Assessing the function of pneumococcal neuraminidases NanA, NanB and NanC in in vitro and in vivo lung infection models using monoclonal antibodies

References

• Henriques-Normark B, Tuomanen EI. The pneumococcus : epidemiology, microbiology, and pathogenesis. Cold Spring Harb Perpect Med. 2013;3:1–16.
   Web of Science ®Google Scholar
• Tong N Background Paper 6.22 Pneumonia. WHO 2013.
   Google Scholar
• Waight PA, Andrews NJ, Ladhani SN, et al. Effect of the 13-valent pneumococcal conjugate vaccine on invasive pneumococcal disease in England and Wales 4 years after its introduction: an observational cohort study. Lancet Infect Dis. 2015;15:535–543.
   PubMed Web of Science ®Google Scholar
• Naucler P, Galanis I, Morfeldt E, et al. Comparison of the impact of pneumococcal conjugate vaccine 10 or pneumococcal conjugate vaccine 13 on invasive pneumococcal disease in equivalent populations. Clin Infect Dis. 2017;65:1780–1789.
   PubMed Web of Science ®Google Scholar
• Jackson LA, Janoff EN. Pneumococcal vaccination of elderly adults: new paradigms for protection. Clin Infect Dis. 2008;47:1328–1338.
   PubMed Web of Science ®Google Scholar
• Pitsiou GG, Kioumis IP. Pneumococcal vaccination in adults: does it really work? Respir Med. 2011;105:1776–1783.
   PubMed Web of Science ®Google Scholar
• Bonten MJM, Huijts SM, Bolkenbaas M, et al. Polysaccharide conjugate vaccine against pneumococcal pneumonia in adults. N Engl J Med. 2015;372:1114–1125.
   PubMed Web of Science ®Google Scholar
• Weinberger DM, Malley R, Lipsitch M. Serotype replacement in disease following pneumococcal vaccination: a discussion of the evidence. Lancet. 2011;378:1962–1973.
   PubMed Web of Science ®Google Scholar
• Keller LE, Robinson DA, McDaniel LS. Nonencapsulated Streptococcus pneumoniae: emergence and pathogenesis. mBio. 2016;7:1–12.
   Web of Science ®Google Scholar
• Kim L, Mcgee L, Tomczyk S, et al. Biological and epidemiological features of antibiotic-resistant Streptococcus pneumoniae in pre- and post-conjugate vaccine eras: a United States perspective. Clin Microbiol Rev. 2016;29:525–552.
   PubMed Web of Science ®Google Scholar
• Paton JC, Lock RA, Hansman DJ. Effect of immunization with pneumolysin on survival time of mice challenged with Streptococcus pneumoniae. Infect Immun. 1983;40:548–552.
   PubMed Web of Science ®Google Scholar
• García-Suárez MM, Cima-Cabal MD, Flórez N, et al. Protection against pneumococcal pneumonia in mice by monoclonal antibodies to pneumolysin. Infect Immun. 2004;72:4534–4540.
   PubMed Web of Science ®Google Scholar
• Mitchell AM, Mitchell TJ. Streptococcus pneumoniae: virulence factors and variation. Clin Microbiol Infect. 2010;16:411–418.
   PubMed Web of Science ®Google Scholar
• Dockrell DH, Whyte MKB, Mitchell TJ. Pneumococcal pneumonia: mechanisms of infection and resolution. Chest. 2012;142:482–491.
   PubMed Web of Science ®Google Scholar
• Feldman C, Anderson R. Recent advances in our understanding of Streptococcus pneumoniae infection. F1000Prime Rep. 2014;6:1111–1162.
   Google Scholar
• Pichichero ME, Khan MN, Xu Q. Next generation protein based Streptococcus pneumoniae vaccines. Hum Vaccines Immunother. 2016;12:194–205.
   PubMed Web of Science ®Google Scholar
• Paixão L, Caldas J, Kloosterman TG, et al. Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism. Front Microbiol. 2015;6:1–19.
   PubMed Web of Science ®Google Scholar
• Philips BJ, Meguer JX, Redman J, et al. Factors determining the appearance of glucose in upper and lower respiratory tract secretions. Intensive Care Med. 2003;29:2204–2210.
   PubMed Web of Science ®Google Scholar
• Camara M, Boulnois GJ, Andrew PW, et al. A neuraminidase from Streptococcus pneumoniae has the features of a surface protein. Infect Immun. 1994;62:3688–3695.
   PubMed Web of Science ®Google Scholar
• Berry AM, Lock RA, Paton JC. Cloning and characterization of nanB, a second Streptococcus pneumoniae neuraminidase gene, and purification of the NanB enzyme from recombinant. . J Bacteriol. 1996;178:4854–4860.
   PubMed Web of Science ®Google Scholar
• Xu G, Kiefel MJ, Wilson JC, et al. Three Streptococcus pneumoniae sialidases: three different products. J Am Chem Soc. 2011;133:1718–1721.
   PubMed Web of Science ®Google Scholar
• Pettigrew MM, Fennie KP, York MP, et al. Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect Immun. 2006;74:3360–3365.
   PubMed Web of Science ®Google Scholar
• Imai S, Ito Y, Ishida T, et al. Distribution and clonal relationship of cell surface virulence genes among Streptococcus pneumoniae isolates in Japan. Clin Microbiol Infect. 2011;17:1409–1414.
   PubMed Web of Science ®Google Scholar
• Gut H, King SJ, Walsh MA. Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett. 2008;582:3348–3352.
   PubMed Web of Science ®Google Scholar
• Xu G, Potter JA, Russell RJM, et al. Crystal structure of the NanB sialidase from Streptococcus pneumoniae. J Mol Biol. 2008;384:436–449.
   PubMed Web of Science ®Google Scholar
• Hsiao Y-S, Parker D, Ratner AJ, et al. Crystal structures of respiratory pathogen neuraminidases. Biochem Biophys Res Commun. 2009;380:467–471.
   PubMed Web of Science ®Google Scholar
• Owen CD, Lukacik P, Potter JA, et al. Streptococcus pneumoniae NanC: structural insights into the specificity and mechanism of a sialidase that produces a sialidase inhibitor. J Biol Chem. 2015;290:27736–27748.
   PubMed Web of Science ®Google Scholar
• King SJ, Hippe KR, Weiser JN. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol. 2006;59:961–974.
   PubMed Web of Science ®Google Scholar
• Burnaugh AM, Frantz LJ, King SJ. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol. 2008;190:221–230.
   PubMed Web of Science ®Google Scholar
• Yesilkaya H, Manco S, Kadioglu A, et al. The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae. FEMS Microbiol Lett. 2008;278:231–235.
   PubMed Web of Science ®Google Scholar
• Song X-M, Connor W, Hokamp K, et al. Streptococcus pneumoniae early response genes to human lung epithelial cells. BMC Res Notes. 2008;1:64.
   Google Scholar
• Dalia AB, Standish AJ, Weiser JN. Three surface exoglycosidases from Streptococcus pneumoniae, NanA, BgaA, and StrH, promote resistance to opsonophagocytic killing by human neutrophils. Infect Immun. 2010;78:2108–2116.
   PubMed Web of Science ®Google Scholar
• Sundberg-Kövamees M, Holme T, Sjögren AM. Interaction of the C-polysaccharide of Streptococcus pneumoniae with the receptor asialo-GM1. Microb Pathog. 1996;21:223–234.
   PubMed Web of Science ®Google Scholar
• Tong HH, McIver MA, Fisher LM, et al. Effect of lacto-N-neotetraose, asialoganglioside-GM1 and neuraminidase on adherence of otitis media-associated serotypes of Streptococcus pneumoniae to chinchilla tracheal epithelium. Microb Pathog. 1999;26:111–119.
   PubMed Web of Science ®Google Scholar
• King SJ. Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol. 2010;25:15–24.
   PubMed Web of Science ®Google Scholar
• Parker D, Soong G, Planet P, et al. The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect Immun. 2009;77:3722–3730.
   PubMed Web of Science ®Google Scholar
• Trappetti C, Kadioglu A, Carter M, et al. Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J Infect Dis. 2009;199:1497–1505.
   PubMed Web of Science ®Google Scholar
• Brittan JL, Buckeridge TJ, Finn A, et al. Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae. Mol Oral Microbiol. 2012;27:270–283.
   PubMed Web of Science ®Google Scholar
• Orihuela CJ, Gao G, Francis KP, et al. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis. 2004;190:1661–1669.
   PubMed Web of Science ®Google Scholar
• Manco S, Hernon F, Yesilkaya H, et al. Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect Immun. 2006;74:4014–4020.
   PubMed Web of Science ®Google Scholar
• Tong HH, Blue LE, James MA, et al. Evaluation of the virulence of a Streptococcus pneumoniae neuraminidase- deficient mutant in nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect Immun. 2000;68:921–924.
   PubMed Web of Science ®Google Scholar
• Long JP, Tong HH, DeMaria TF. Immunization with native or recombinant Streptococcus pneumoniae neuraminidase affords protection in the chinchilla otitis media model. Infect Immun. 2004;72:4309–4313.
   PubMed Web of Science ®Google Scholar
• Tong HH, Li D, Chen S, et al. Immunization with recombinant Streptococcus pneumoniae neuraminidase NanA protects chinchillas against nasopharyngeal colonization. Infect Immun. 2005;73:7775–7778.
   PubMed Web of Science ®Google Scholar
• Uchiyama S, Carlin AF, Khosravi A, et al. The surface-anchored NanA protein promotes pneumococcal brain endothelial cell invasion. J Exp Med. 2009;206:1845–1852.
   PubMed Web of Science ®Google Scholar
• Berry AM, Paton JC. Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun. 2000;68:133–140.
   PubMed Web of Science ®Google Scholar
• Chang YC, Uchiyama S, Varki A, et al. Leukocyte inflammatory responses provoked by pneumococcal sialidase. mBio. 2012;3:1–10.
   Web of Science ®Google Scholar
• Blumental S, Granger-Farbos A, Moïsi JC, et al. Virulence factors of Streptococcus pneumoniae. Comparison between African and French invasive isolates and implication for future vaccines. PLoS One. 2015;10:e0133885.
   PubMed Web of Science ®Google Scholar
• Janapatla R-P, Hsu M-H, Y-C H, et al. Necrotizing pneumonia caused by nanC-carrying serotypes is associated with pneumococcal haemolytic uraemic syndrome in children. Clin Microbiol Infect. 2013;19:480–486.
   PubMed Web of Science ®Google Scholar
• Singh AK, Osman AS, Woodiga SA, et al. Defining the role of pneumococcal neuraminidases and O-glycosidase in pneumococcal haemolytic uraemic syndrome. J Med Microbiol. 2016;65:975–984.
   PubMed Web of Science ®Google Scholar
• Janapatla RP, Hsu M-H, Liao WT, et al. Low serum fetuin-a as a biomarker to predict pneumococcal necrotizing pneumonia and hemolytic uremic syndrome in children. Medicine. 2016;95:e3221.
   PubMed Web of Science ®Google Scholar
• Janapatla R-P, Chen C-L, Hsu M-H, et al. Immunization with pneumococcal neuraminidases NanA, NanB and NanC to generate neutralizing antibodies and to increase survival in mice. J Med Microbiol. 2018;1–15. [epub ahead of print].
   PubMed Web of Science ®Google Scholar
• Petersen TN, Brunak S, Von Heijne G, et al. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–786.
   PubMed Web of Science ®Google Scholar
• Hayre JK, Xu G, Borgianni L, et al. Optimization of a direct spectrophotometric method to investigate the kinetics and inhibition of sialidases. BMC Biochem. 2012;13:1–7.
   PubMed Web of Science ®Google Scholar
• Dobay O, Ungvári Á, Kardos S, et al. Genotypic and phenotypic characterisation of invasive Streptococcus pneumoniae isolates from Hungary, and coverage of the conjugate vaccines. J Clin Pathol. 2010;63:1116–1120.
   PubMed Web of Science ®Google Scholar
• King SJ, Hippe KR, Gould JM, et al. Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol Microbiol. 2004;54:159–171.
   PubMed Web of Science ®Google Scholar
• Song J-H, Ko KS, Lee J-Y, et al. Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Mol Cells. 2005;19:365–374.
   PubMed Web of Science ®Google Scholar
• Smith A, Johnston C, Inverarity D, et al. Investigating the role of pneumococcal neuraminidase A activity in isolates from pneumococcal haemolytic uraemic syndrome. J Med Microbiol. 2013;62:1735–1742.
   PubMed Web of Science ®Google Scholar
• Hollingshead SK, Becker R, Briles DE. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect Immun. 2000;68:5889–5900.
   PubMed Web of Science ®Google Scholar
• Jefferies JMC, Johnston CHG, Kirkham L-AS, et al. Presence of nonhemolytic pneumolysin in serotypes of Streptococcus pneumoniae associated with disease outbreaks. J Infect Dis. 2007;196:936–944.
   PubMed Web of Science ®Google Scholar
• Jefferies JMC, Tocheva AS, Rubery H, et al. Identification of novel pneumolysin alleles from paediatric carriage isolates of Streptococcus pneumoniae. J Med Microbiol. 2010;59:808–814.
   PubMed Web of Science ®Google Scholar
• Boder ET, Wittrup KD. Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol. 1997;15:328–330.
   PubMed Web of Science ®Google Scholar
• Blaise L, Wehnert A, Steukers MPG, et al. Construction and diversification of yeast cell surface displayed libraries by yeast mating: application to the affinity maturation of Fab antibody fragments. Gene. 2004;342:211–218.
   PubMed Web of Science ®Google Scholar
• Rakestraw JA, Aird D, Aha PM, et al. Secretion-and-capture cell-surface display for selection of target-binding proteins. Protein Eng Des Sel. 2011;24:525–530.
   PubMed Web of Science ®Google Scholar
• Xu Y, Roach W, Sun T, et al. Addressing polyspecificity of antibodies selected from an in vitro yeast presentation system: A FACS-based, high-throughput selection and analytical tool. Protein Eng Des Sel. 2013;26:663–670.
   PubMed Web of Science ®Google Scholar
• Brochet X, Lefranc MP, Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 2008;36:503–508.
   PubMed Web of Science ®Google Scholar
• Yang L, Connaris H, Potter JA, et al. Structural characterization of the carbohydrate-binding module of NanA sialidase, a pneumococcal virulence factor. BMC Struct Biol. 2015;15:1–10.
   PubMed Web of Science ®Google Scholar
• Yesilkaya H, Soma-Haddrick S, Crennell SJ, et al. Identification of amino acids essential for catalytic activity of pneumococcal neuraminidase A. Res Microbiol. 2006;157:569–574.
   PubMed Web of Science ®Google Scholar
• Kahya HF, Andrew PW, Yesilkaya H. Deacetylation of sialic acid by esterases potentiates pneumococcal neuraminidase activity for mucin utilization, colonization and virulence. PLoS Pathog. 2017;13:1–21.
   Web of Science ®Google Scholar
• Blanchette KA, Shenoy AT, Ii M, et al. Neuraminidase A-exposed galactose promotes Streptococcus pneumoniae biofilm formation during colonization. Infect Immun. 2016;84:2922–2932.
   PubMed Web of Science ®Google Scholar
• Wren JT, Blevins LK, Pang B, et al. Pneumococcal neuraminidase A (NanA) promotes biofilm formation and synergizes with influenza A virus in nasal colonization and middle ear infection. Infect Immun. 2017;85:1–10.
   Web of Science ®Google Scholar
• Paton JC, Berry AM, Lock RA. Molecular analysis of putative pneumococcal virulence proteins. Microb Drug Resist. 1997;3:1–10.
   PubMed Web of Science ®Google Scholar
• King QO, Lei B, Harmsen AG. Pneumococcal Surface Protein A contributes to secondary Streptococcus pneumoniae infection after influenza virus infection. J Infect Dis. 2009;200:537–545.
   PubMed Web of Science ®Google Scholar
• Marion C, Burnaugh AM, Woodiga SA, et al. Sialic acid transport contributes to pneumococcal colonization. Infect Immun. 2011;79:1262–1269.
   PubMed Web of Science ®Google Scholar
• Simell B, Jaakkola T, Lahdenkari M, et al. Serum antibodies to pneumococcal neuraminidase NanA in relation to pneumococcal carriage and acute otitis media. Clin Vaccine Immunol. 2006;13:1177–1179.
   PubMed Web of Science ®Google Scholar
• Xu Z, von Grafenstein S, Walther E, et al. Sequence diversity of NanA manifests in distinct enzyme kinetics and inhibitor susceptibility. Sci Rep. 2016;6:1–12.
   PubMed Web of Science ®Google Scholar
• Walther E, Richter M, Xu Z, et al. Antipneumococcal activity of neuraminidase inhibiting artocarpin. Int J Med Microbiol. 2015;305:289–297.
   PubMed Web of Science ®Google Scholar
• Park JY, Hwan Lim S, Ram Kim B, et al. Sialidase inhibitory activity of diarylnonanoid and neolignan compounds extracted from the seeds of Myristica fragrans. Bioorganic Med Chem Lett. 2017;27:3060–3064.
   PubMed Web of Science ®Google Scholar
• Chen J, Liu T, Gao J, et al. Variation in carbohydrates between cancer and normal cell membranes revealed by super-resolution fluorescence imaging. Adv Sci. 2016;3:1–9.
   Web of Science ®Google Scholar
• Kato K, Takegawa Y, Ralston KS, et al. Sialic acid-dependent attachment of mucins from three mouse strains to Entamoeba histolytica. Biochem Biophys Res Commun. 2013;436:252–258.
   PubMed Web of Science ®Google Scholar
• Ibricevic A, Pekosz A, Walter MJ, et al. Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol. 2006;80:7469–7480.
   PubMed Web of Science ®Google Scholar
• Shinya K, Ebina M, Yamada S, et al. Avian flu: influenza virus receptors in the human airway. Nature. 2006;440:435–436.
   PubMed Web of Science ®Google Scholar
• Hentrich K, Löfling J, Pathak A, et al. Streptococcus pneumoniae senses a human-like sialic acid profile via the response regulator CiaR. Cell Host Microbe. 2016;20:1–11.
   PubMed Web of Science ®Google Scholar