Detection of influenza virus by agglutination using nanoparticles conjugated with a sialic acid-mimic peptide

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Abstract

Influenza virus (IFV) detection in the early phase of disease is critical for effective anti-influenza therapy using neuraminidase inhibitors. Sialyloligosaccharide receptors on the surface of respiratory cells are recognized by IFV hemagglutinin (HA) in the infection. Here, we show that agglutination of IFV is detected using poly(glycidyl methacrylate) (PGMA)-coated polystyrene nanoparticles conjugated with a sialic acid-mimic peptide. The azido peptide was immobilized onto the surface of the PGMA-coated nanoparticles by click chemistry. The distribution of particle size, determined by dynamic light scattering, indicated that the peptide-conjugated nanoparticles were agglutinated in the presence of HA and IFV. Nanoparticles conjugated with the receptor-mimic peptide may be a useful alternative to red blood cells in the global surveillance and clinical diagnosis of influenza.

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References

  1. 1.

    Paules C, Subbarao K. Influenza. Lancet. 2017;390:697–708.

  2. 2.

    Gamblin SJ, Skehel JJ. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem. 2010;285:28403–9.

  3. 3.

    Webster RG, Govorkova EA. Continuing challenges in influenza. Ann N Y Acad Sci. 2014;1323:115–39.

  4. 4.

    Salomon R, Webster RG. The influenza virus enigma. Cell. 2009;136:402–10.

  5. 5.

    Truelove S, Zhu H, Lessler J, Riley S, Read JM, Wang S, et al. A comparison of hemagglutination inhibition and neutralization assays for characterizing immunity to seasonal influenza A. Influenza Other Respir Virus. 2016;10:518–24.

  6. 6.

    Pedersen JC. Hemagglutination-inhibition assay for influenza virus subtype identification and the detection and quantitation of serum antibodies to influenza virus. Methods Mol Biol. 2014;1161:11–25.

  7. 7.

    Suzuki Y. Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull. 2005;28:399–408.

  8. 8.

    Nobusawa E, Ishihara H, Morishita T, Sato K, Nakajima K. Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Virology. 2000;278:587–96.

  9. 9.

    Matsubara T, Onishi A, Saito T, Shimada A, Inoue H, Taki T, et al. Sialic acid-mimic peptides as hemagglutinin inhibitors for anti-influenza therapy. J Med Chem. 2010;53:4441–9.

  10. 10.

    Hatano K, Matsubara T, Muramatsu Y, Ezure M, Koyama T, Matsuoka K, et al. Synthesis and influenza virus inhibitory activities of carbosilane dendrimers peripherally functionalized with hemagglutinin-binding Peptide. J Med Chem. 2014;57:8332–9.

  11. 11.

    Matsubara T, Ujie M, Yamamoto T, Akahori M, Einaga Y, Sato T. Highly sensitive detection of influenza virus by boron-doped diamond electrode terminated with sialic acid-mimic peptide. Proc Natl Acad Sci USA. 2016;113:8981–4.

  12. 12.

    Matsubara T, Onishi A, Saito T, Yamaguchi D, Sato T. Multivalent Effect in Influenza Hemagglutinin-Binding Activity of Sugar-Mimic Peptide. KOBUNSHI RONBUNSHU. 2016;73:62–8.

  13. 13.

    Chao HG, Bernatowicz MS, Matsueda GR. Preparation and use of the 4-[1-[N-(9-fluorenylmethyloxycarbonyl)amino]-2-(trimethylsilyl)ethyl]phenoxyacetic acid linkage agent for solid-phase synthesis of C-terminal peptide amides: improved yields of tryptophan-containing peptides. J Org Chem. 1993;58:2640–4.

  14. 14.

    Asahi Y, Yoshikawa T, Watanabe I, Iwasaki T, Hasegawa H, Sato Y, et al. Protection against influenza virus infection in polymeric Ig receptor knockout mice immunized intranasally with adjuvant-combined vaccines. J Immunol. 2002;168:2930–8.

  15. 15.

    Matsubara T, Sumi M, Kubota H, Taki T, Okahata Y, Sato T. Inhibition of influenza virus infections by sialylgalactose-binding peptides selected from a phage library. J Med Chem. 2009;52:4247–56.

  16. 16.

    Sakamoto S, Hatakeyama M, Ito T, Handa H. Tools and methodologies capable of isolating and identifying a target molecule for a bioactive compound. Bioorg Med Chem. 2012;20:1990–2001.

  17. 17.

    Matlin KS, Reggio H, Helenius A, Simons K. Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol. 1981;91(3 Pt 1):601–13.

  18. 18.

    Sakai-Tagawa Y, Ozawa M, Yamada S, Uchida Y, Saito T, Takahashi K, et al. Detection sensitivity of influenza rapid diagnostic tests. Microbiol Immunol. 2014;58:600–6.

  19. 19.

    Jannetto PJ, Buchan BW, Vaughan KA, Ledford JS, Anderson DK, Henley DC, et al. Real-time detection of influenza a, influenza B, and respiratory syncytial virus a and B in respiratory specimens by use of nanoparticle probes. J Clin Microbiol. 2010;48:3997–4002.

  20. 20.

    Wei J, Zheng L, Lv X, Bi Y, Chen W, Zhang W, et al. Analysis of influenza virus receptor specificity using glycan-functionalized gold nanoparticles. ACS Nano. 2014;8:4600–7.

  21. 21.

    Bray BL. Large-scale manufacture of peptide therapeutics by chemical synthesis. Nat Rev Drug Disco. 2003;2:587–93.

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Acknowledgements

This work was supported in part by AMED under Grant Number JP19hm0102056.

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Correspondence to Toshinori Sato.

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