Dual acting neuraminidase inhibitors open new opportunities to disrupt the lethal synergism between Streptococcus pneumoniae and influenza virus

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Walther, Elisabeth ^a   Xu, Zhongli ^a   Richter, Martina ^a   Kirchmair, Johannes ^b   Grienke, Ulrike ^c   Rollinger, Judith M ^c   Krumbholz, Andi ^d   Saluz, Hans P ^e   Pfister, Wolfgang ^a   Sauerbrei, Andreas ^a   Schmidtke, Michaela ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^e HANS KNÖLL INSTITUTE   (Germany)

Author keywords

Antibacterial; Antiviral; Co pathogenesis; Enzyme inhibition; Microbial communication; Pandemic influenza; Pneumococci; Secondary pneumococcal pneumonia

Indexed keywords

ARTOCARPIN; GALACTOSE; KATSUMADAIN A; N ACETYL 2,3 DEHYDRO 2 DEOXYNEURAMINIC ACID; OSELTAMIVIR; SIALIC ACID; SIALIDASE; SIALIDASE INHIBITOR; UNCLASSIFIED DRUG; ZANAMIVIR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ASSAY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLUENZA VIRUS; NONHUMAN; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; STREPTOCOCCUS PNEUMONIAE; VIRUS REPLICATION; VIRUS VIRULENCE;

EID: 84964330101     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00357     Document Type: Article

References (46)

1. Bauer, K., Durrwald, R., Schlegel, M., Pfarr, K., Topf, D., Wiesener, N., et al. (2012). Neuraminidase inhibitor susceptibility of swine influenza A viruses isolated in Germany between 1981 and 2008. Med. Microbiol. Immunol. 201, 61-72. doi: 10.1007/s00430-011-0206-1
2. Bauer, K., Schrader, C., Suess, J., Wutzler, P., and Schmidtke, M. (2007). Neuraminidase inhibitor susceptibility of porcine H3N2 influenza A viruses isolated in Germany between 1982 and 1999. Antiviral Res. 75, 219-226. doi: 10.1016/j.antiviral.2007.03.007
3. Berry, A. M., Lock, R. A., and Paton, J. C. (1996). Cloning and characterization of nanB, a second Streptococcus pneumoniae neuraminidase gene, and purification of the NanB enzyme from recombinant Escherichia coli. J. Bacteriol. 178, 4854-4860.
4. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., et al. (2014). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-W258. doi: 10.1093/nar/gku340
5. Burnaugh, A. M., Frantz, L. J., and King, S. J. (2008). Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J. Bacteriol. 190, 221-230. doi: 10.1128/JB.01251-07
6. Childs, R. A., Palma, A. S., Wharton, S., Matrosovich, T., Liu, Y., Chai, W., et al. (2009). Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray. Nat. Biotechnol. 27, 797-799. doi: 10.1038/nbt0909-797
7. Dobson, J., Whitley, R. J., Pocock, S., and Monto, A. S. (2015). Oseltamivir treatment for influenza in adults: a meta-analysis of randomised controlled trials. Lancet 385, 1729-1737. doi: 10.1016/S0140-6736(14)62449-1
8. DeLano, W. L. (2006). The PyMOL Molecular Graphics System, v0.99. Palo Alto, CA: DeLano Scientific LLC.
9. Grienke, U., Schmidtke, M., Kirchmair, J., Pfarr, K., Wutzler, P., Durrwald, R., et al. (2010). Antiviral potential and molecular insight into neuraminidase inhibiting diarylheptanoids from Alpinia katsumadai. J. Med. Chem. 53, 778-786. doi: 10.1021/jm901440f
10. Gut, H., King, S. J., and Walsh, M. A. (2008). Structural and functional studies of Streptococcus pneumoniae neuraminidase B: an intramolecular trans-sialidase. FEBS Lett. 582, 3348-3352. doi: 10.1016/j.febslet.2008.08.026
11. Gut, H., Xu, G., Taylor, G. L., and Walsh, M. A. (2011). Structural basis for Streptococcus pneumoniae NanA inhibition by influenza antivirals zanamivir and oseltamivir carboxylate. J. Mol. Biol. 409, 496-503. doi: 10.1016/j.jmb.2011.04.016
12. Hayre, J. K., Xu, G., Borgianni, L., Taylor, G. L., Andrew, P. W., Docquier, J. D., et al. (2012). Optimization of a direct spectrophotometric method to investigate the kinetics and inhibition of sialidases. BMC Biochem. 13:19. doi: 10.1186/1471-2091-13-19
13. King, S. J., Hippe, K. R., Gould, J. M., Bae, D., Peterson, S., Cline, R. T., et al. (2004). Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol. Microbiol. 54, 159-171. doi: 10.1111/j.1365-2958.2004.04252.x
14. King, S. J., Whatmore, A. M., and Dowson, C. G. (2005). NanA, a neuraminidase from Streptococcus pneumoniae, shows high levels of sequence diversity, at least in part through recombination with Streptococcus oralis. J. Bacteriol. 187, 5376-5386. doi: 10.1128/JB.187.15.5376-5386.2005
15. Kirchmair, J., Rollinger, J. M., Liedl, K. R., Seidel, N., Krumbholz, A., and Schmidtke, M. (2011). Novel neuraminidase inhibitors: identification, biological evaluation and investigations of the binding mode. Future Med. Chem. 3, 437-450. doi: 10.4155/fmc.10.292
16. Kumari, K., Gulati, S., Smith, D. F., Gulati, U., Cummings, R. D., and Air, G. M. (2007). Receptor binding specificity of recent human H3N2 influenza viruses. Virol. J. 4, 42. doi: 10.1186/1743-422X-4-42
17. Manco, S., Hernon, F., Yesilkaya, H., Paton, J. C., Andrew, P. W., and Kadioglu, A. (2006). Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect. Immun. 74, 4014-4020. doi: 10.1128/IAI.01237-05
18. McCullers, J. A. (2004). Effect of antiviral treatment on the outcome of secondary bacterial pneumonia after influenza. J. Infect. Dis. 190, 519-526. doi: 10.1086/421525
19. McCullers, J. A. (2014). The co-pathogenesis of influenza viruses with bacteria in the lung. Nat. Rev. Microbiol. 12, 252-262. doi: 10.1038/nrmicro3231
20. McCullers, J. A., and Bartmess, K. C. (2003). Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J. Infect. Dis. 187, 1000-1009. doi: 10.1086/368163
21. McCullers, J. A., and English, B. K. (2008). Improving therapeutic strategies for secondary bacterial pneumonia following influenza. Future Microbiol. 3, 397-404. doi: 10.2217/17460913.3.4.397
22. McCullers, J. A., and Rehg, J. E. (2002). Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J. Infect. Dis. 186, 341-350. doi: 10.1086/341462
23. Muthuri, S. G., Venkatesan, S., Myles, P. R., Leonardi-Bee, J., Al Khuwaitir, T. S., Al Mamun, A., et al. (2014). Effectiveness of neuraminidase inhibitors in reducing mortality in patients admitted to hospital with influenza A H1N1pdm09 virus infection: a meta-analysis of individual participant data. Lancet Respir. Med. 2, 395-404. doi: 10.1016/S2213-2600(14)70041-4
24. Nicholls, J. M., Bourne, A. J., Chen, H., Guan, Y., and Peiris, J. S. (2007). Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir. Res. 8:73. doi: 10.1186/1465-9921-8-73
25. Nicholls, J. M., Moss, R. B., and Haslam, S. M. (2013). The use of sialidase therapy for respiratory viral infections. Antiviral Res. 98, 401-409. doi: 10.1016/j.antiviral.2013.04.012
26. Nishikawa, T., Shimizu, K., Tanaka, T., Kuroda, K., Takayama, T., Yamamoto, T., et al. (2012). Bacterial neuraminidase rescues influenza virus replication from inhibition by a neuraminidase inhibitor. PLoS ONE 7:e45371. doi: 10.1371/journal.pone.0045371
27. Oggioni, M. R., Trappetti, C., Kadioglu, A., Cassone, M., Iannelli, F., Ricci, S., et al. (2006). Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol. Microbiol. 61, 1196-1210. doi: 10.1111/j.1365-2958.2006.05310.x
28. Orihuela, C. J., Gao, G., Francis, K. P., Yu, J., and Tuomanen, E. I. (2004). Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J. Infect. Dis. 190, 1661-1669. doi: 10.1086/424596
29. Owen, C. D., Lukacik, P., Potter, J. A., Sleator, O., Taylor, G. L., and Walsh, M. A. (2015). Streptococcus pneumoniae NanC: structural insights into the specificity and mechanism of a sialidase that produces a sialidase inhibitor. J. Biol. Chem. 290, 27736-27748. doi: 10.1074/jbc.M115.673632
30. Parker, D., Soong, G., Planet, P., Brower, J., Ratner, A. J., and Prince, A. (2009). The NanA neuraminidase of Streptococcus pneumoniae is involved in biofilm formation. Infect. Immun. 77, 3722-3730. doi: 10.1128/IAI.00228-09
31. Peltola, V. T., and McCullers, J. A. (2004). Respiratory viruses predisposing to bacterial infections: role of neuraminidase. Pediatr. Infect. Dis. J. 23, S87-S97. doi: 10.1097/01.inf.0000108197.81270.35
32. Pettigrew, M. M., Fennie, K. P., York, M. P., Daniels, J., and Ghaffar, F. (2006). Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect. Immun. 74, 3360-3365. doi: 10.1128/IAI.01442-05
33. Richter, M., Schumann, L., Walther, E., Hoffmann, A., Braun, H., Grienke, U., et al. (2015). Complementary assays helping to overcome challenges for identifying neuraminidase inhibitors. Future Virol. 10, 77-88. doi: 10.2217/fvl.14.97
34. Seidel, N., Sauerbrei, A., Wutzler, P., and Schmidtke, M. (2014). Hemagglutinin 222D/G polymorphism facilitates fast intra-host evolution of pandemic (H1N1) 2009 influenza A viruses. PLoS ONE 9:e104233. doi: 10.1371/journal.pone.0104233
35. Siegel, S. J., Roche, A. M., and Weiser, J. N. (2014). Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe 16, 55-67. doi: 10.1016/j.chom.2014.06.005
36. Smith, A. M., Adler, F. R., Ribeiro, R. M., Gutenkunst, R. N., Mcauley, J. L., Mccullers, J. A., et al. (2013). Kinetics of coinfection with influenza A virus and Streptococcus pneumoniae. PLoS Pathog. 9:e1003238. doi: 10.1371/journal.ppat.1003238
37. Song, X. M., Connor, W., Hokamp, K., Babiuk, L. A., and Potter, A. A. (2008). Streptococcus pneumoniae early response genes to human lung epithelial cells. BMC Res. Notes 1:64. doi: 10.1186/1756-0500-1-64
38. Stevens, J., Blixt, O., Glaser, L., Taubenberger, J. K., Palese, P., Paulson, J. C., et al. (2006). Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355, 1143-1155. doi: 10.1016/j.jmb.2005.11.002
39. Tanaka, A., Nakamura, S., Seki, M., Iwanaga, N., Kajihara, T., Kitano, M., et al. (2014). The effect of intravenous peramivir, compared with oral oseltamivir, on the outcome of post-influenza pneumococcal pneumonia in mice. Antivir. Ther. 20, 11-19. doi: 10.3851/IMP2744
40. Tong, H. H., Weiser, J. N., James, M. A., and Demaria, T. F. (2001). Effect of influenza A virus infection on nasopharyngeal colonization and otitis media induced by transparent or opaque phenotype variants of Streptococcus pneumoniae in the chinchilla model. Infect. Immun. 69, 602-606. doi: 10.1128/IAI.69.1.602-606.2001
41. Trappetti, C., Kadioglu, A., Carter, M., Hayre, J., Iannelli, F., Pozzi, G., et al. (2009). Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J. Infect. Dis. 199, 1497-1505. doi: 10.1086/598483
42. von Grafenstein, S., Wallnoefer, H. G., Kirchmair, J., Fuchs, J. E., Huber, R. G., Schmidtke, M., et al. (2015). Interface dynamics explain assembly dependency of influenza neuraminidase catalytic activity. J. Biomol. Struct. Dyn. 33, 104-120. doi: 10.1080/07391102.2013.855142
43. Walther, E., Richter, M., Xu, Z., Kramer, C., Von Grafenstein, S., Kirchmair, J., et al. (2015). Antipneumococcal activity of neuraminidase inhibiting artocarpin. Int. J. Med. Microbiol. 305, 289-297. doi: 10.1016/j.ijmm.2014.12.004
44. Webster, R. G., and Govorkova, E. A. (2014). Continuing challenges in influenza. Ann. N. Y. Acad. Sci. 1323, 115-139. doi: 10.1111/nyas.12462
45. Xu, G., Kiefel, M. J., Wilson, J. C., Andrew, P. W., Oggioni, M. R., and Taylor, G. L. (2011). Three Streptococcus pneumoniae sialidases: three different products. J. Am. Chem. Soc. 133, 1718-1721. doi: 10.1021/ja110733q
46. Xu, G., Potter, J. A., Russell, R. J., Oggioni, M. R., Andrew, P. W., and Taylor, G. L. (2008). Crystal structure of the NanB sialidase from Streptococcus pneumoniae. J. Mol. Biol. 384, 436-449. doi: 10.1016/j.jmb.2008.09.032