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Research Paper

Haemophilus parasuis α-2,3-sialyltransferase-mediated lipooligosaccharide sialylation contributes to bacterial pathogenicity

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Pages 1247-1262 | Received 02 May 2018, Accepted 12 Jul 2018, Published online: 12 Aug 2018

References

  • Oliveira S, Pijoan C. Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet Microbiol. 2004;99:1–12.
  • Huang J, Wang X, Cao Q, et al. ClpP participates in stress tolerance and negatively regulates biofilm formation in Haemophilus parasuis. Vet Microbiol. 2016;182:141–149.
  • Cai X, Chen H, Blackall PJ, et al. Serological characterization of Haemophilus parasuis isolates from China. Vet Microbiol. 2005;111:231–236.
  • Rubies X, Kielstein P, Costa L, et al. Prevalence of Haemophilus parasuis serovars isolated in Spain from 1993 to 1997. Vet Microbiol. 1999;66:245–248.
  • Lichtensteiger CA, Vimr ER. Purification and renaturation of membrane neuraminidase from Haemophilus parasuis. Vet Microbiol. 2003;93:79–87.
  • Lichtensteiger CA, Vimr ER. Neuraminidase (sialidase) activity of Haemophilus parasuis. FEMS Microbiol Lett. 1997;152:269–274.
  • Honke K, Taniguchi N. Sulfotransferases and sulfated oligosaccharides. Med Res Rev. 2002;22:637–654.
  • Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, et al. The human sialyltransferase family. Biochimie. 2001;83:727–737.
  • Brockhausen I. Crossroads between bacterial and mammalian glycosyltransferases. Front Immunol. 2014;5:492.
  • Houliston RS, Vinogradov E, Dzieciatkowska M, et al. Lipooligosaccharide of Campylobacter jejuni: similarity with multiple types of mammalian glycans beyond gangliosides. J Biol Chem. 2011;286:12361–12370.
  • Whitfield C, Trent MS. Biosynthesis and export of bacterial lipopolysaccharides. Annu Rev Biochem. 2014;83:99–128.
  • Yuki N, Odaka M. Ganglioside mimicry as a cause of Guillain-Barre syndrome. Curr Opin Neurol. 2005;18:557–561.
  • Varki A. Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature. 2007;446:1023–1029.
  • Rosen SD. Ligands for L-selectin: homing, inflammation, and beyond. Annu Rev Immunol. 2004;22:129–156.
  • Stencel-Baerenwald JE, Reiss K, Reiter DM, et al. The sweet spot: defining virus-sialic acid interactions. Nat Rev Microbiol. 2014;12:739–749.
  • Lopez PH, Schnaar RL. Gangliosides in cell recognition and membrane protein regulation. Curr Opin Struct Biol. 2009;19:549–557.
  • Martinez-Moliner V, Soler-Llorens P, Moleres J, et al. Distribution of genes involved in sialic acid utilization in strains of Haemophilus parasuis. Microbiology. 2012;158:2117–2124.
  • Li Y, Chen X. Sialic acid metabolism and sialyltransferases: natural functions and applications. App Microbiol Biotechnol. 2012;94:887–905.
  • Cantarel BL, Coutinho PM, Rancurel C, et al. The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 2009;37:D233–D238.
  • Xu Z, Yue M, Zhou R, et al. Genomic characterization of Haemophilus parasuis SH0165, a highly virulent strain of serovar 5 prevalent in China. PloS One. 2011;6:e19631.
  • Freiberger F, Claus H, Gunzel A, et al. Biochemical characterization of a Neisseria meningitidis polysialyltransferase reveals novel functional motifs in bacterial sialyltransferases. Mol Microbiol. 2007;65:1258–1275.
  • Labandeira-Rey M, Brautigam CA, Hansen EJ. Characterization of the CpxRA regulon in Haemophilus ducreyi. Infect Immun. 2010;78:4779–4791.
  • Macedo N, Rovira A, Torremorell M. Haemophilus parasuis: infection, immunity and enrofloxacin. Vet Res. 2015;46:128.
  • Vahle JL, Haynes JS, Andrews JJ. Experimental reproduction of Haemophilus parasuis infection in swine: clinical, bacteriological, and morphologic findings. J Vet Diagn Invest. 1995;7:476–480.
  • Pomorska-Mol M, Markowska-Daniel I, Rachubik J, et al. Effect of maternal antibodies and pig age on the antibody response after vaccination against Glässers disease. Vet Res Commun. 2011;35:337–343.
  • Oliveira S, Pijoan C, Morrison R. Evaluation of Haemophilus parasuis control in the nursery using vaccination and controlled exposure. J Swine Health Prod. 2004;12:123–128.
  • Olvera A, Cerda-Cuellar M, Nofrarias M, et al. Dynamics of Haemophilus parasuis genotypes in a farm recovered from an outbreak of Glässer’s disease. Vet Microbiol. 2007;123:230–237.
  • Pomorska-Mol M, Dors A, Kwit K, et al. Coinfection modulates inflammatory responses, clinical outcome and pathogen load of H1N1 swine influenza virus and Haemophilus parasuis infections in pigs. BMC Vet Res. 2017;13:376.
  • Bouchet B, Vanier G, Jacques M, et al. Interactions of Haemophilus parasuis and its LOS with porcine brain microvascular endothelial cells. Vet Res. 2008;39:42.
  • Bouchet B, Vanier G, Jacques M, et al. Studies on the interactions of Haemophilus parasuis with porcine epithelial tracheal cells: limited role of LOS in apoptosis and pro-inflammatory cytokine release. Microb Pathog. 2009;46:108–113.
  • Frandoloso R, Martinez-Martinez S, Gutierrez-Martin CB, et al. Haemophilus parasuis serovar 5 Nagasaki strain adheres and invades PK-15 cells. Vet Microbiol. 2012;154:347–352.
  • Mullins MA, Register KB, Bayles DO, et al. Haemophilus parasuis exhibits IgA protease activity but lacks homologs of the IgA protease genes of Haemophilus influenzae. Vet Microbiol. 2011;153:407–412.
  • Cerda-Cuellar M, Aragon V. Serum-resistance in Haemophilus parasuis is associated with systemic disease in swine. Vet J. 2008;175:384–389.
  • Olvera A, Ballester M, Nofrarias M, et al. Differences in phagocytosis susceptibility in Haemophilus parasuis strains. Vet Res. 2009;40:24.
  • Costa-Hurtado M, Ballester M, Galofre-Mila N, et al. VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages. Vet Res. 2012;43:57.
  • Angata T, Varki A. Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev. 2002;102:439–469.
  • Hood DW, Cox AD, Gilbert M, et al. Identification of a lipopolysaccharide alpha-2,3-sialyltransferase from Haemophilus influenzae. Mol Microbiol. 2001;39:341–350.
  • Gao L, Linden L, Parsons NJ, et al. Uptake of metabolites by gonococci grown with lactate in a medium containing glucose: evidence for a surface location of the sialyltransferase. Microb Pathog. 2000;28:257–266.
  • Mandrell RE, Lesse AJ, Sugai JV, et al. In vitro and in vivo modification of Neisseria gonorrhoeae lipooligosaccharide epitope structure by sialylation. J Exp Med. 1990;171:1649–1664.
  • Vimr E, Lichtensteiger C. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 2002;10:254–257.
  • Schilling B, Goon S, Samuels NM, et al. Biosynthesis of sialylated lipooligosaccharides in Haemophilus ducreyi is dependent on exogenous sialic acid and not mannosamine. Incorporation studies using N-acylmannosamine analogues, N-glycolylneuraminic acid, and 13C-labeled N-acetylneuraminic acid. Biochemistry. 2001;40:12666–12677.
  • Inzana TJ, Glindemann G, Cox AD, et al. Incorporation of N-acetylneuraminic acid into Haemophilus somnus lipooligosaccharide (LOS): enhancement of resistance to serum and reduction of LOS antibody binding. Infect Immun. 2002;70:4870–4879.
  • Janda JM, Oshiro LS, Abbott SL, et al. Virulence markers of mesophilic aeromonads: association of the autoagglutination phenomenon with mouse pathogenicity and the presence of a peripheral cell-associated layer. Infect Immun. 1987;55:3070–3077.
  • Hamann J, Aust G, Arac D, et al. International union of basic and clinical pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol Rev. 2015;67:338–367.
  • Uenishi H, Eguchi-Ogawa T, Shinkai H, et al. PEDE (Pig EST Data Explorer) has been expanded into Pig Expression Data Explorer, including 10 147 porcine full-length cDNA sequences. Nucleic Acids Res. 2007;35:D650–D653.
  • Parsons NJ, Patel PV, Tan EL, et al. Cytidine 5ʹ-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum. Microb Pathog. 1988;5:303–309.
  • Lewis LA, Gulati S, Burrowes E, et al. alpha-2,3-sialyltransferase expression level impacts the kinetics of lipooligosaccharide sialylation, complement resistance, and the ability of Neisseria gonorrhoeae to colonize the murine genital tract. MBio. 2015;6:e02465-1.
  • Ram S, McQuillen DP, Gulati S, et al. Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J Exp Med. 1998;188:671–680.
  • Zaleski A, Scheffler NK, Densen P, et al. Lipooligosaccharide P(k) (Galalpha1-4Galbeta1-4Glc) epitope of moraxella catarrhalis is a factor in resistance to bactericidal activity mediated by normal human serum. Infect Immun. 2000;68:5261–5268.
  • Altschul SF, Madden TL, Schaffer AA, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402.
  • Zhang B, Feng S, Xu C, et al. Serum resistance in Haemophilus parasuis SC096 strain requires outer membrane protein P2 expression. FEMS Microbiol Lett. 2012;326:109–115.
  • Zhang B, He Y, Xu C, et al. Cytolethal distending toxin (CDT) of the Haemophilus parasuis SC096 strain contributes to serum resistance and adherence to and invasion of PK-15 and PUVEC cells. Vet Microbiol. 2012;157:237–242.
  • Hitchcock PJ, Brown TM. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol. 1983;154:269–277.
  • Frandoloso R, Pivato M, Martinez-Martinez S, et al. Differences in Haemophilus parasuis adherence to and invasion of AOC-45 porcine aorta endothelial cells. BMC Vet Res. 2013;9:207.
  • Ram S, Sharma AK, Simpson SD, et al. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J Exp Med. 1998;187:743–752.