerrard JG, Joyce SA, Clarke DJ, ffrench-Constant RH, Nimmo GR, Looke DFM, et al. Nematode symbiont for Photorhabdus asymbiotica. Emerg Infect Dis. 2006. October;12(10):1562–4. doi: 10.3201/eid1210.060464 PubMed DOI PMC
Imberty A, Varrot A. Microbial recognition of human cell surface glycoconjugates. Curr Opin Struct Biol. 2008. October;18(5):567–76. doi: 10.1016/j.sbi.2008.08.001 PubMed DOI
Pieters RJ. Carbohydrate mediated bacterial adhesion. Adv Exp Med Biol. 2011. March;715:227–40. doi: 10.1007/978-94-007-0940-9_14 PubMed DOI
Sharon N. Lectins: carbohydrate-specific reagents and biological recognition molecules. J Biol Chem. 2007. February;282(5):2753–64. doi: 10.1074/jbc.X600004200 PubMed DOI
Berg JM, Tymoczko JL, Stryer L, Stryer L. Biochemistry. 5th ed New York: W.H. Freeman; 2002. 1 p.
Sharon N, Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology. 2004. November;14(11):53R–62R. doi: 10.1093/glycob/cwh122 PubMed DOI
Kumar A, Sýkorová P, Demo G, Dobeš P, Hyršl P, Wimmerová M. A Novel fucose-binding lectin from Photorhabdus luminescens (PLL) with an unusual hepta-bladed β-propeller tetrameric structure. J Biol Chem. 2016. October;291:25032–49. doi: 10.1074/jbc.M115.693473 PubMed DOI PMC
Hunter SW, Fujiwara T, Brennan PJ. Structure and antigenicity of the major specific glycolipid antigen of Mycobacterium leprae. J Biol Chem. 1982. December;257(24):15072–8. PubMed
Kondakov NN, Mel´nikova TM, Chekryzhova TV, Mel´nikova MV, Zinin AI, Torgov VI, et al. Synthesis of a disaccharide of phenolic glycolipid from Mycobacterium leprae (PGL-I) and its conjugates with bovine serum albumin. Russ Chem Bull. 2015. May;64(5):1142–8.
Brautigam CA. Calculations and publication-quality illustrations for analytical ultracentrifugation data. Methods Enzymol. 2015. June;562:109–33. doi: 10.1016/bs.mie.2015.05.001 PubMed DOI
Hyršl P, Číž M, Kubala L, Lojek A. Silkworm (Bombyx mori) hemocytes do not produce reactive oxygen metabolites as a part of defense mechanisms. Folia Microbiol (Praha). 2004. May;49(3):315–9. PubMed
Glupov VV, Khvoshevskaya MF, Lozinskaya YL, Dubovski IM, Martemyanov VV, Sokolova JY. Application of the nitroblue tetrazolium-reduction method for studies on the production of reactive oxygen species in insect haemocytes. Cytobios. 2001. February;106 Suppl 2:165–78. PubMed
Cerenius L, Söderhäll K. The prophenoloxidase-activating system in invertebrates. Immunol Rev. 2004. April;198:116–26. PubMed
Šulák O, Cioci G, Lameignère E, Balloy V, Round A, Gutsche I, et al. Burkholderia cenocepacia BC2L-C is a super lectin with dual specificity and proinflammatory activity. Saper MA, editor. PLoS Pathog. 2011. September;7(9):e1002238 doi: 10.1371/journal.ppat.1002238 PubMed DOI PMC
Shimokawa M, Haraguchi T, Minami Y, Yagi F, Hiemori K, Tateno H, et al. Two carbohydrate recognizing domains from Cycas revoluta leaf lectin show the distinct sugar-binding specificity—A unique mannooligosaccharide recognition by N-terminal domain. J Biochem. 2016. July;160(1):27–35. doi: 10.1093/jb/mvw011 PubMed DOI
Nakamura-Tsuruta S, Kominami J, Kuno A, Hirabayashi J. Evidence that Agaricus bisporus agglutinin (ABA) has dual sugar-binding specificity. Biochem Biophys Res Commun. 2006. August;347(1):215–20. doi: 10.1016/j.bbrc.2006.06.073 PubMed DOI
Leonidas DD, Swamy BM, Hatzopoulos GN, Gonchigar SJ, Chachadi VB, Inamdar SR, et al. Structural basis for the carbohydrate recognition of the Sclerotium rolfsii lectin. J Mol Biol. 2007. May;368(4):1145–61. doi: 10.1016/j.jmb.2007.02.092 PubMed DOI
Wimmerova M, Mitchell E, Sanchez J-F, Gautier C, Imberty A. Crystal structure of fungal lectin: six-bladed beta-propeller fold and novel fucose recognition mode for Aleuria aurantia lectin. J Biol Chem. 2003. July;278(29):27059–67. doi: 10.1074/jbc.M302642200 PubMed DOI
Houser J, Komarek J, Cioci G, Varrot A, Imberty A, Wimmerova M. Structural insights into Aspergillus fumigatus lectin specificity: AFL binding sites are functionally non-equivalent. Acta Crystallogr D Biol Crystallogr. 2015. March;71(3):442–53. PubMed
Kostlánová N, Mitchell EP, Lortat-Jacob H, Oscarson S, Lahmann M, Gilboa-Garber N, et al. The fucose-binding lectin from Ralstonia solanacearum. A new type of beta-propeller architecture formed by oligomerization and interacting with fucoside, fucosyllactose, and plant xyloglucan. J Biol Chem. 2005. July;280(30):27839–49. doi: 10.1074/jbc.M505184200 PubMed DOI
Audfray A, Claudinon J, Abounit S, Ruvoen-Clouet N, Larson G, Smith DF, et al. Fucose-binding lectin from opportunistic pathogen Burkholderia ambifaria binds to both plant and human oligosaccharidic epitopes. J Biol Chem. 2012. February;287(6):4335–47. doi: 10.1074/jbc.M111.314831 PubMed DOI PMC
Staudacher E. Methylation—an uncommon modification of glycans. Biol Chem. 2012. August;393(8):675–85. doi: 10.1515/hsz-2012-0132 PubMed DOI PMC
Wohlschlager T, Butschi A, Grassi P, Sutov G, Gauss R, Hauck D, et al. Methylated glycans as conserved targets of animal and fungal innate defense. Proc Natl Acad Sci. 2014. July;111(27):E2787–96. doi: 10.1073/pnas.1401176111 PubMed DOI PMC
Dam TK, Brewer CF. Lectins as pattern recognition molecules: the effects of epitope density in innate immunity. Glycobiology. 2010. March;20(3):270–9. doi: 10.1093/glycob/cwp186 PubMed DOI
Au C, Dean P, Reynolds SE, ffrench-Constant RH. Effect of the insect pathogenic bacterium Photorhabdus on insect phagocytes. Cell Microbiol. 2004. January;6(1):89–95. PubMed
Shokal U, Eleftherianos I. Thioester-containing Protein-4 regulates the Drosophila immune signaling and function against the pathogen Photorhabdus. J Innate Immun. 2016. October; 9 (1):83–93. doi: 10.1159/000450610 PubMed DOI PMC
Cooper NR, Nemerow GR. Complement effector mechanisms in health and disease. J Invest Dermatol. 1985. July;85(1 Suppl):39s–46s. PubMed
Sarma JV, Ward PA. The complement system. Cell Tissue Res. 2011. January;343(1):227–35. doi: 10.1007/s00441-010-1034-0 PubMed DOI PMC
Ashida M., Yamazaki H. I. Biochemistry of the phenoloxidase system in insects: with special reference to its activation Molting and Metamorphosis (Ed. by Ohinishi E. & Ishizki H.). Jpn Sci Soc Press; Tokyo: 1990;(Berlin: Springer-Verlag):239–65.
Held KG, LaRock CN, D’Argenio DA, Berg CA, Collins CM. A metalloprotease secreted by the insect pathogen Photorhabdus luminescens induces melanization. Appl Environ Microbiol. 2007. December;73(23):7622–8. doi: 10.1128/AEM.01000-07 PubMed DOI PMC
Wiseman T, Williston S, Brandts JF, Lin L-N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem. 1989. May;179(1):131–7. PubMed
Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J. 2000. March;78(3):1606–19. doi: 10.1016/S0006-3495(00)76713-0 PubMed DOI PMC
Schuck P. On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal Biochem. 2003. September;320(1):104–24. PubMed
Mueller U, Darowski N, Fuchs MR, Förster R, Hellmig M, Paithankar KS, et al. Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J Synchrotron Radiat. 2012. May;19(Pt 3):442–9. doi: 10.1107/S0909049512006395 PubMed DOI PMC
Krug M, Weiss MS, Heinemann U, Mueller U. XDSAPP: a graphical user interface for the convenient processing of diffraction data using XDS. J Appl Crystallogr. 2012. June;45(3):568–72.
Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, et al. Overview of the CCP 4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011. April;67(4):235–42. PubMed PMC
Kelley LA, Sternberg MJE. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009. February;4(3):363–71. doi: 10.1038/nprot.2009.2 PubMed DOI
Vagin A, Teplyakov A. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr. 2010. January;66(1):22–5. PubMed
Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, et al. REFMAC 5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr. 2011. April;67(4):355–67. PubMed PMC
Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010. April;66(4):486–501. PubMed PMC
Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr. 2010. January;66(1):12–21. PubMed PMC
Adamová L, Malinovská L, Wimmerová M. New sensitive detection method for lectin hemagglutination using microscopy. Microsc Res Tech. 2014. October;77(10):841–9. doi: 10.1002/jemt.22407 PubMed DOI
Haydak M. H. A food for rearing laboratory animals. J Econ Entomol. 1936;29:1026.
Buchtíková S, Šimková A, Rohlenová K, Flajšhans M, Lojek A, Lilius E-M, et al. The seasonal changes in innate immunity of the common carp (Cyprinus carpio). Aquaculture. 2011. July;318(1–2):169–75.
Atosuo J, Lehtinen J, Vojtek L, Lilius E-M. Escherichia coli K-12 (pEGFPluxABCDEamp): a tool for analysis of bacterial killing by antibacterial agents and human complement activities on a real-time basis. Lumin J Biol Chem Lumin. 2013. October;28(5):771–9. PubMed
Vojtek L, Dobes P, Buyukguzel E, Atosuo J, Hyrsl P. Bioluminescent assay for evaluating antimicrobial activity in insect haemolymph. Eur J Entomol. 2014. July;111(3):335–40.
Panzarino O, Hyršl P, Dobeš P, Vojtek L, Vernile P, Bari G, et al. Rank-based biomarker index to assess cadmium ecotoxicity on the earthworm Eisenia andrei. Chemosphere. 2016. February;145:480–6. doi: 10.1016/j.chemosphere.2015.11.077 PubMed DOI
Ashida M, Söderhäll K. The prophenoloxidase activating system in crayfish. Comp Biochem Physiol Part B Comp Biochem. 1984. January;77(1):21–6.