N-Glycan Profiles of Neuraminidase from Avian Influenza Viruses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of the AAMPs
2.2. Viral Whole Protein Preparation
2.3. NA Isolation
2.4. NA Identification by MALDI-TOF-MS
2.5. Glycopattern Analysis of NA Using Lectin Microarray
2.6. Characterization of N-Glycan Profiles of NAs by MALDI-TOF/TOF-MS
2.7. Docking Analysis for NA and p-Aminophenyloxamic Acid Interaction
3. Results
3.1. NA Isolation by the AAMPs
3.2. Glycopatterns Analysis of NAs by Lectin Microarray
3.3. N-Glycan Profiles of NAs by MALDI-TOF/TOF-MS Analysis
3.4. Docking Analysis of NA and p-Aminophenyloxamic Acid
4. Discussion and Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Chen, W.; Xu, Q.; Zhong, Y.; Yu, H.; Shu, J.; Ma, T.; Li, Z. Genetic variation and co-evolutionary relationship of RNA polymerase complex segments in influenza A viruses. Virology 2017, 511, 193–206. [Google Scholar] [CrossRef]
- Bai, L.; Zhao, Y.; Dong, J.; Liang, S.; Guo, M.; Liu, X.; Wang, X.; Huang, Z.; Sun, X.; Zhang, Z.; et al. Coinfection with influenza A virus enhances SARS-CoV-2 infectivity. Cell Res. 2021, 31, 395–403. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Sun, S.; Li, Z. Two glycosylation sites in H5N1 influenza virus hemagglutinin that affect binding preference by computer-based analysis. PLoS ONE 2012, 7, e38794. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Zhong, Y.; Qin, Y.; Sun, S.; Li, Z. The evolutionary pattern of glycosylation sites in influenza virus (H5N1) hemagglutinin and neu-raminidase. PLoS ONE 2012, 7, e49224. [Google Scholar]
- Shtyrya, Y.A.; Mochalova, L.V.; Bovin, N.V. Influenza virus neuraminidase: Structure and function. Acta Naturae 2009, 1, 26–32. [Google Scholar] [CrossRef]
- Mitrasinovic, P.M. On the structure-based design of novel inhibitors of H5N1 influenza A virus neuraminidase (NA). Biophys. Chem. 2009, 140, 35–38. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Cheng, L.P.; Pang, W.; Zhong, Z.J.; Guo, L.L. Design, Synthesis, and Biological Evaluation of Novel Acylhydrazone Derivatives as Potent Neuraminidase Inhibitors. ACS Med. Chem. Lett. 2020, 11, 1745–1750. [Google Scholar] [CrossRef]
- Vavricka, C.J.; Liu, Y.; Kiyota, H.; Sriwilaijaroen, N.; Qi, J.; Tanaka, K.; Wu, Y.; Li, Q.; Li, Y.; Yan, J.; et al. Influenza neuraminidase operates via a nucleophilic mechanism and can be targeted by covalent inhibitors. Nat. Commun. 2013, 4, 1491. [Google Scholar] [CrossRef] [PubMed]
- McKimm-Breschkin, J.L. Influenza neuraminidase inhibitors: Antiviral action and mechanisms of resistance. Influenza Other Respir. Viruses 2013, 7 (Suppl. S1), 25–36. [Google Scholar] [CrossRef]
- Schmidt, P.M.; Attwood, R.M.; Mohr, P.G.; Barrett, S.A.; McKimm-Breschkin, J.L. A generic system for the expression and purification of soluble and stable influenza neuraminidase. PLoS ONE 2011, 6, e16284. [Google Scholar] [CrossRef]
- Baz, M.; Paskel, M.; Matsuoka, Y.; Zengel, J.R.; Cheng, X.; Treanor, J.J.; Jin, H.; Subbarao, K. A Single Dose of an Avian H3N8 Influenza Virus Vaccine Is Highly Immunogenic and Efficacious against a Recently Emerged Seal Influenza Virus in Mice and Ferrets. J. Virol. 2015, 89, 6907–6917. [Google Scholar] [CrossRef]
- Vilei, E.M.; Johansson, A.; Schlatter, Y.; Redhead, K.; Frey, J. Genetic and functional characterization of the NanA sialidase from Clostridium chauvoei. Vet.-Res. 2011, 42, 2–9. [Google Scholar] [CrossRef]
- Yang, G.; Cui, T.; Chen, Q.; Ma, T.; Li, Z. Isolation and identification of native membrane glycoproteins from living cell by concanavalin A–magnetic particle conjugates. Anal. Biochem. 2012, 421, 339–341. [Google Scholar] [CrossRef] [PubMed]
- Qin, Y.; Zhong, Y.; Yang, G.; Ma, T.; Jia, L.; Huang, C.; Li, Z. Profiling of concanavalin A-binding glycoproteins in human hepatic stellate cells activated with transforming growth factor-beta1. Molecules 2014, 19, 19845–19867. [Google Scholar] [CrossRef]
- Zhong, Y.; Zhang, J.; Yu, H.; Zhang, J.; Sun, X.X.; Chen, W.; Bian, H.; Li, Z. Characterization and sub-cellular localization of GalNAc-binding proteins isolated from human hepatic stellate cells. Biochem. Biophys. Res. Commun. 2015, 468, 906–912. [Google Scholar] [CrossRef]
- Zhong, Y.; Sun, X.X.; Zhang, P.; Qin, X.; Chen, W.; Guo, Y.; Jia, Z.; Bian, H.; Li, Z. Identification and localization of xylose-binding proteins as potential biomarkers for liver fibro-sis/cirrhosis. Mol. Biosyst. 2016, 12, 598–605. [Google Scholar] [CrossRef]
- Qin, Y.; Zhong, Y.; Zhu, M.; Dang, L.; Yu, H.; Chen, Z.; Chen, W.; Wang, X.; Zhang, H.; Li, Z. Age- and sex-associated differences in the glycopatterns of human salivary glycoproteins and their roles against influenza A virus. J. Proteome Res. 2013, 12, 2742–2754. [Google Scholar] [CrossRef] [PubMed]
- Zhong, Y.; Qin, Y.; Yu, H.; Yu, J.; Wu, H.; Chen, L.; Zhang, P.; Wang, X.; Jia, Z.; Guo, Y.; et al. Avian influenza virus infection risk in humans with chronic diseases. Sci. Rep. 2015, 5, 8971. [Google Scholar] [CrossRef]
- Chen, W.; Zhong, Y.; Su, R.; Qi, H.; Deng, W.; Sun, Y.; Ma, T.; Wang, X.; Yu, H.; Wang, X.; et al. N-glycan profiles in H9N2 avian influenza viruses from chicken eggs and human embryonic lung fibroblast cells. J. Virol. Methods 2017, 249, 10–20. [Google Scholar] [CrossRef] [PubMed]
- Dang, J.; Shu, J.; Wang, R.; Yu, H.; Chen, Z.; Yan, W.; Zhao, B.; Ding, L.; Wang, Y.; Hu, H.; et al. The glycopatterns of Pseudomonas aeruginosa as a potential biomarker for its carbapenem resistance. Microbiol. Spectr. 2023, 11, e0200123. [Google Scholar] [CrossRef]
- Ren, X.; Shu, J.; Wang, J.; Guo, Y.; Zhang, Y.; Yue, L.; Yu, H.; Chen, W.; Zhang, C.; Ma, J.; et al. Machine learning reveals salivary glycopatterns as potential biomarkers for the diagnosis and prognosis of papillary thyroid cancer. Int. J. Biol. Macromol. 2022, 215, 280–289. [Google Scholar] [CrossRef]
- Wang, X.; Ma, T.; Yu, H.; Chen, Z.; Zhu, B.; Chen, W.; Sun, S.; Li, Z. Purification of sialoglycoproteins from bovine milk using serotonin-functionalized magnetic particles and their application against influenza A virus. Food Funct. 2020, 11, 6911–6920. [Google Scholar] [CrossRef]
- Shu, J.; Yu, H.; Du, H.; Zhang, J.; Zhang, K.; Li, X.; Xie, H.; Li, Z. Identification of N- and O-linked glycans recognized by AAL in saliva of patients with atrophic gastritis and gastric cancer. Cancer Biomark. 2018, 22, 669–681. [Google Scholar] [CrossRef]
- Shu, J.; Ren, X.; Cheng, H.; Wang, S.; Yue, L.; Li, X.; Yin, M.; Chen, X.; Zhang, T.; Hui, Z.; et al. Beneficial or detrimental: Recruiting more types of benign cases for cancer diagnosis based on salivary glycopatterns. Int. J. Biol. Macromol. 2023, 252, 126354. [Google Scholar] [CrossRef] [PubMed]
- Du, H.; Yu, H.; Ma, T.; Yang, F.; Jia, L.; Zhang, C.; Zhang, J.; Niu, L.; Yang, J.; Zhang, Z.; et al. Analysis of Glycosphingolipid Glycans by Lectin Microarrays. Anal. Chem. 2019, 91, 10663–10671. [Google Scholar] [CrossRef]
- Shu, J.; Ma, J.; Ren, X.; Wang, J.; Wang, Y.; Zhang, K.; Yu, H.; Guo, X.; Li, Z. The Abnormal Glycopatterns of Salivary Glycoproteins in Esophageal Squamous Cell Carcinoma Patients. Front. Chem. 2021, 9, 637730. [Google Scholar] [CrossRef]
- Russell, R.J.; Haire, L.F.; Stevens, D.J.; Collins, P.J.; Lin, Y.P.; Blackburn, G.M.; Hay, A.J.; Gamblin, S.J.; Skehel, J.J. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 2006, 443, 45–49. [Google Scholar] [CrossRef]
- Rizvi, S.M.; Shakil, S.; Haneef, M. A simple click by click protocol to perform docking: AutoDock 4.2 made easy for non-bioinformaticians. EXCLI J. 2013, 12, 831–857. [Google Scholar] [PubMed]
- Bohne, A.; Lang, E.; von der Lieth, C.W. SWEET—WWW-based rapid 3D construction of oligo- and polysaccharides. Bioinformatics 1999, 15, 767–768. [Google Scholar] [CrossRef]
- Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010, 31, 455–461. [Google Scholar] [CrossRef] [PubMed]
- Ilyushina, N.A.; Seiler, J.P.; Rehg, J.E.; Webster, R.G.; Govorkova, E.A. Effect of neuraminidase inhibitor-resistant mutations on pathogenicity of clade 2.2 A/Turkey/15/06 (H5N1) influenza virus in ferrets. PLoS Pathog. 2010, 6, e1000933. [Google Scholar] [CrossRef]
- Zhang, J.; Zhong, Y.; Zhang, P.; Du, H.; Shu, J.; Liu, X.; Zhang, H.; Guo, Y.; Jia, Z.; Niu, L.; et al. Identification of abnormal fucosylated-glycans recognized by LTL in saliva of HBV-induced chron-ic hepatitis, cirrhosis, and hepatocellular carcinoma. Glycobiology 2019, 29, 242–259. [Google Scholar] [CrossRef] [PubMed]
- She, Y.-M.; Farnsworth, A.; Li, X.; Cyr, T.D. Topological N-glycosylation and site-specific N-glycan sulfation of influenza proteins in the highly expressed H1N1 candidate vaccines. Sci. Rep. 2017, 7, 10232. [Google Scholar] [CrossRef] [PubMed]
- Cherry, J.L.; Lipman, D.J.; Nikolskaya, A.; Wolf, Y.I. Evolutionary dynamics of N-glycosylation sites of influenza virus hemagglutinin. PLoS Curr. 2009, 1, RRN1001. [Google Scholar] [CrossRef] [PubMed]
- Suga, A.; Nagae, M.; Yamaguchi, Y. Analysis of protein landscapes around N-glycosylation sites from the PDB repository for under-standing the structural basis of N-glycoprotein processing and maturation. Glycobiology 2018, 28, 774–785. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.; Wang, Z.; Zhang, L.; Li, D.; Lin, J. The Mechanism by which 146-N-Glycan Affects the Active Site of Neuraminidase. PLoS ONE 2015, 10, e0135487. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.; Lambert, J. Clade-specific genes and the evolutionary origin of novelty; new tools in the toolkit. Semin. Cell Dev. Biol. 2023, 145, 52–59. [Google Scholar] [CrossRef]
- Youk, S.; Lee, D.H.; Ferreira, H.L.; Afonso, C.L.; Absalon, A.E.; Swayne, D.E.; Suarez, D.L.; Pantin-Jackwood, M.J. Rapid evolution of Mexican H7N3 highly pathogenic avian influenza viruses in poultry. PLoS ONE 2019, 14, e0222457. [Google Scholar] [CrossRef]
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Chen, W.; Ma, T.; Liu, S.; Zhong, Y.; Yu, H.; Shu, J.; Wang, X.; Li, Z. N-Glycan Profiles of Neuraminidase from Avian Influenza Viruses. Viruses 2024, 16, 190. https://doi.org/10.3390/v16020190
Chen W, Ma T, Liu S, Zhong Y, Yu H, Shu J, Wang X, Li Z. N-Glycan Profiles of Neuraminidase from Avian Influenza Viruses. Viruses. 2024; 16(2):190. https://doi.org/10.3390/v16020190
Chicago/Turabian StyleChen, Wentian, Tianran Ma, Sinuo Liu, Yaogang Zhong, Hanjie Yu, Jian Shu, Xiurong Wang, and Zheng Li. 2024. "N-Glycan Profiles of Neuraminidase from Avian Influenza Viruses" Viruses 16, no. 2: 190. https://doi.org/10.3390/v16020190