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Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site.

Proc Natl Acad Sci U S A 109 18903-8 (2012)
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Cited: 74 times
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Abstract

Recently, we reported a unique influenza A virus subtype H17N10 from little yellow-shouldered bats. Its neuraminidase (NA) gene encodes a protein that appears to be highly divergent from all known influenza NAs and was assigned as a new subtype N10. To provide structural and functional insights on the bat H17N10 virus, X-ray structures were determined for N10 NA proteins from influenza A viruses A/little yellow-shouldered bat/Guatemala/164/2009 (GU09-164) in two crystal forms at 1.95 Å and 2.5 Å resolution and A/little yellow-shouldered bat/Guatemala/060/2010 (GU10-060) at 2.0 Å. The overall N10 structures are similar to each other and to other known influenza NA structures, with a single highly conserved calcium binding site in each monomer. However, the region corresponding to the highly conserved active site of influenza A N1-N9 NA subtypes and influenza B NA differs substantially. In particular, most of the amino acid residues required for NA activity are substituted, and the putative active site is much wider because of displacement of the 150-loop and 430-loop. These structural features and the fact that the recombinant N10 protein exhibits no, or extremely low, NA activity suggest that it may have a different function than the NA proteins of other influenza viruses. Accordingly, we propose that the N10 protein be termed an NA-like protein until its function is elucidated.

Articles - 4gdj mentioned but not cited (1)

  1. Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Zhu X, Yang H, Guo Z, Yu W, Carney PJ, Li Y, Chen LM, Paulson JC, Donis RO, Tong S, Stevens J, Wilson IA. Proc. Natl. Acad. Sci. U.S.A. 109 18903-18908 (2012)


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  1. Bat-derived influenza-like viruses H17N10 and H18N11. Wu Y, Wu Y, Tefsen B, Shi Y, Gao GF. Trends Microbiol. 22 183-191 (2014)
  2. Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Chan JF, To KK, Tse H, Jin DY, Yuen KY. Trends Microbiol. 21 544-555 (2013)
  3. Emerging antiviral strategies to interfere with influenza virus entry. Vanderlinden E, Naesens L. Med Res Rev 34 301-339 (2014)
  4. Developing Universal Influenza Vaccines: Hitting the Nail, Not Just on the Head. Wiersma LC, Rimmelzwaan GF, de Vries RD. Vaccines (Basel) 3 239-262 (2015)
  5. Expected and Unexpected Features of the Newly Discovered Bat Influenza A-like Viruses. Ma W, García-Sastre A, Schwemmle M. PLoS Pathog. 11 e1004819 (2015)
  6. Exploration of sialic acid diversity and biology using sialoglycan microarrays. Deng L, Chen X, Varki A. Biopolymers 99 650-665 (2013)
  7. Unusual influenza A viruses in bats. Mehle A. Viruses 6 3438-3449 (2014)
  8. Laridae: A neglected reservoir that could play a major role in avian influenza virus epidemiological dynamics. Arnal A, Vittecoq M, Pearce-Duvet J, Gauthier-Clerc M, Boulinier T, Jourdain E. Crit. Rev. Microbiol. 41 508-519 (2015)
  9. Influenza A Virus Cell Entry, Replication, Virion Assembly and Movement. Dou D, Revol R, Östbye H, Wang H, Daniels R. Front Immunol 9 1581 (2018)
  10. Bat-Borne Influenza A Viruses: An Awakening. Ciminski K, Schwemmle M. Cold Spring Harb Perspect Med 11 a038612 (2021)
  11. Chiropteran influenza viruses: flu from bats or a relic from the past? Brunotte L, Beer M, Horie M, Schwemmle M. Curr Opin Virol 16 114-119 (2016)
  12. Bat Influenza Viruses: Current Status and Perspective. Yang W, Schountz T, Ma W. Viruses 13 547 (2021)
  13. Neutrophils and Influenza: A Thin Line between Helpful and Harmful. George ST, Lai J, Ma J, Stacey HD, Miller MS, Mullarkey CE. Vaccines (Basel) 9 597 (2021)
  14. Unraveling virus relationships by structure-based phylogenetic classification. Ng WM, Stelfox AJ, Bowden TA. Virus Evol 6 veaa003 (2020)
  15. Avian Influenza Virus Tropism in Humans. AbuBakar U, Amrani L, Kamarulzaman FA, Karsani SA, Hassandarvish P, Khairat JE. Viruses 15 833 (2023)
  16. Co-infection of the respiratory epithelium, scene of complex functional interactions between viral, bacterial, and human neuraminidases. Escuret V, Terrier O. Front Microbiol 14 1137336 (2023)
  17. Inferring the Urban Transmission Potential of Bat Influenza Viruses. Giotis ES. Front Cell Infect Microbiol 10 264 (2020)
  18. Live attenuated influenza A virus vaccines with modified NS1 proteins for veterinary use. Nogales A, DeDiego ML, Martínez-Sobrido L. Front Cell Infect Microbiol 12 954811 (2022)
  19. Roles of Glycans and Non-glycans on the Epithelium and in the Immune System in H1-H18 Influenza A Virus Infections. Sriwilaijaroen N, Suzuki Y. Methods Mol Biol 2556 205-242 (2022)

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  1. New world bats harbor diverse influenza A viruses. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO. PLoS Pathog. 9 e1003657 (2013)
  2. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Zhu X, Yu W, McBride R, Li Y, Chen LM, Donis RO, Tong S, Paulson JC, Wilson IA. Proc. Natl. Acad. Sci. U.S.A. 110 1458-1463 (2013)
  3. The K526R substitution in viral protein PB2 enhances the effects of E627K on influenza virus replication. Song W, Wang P, Mok BW, Lau SY, Huang X, Wu WL, Zheng M, Wen X, Yang S, Chen Y, Li L, Yuen KY, Chen H. Nat Commun 5 5509 (2014)
  4. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Sun X, Shi Y, Lu X, He J, Gao F, Yan J, Qi J, Gao GF. Cell Rep 3 769-778 (2013)
  5. An infectious bat-derived chimeric influenza virus harbouring the entry machinery of an influenza A virus. Juozapaitis M, Aguiar Moreira É, Mena I, Giese S, Riegger D, Pohlmann A, Höper D, Zimmer G, Beer M, García-Sastre A, Schwemmle M. Nat Commun 5 4448 (2014)
  6. Characterization of uncultivable bat influenza virus using a replicative synthetic virus. Zhou B, Ma J, Liu Q, Bawa B, Wang W, Shabman RS, Duff M, Lee J, Lang Y, Cao N, Nagy A, Lin X, Stockwell TB, Richt JA, Wentworth DE, Ma W. PLoS Pathog. 10 e1004420 (2014)
  7. Adaptation of avian influenza A (H6N1) virus from avian to human receptor-binding preference. Wang F, Qi J, Bi Y, Zhang W, Wang M, Zhang B, Wang M, Liu J, Yan J, Shi Y, Gao GF. EMBO J. 34 1661-1673 (2015)
  8. Avian influenza H9N2 seroprevalence among swine farm residents in China. Zhou P, Zhu W, Gu H, Fu X, Wang L, Zheng Y, He S, Ke C, Wang H, Yuan Z, Ning Z, Qi W, Li S, Zhang G. J. Med. Virol. 86 597-600 (2014)
  9. Molecular Characterizations of Surface Proteins Hemagglutinin and Neuraminidase from Recent H5Nx Avian Influenza Viruses. Yang H, Carney PJ, Mishin VP, Guo Z, Chang JC, Wentworth DE, Gubareva LV, Stevens J. J. Virol. 90 5770-5784 (2016)
  10. The N-terminal domain of PA from bat-derived influenza-like virus H17N10 has endonuclease activity. Tefsen B, Lu G, Zhu Y, Haywood J, Zhao L, Deng T, Qi J, Gao GF. J. Virol. 88 1935-1941 (2014)
  11. The effect of the MDCK cell selected neuraminidase D151G mutation on the drug susceptibility assessment of influenza A(H3N2) viruses. Mishin VP, Sleeman K, Levine M, Carney PJ, Stevens J, Gubareva LV. Antiviral Res. 101 93-96 (2014)
  12. Structural basis for a class of nanomolar influenza A neuraminidase inhibitors. Kerry PS, Mohan S, Russell RJ, Bance N, Niikura M, Pinto BM. Sci Rep 3 2871 (2013)
  13. Influenza A virus polymerase is a site for adaptive changes during experimental evolution in bat cells. Poole DS, Yú S, Caì Y, Dinis JM, Müller MA, Jordan I, Friedrich TC, Kuhn JH, Mehle A. J. Virol. 88 12572-12585 (2014)
  14. Kinetics of influenza A virus nucleoprotein antibody (IgM, IgA, and IgG) in serum and oral fluid specimens from pigs infected under experimental conditions. Panyasing Y, Goodell CK, Giménez-Lirola L, Kittawornrat A, Wang C, Schwartz KJ, Zimmerman JJ. Vaccine 31 6210-6215 (2013)
  15. The neuraminidase of bat influenza viruses is not a neuraminidase. García-Sastre A. Proc. Natl. Acad. Sci. U.S.A. 109 18635-18636 (2012)
  16. Functional and structural analysis of influenza virus neuraminidase N3 offers further insight into the mechanisms of oseltamivir resistance. Li Q, Qi J, Wu Y, Kiyota H, Tanaka K, Suhara Y, Ohrui H, Suzuki Y, Vavricka CJ, Gao GF. J. Virol. 87 10016-10024 (2013)
  17. Microsecond Molecular Dynamics Simulations of Influenza Neuraminidase Suggest a Mechanism for the Increased Virulence of Stalk-Deletion Mutants. Durrant JD, Bush RM, Amaro RE. J Phys Chem B 120 8590-8599 (2016)
  18. Synthetically derived bat influenza A-like viruses reveal a cell type- but not species-specific tropism. Moreira ÉA, Locher S, Kolesnikova L, Bolte H, Aydillo T, García-Sastre A, Schwemmle M, Zimmer G. Proc. Natl. Acad. Sci. U.S.A. 113 12797-12802 (2016)
  19. Characterization of the glycoproteins of bat-derived influenza viruses. Maruyama J, Nao N, Miyamoto H, Maeda K, Ogawa H, Yoshida R, Igarashi M, Takada A. Virology 488 43-50 (2016)
  20. Influenza viruses with receptor-binding N1 neuraminidases occur sporadically in several lineages and show no attenuation in cell culture or mice. Hooper KA, Crowe JE, Bloom JD. J. Virol. 89 3737-3745 (2015)
  21. Serendipitous discovery of a potent influenza virus a neuraminidase inhibitor. Mohan S, Kerry PS, Bance N, Niikura M, Pinto BM. Angew. Chem. Int. Ed. Engl. 53 1076-1080 (2014)
  22. Characterization of the anti-influenza activity of the Chinese herbal plant Paeonia lactiflora. Ho JY, Chang HW, Lin CF, Liu CJ, Hsieh CF, Horng JT. Viruses 6 1861-1875 (2014)
  23. Influenza A Virus Surveillance Based on Pre-Weaning Piglet Oral Fluid Samples. Panyasing Y, Goodell C, Kittawornrat A, Wang C, Levis I, Desfresne L, Rauh R, Gauger PC, Zhang J, Lin X, Azeem S, Ghorbani-Nezami S, Yoon KJ, Zimmerman J. Transbound Emerg Dis 63 e328-38 (2016)
  24. Novel Bat Influenza Virus NS1 Proteins Bind Double-Stranded RNA and Antagonize Host Innate Immunity. Turkington HL, Juozapaitis M, Kerry PS, Aydillo T, Ayllon J, García-Sastre A, Schwemmle M, Hale BG. J. Virol. 89 10696-10701 (2015)
  25. The Hemagglutinin of Bat-Associated Influenza Viruses Is Activated by TMPRSS2 for pH-Dependent Entry into Bat but Not Human Cells. Hoffmann M, Krüger N, Zmora P, Wrensch F, Herrler G, Pöhlmann S. PLoS ONE 11 e0152134 (2016)
  26. Evaluation of the antigenic relatedness and cross-protective immunity of the neuraminidase between human influenza A (H1N1) virus and highly pathogenic avian influenza A (H5N1) virus. Lu X, Liu F, Zeng H, Sheu T, Achenbach JE, Veguilla V, Gubareva LV, Garten R, Smith C, Yang H, Stevens J, Xu X, Katz JM, Tumpey TM. Virology 454-455 169-175 (2014)
  27. Survival analysis of infected mice reveals pathogenic variations in the genome of avian H1N1 viruses. Koçer ZA, Fan Y, Huether R, Obenauer J, Webby RJ, Zhang J, Webster RG, Wu G. Sci Rep 4 7455 (2014)
  28. The Genomic Contributions of Avian H1N1 Influenza A Viruses to the Evolution of Mammalian Strains. Koçer ZA, Carter R, Wu G, Zhang J, Webster RG. PLoS ONE 10 e0133795 (2015)
  29. Pathogenicity of modified bat influenza virus with different M genes and its reassortment potential with swine influenza A virus. Yang J, Lee J, Ma J, Lang Y, Nietfeld J, Li Y, Duff M, Li Y, Yang Y, Liu H, Zhou B, Wentworth DE, Richt JA, Li Z, Ma W. J. Gen. Virol. 98 577-584 (2017)
  30. Serological Evidence and Risk Factors for Swine Influenza Infections among Chinese Swine Workers in Guangdong Province. Ma M, Anderson BD, Wang T, Chen Y, Zhang D, Gray GC, Lu J. PLoS ONE 10 e0128479 (2015)
  31. Analysis of the phylogeny of Chinese H9N2 avian influenza viruses and their pathogenicity in mice. Lin Z, Xu C, Liu B, Ji Y, Fu Y, Guo J, Zhu Q. Arch. Virol. 159 2575-2586 (2014)
  32. Distribution of sialic acid receptors and experimental infections with different subtypes of influenza A viruses in Qinghai-Tibet plateau wild pika. Li Y, Xiao H, Huang C, Sun H, Li L, Su J, Ma J, Liu D, Wang H, Liu W, Gao GF, Li X, Yan J. Virol. J. 12 63 (2015)
  33. Genetic diversity and pathogenic potential of low pathogenic H7 avian influenza viruses isolated from wild migratory birds in Korea. Kim YI, Kim SW, Si YJ, Kwon HI, Park SJ, Kim EH, Kim SM, Lee IW, Song MS, Choi YK. Infect. Genet. Evol. 45 268-284 (2016)
  34. Limited adaptation of chimeric H9N2 viruses containing internal genes from bat influenza viruses in chickens. Ren C, Chen Y, Zhang M, Zhang T, Bao D, Lu C, Xue R, Zhang Y, Liu W, Chen H, Teng Q, Yang J, Li X, Li Z, Liu Q. Vet Microbiol 232 151-155 (2019)
  35. Mutations in the Neuraminidase-Like Protein of Bat Influenza H18N11 Virus Enhance Virus Replication in Mammalian Cells, Mice, and Ferrets. Zhong G, Fan S, Hatta M, Nakatsu S, Walters KB, Lopes TJS, Wang JI, Ozawa M, Karasin A, Li Y, Tong S, Donis RO, Neumann G, Kawaoka Y. J Virol 94 (2020)
  36. Specific Mutations in the PB2 Protein of Influenza A Virus Compensate for the Lack of Efficient Interferon Antagonism of the NS1 Protein of Bat Influenza A-Like Viruses. Aydillo T, Ayllon J, Pavlisin A, Martinez-Romero C, Tripathi S, Mena I, Moreira-Soto A, Vicente-Santos A, Corrales-Aguilar E, Schwemmle M, García-Sastre A. J. Virol. 92 (2018)
  37. Unexpected Functional Divergence of Bat Influenza Virus NS1 Proteins. Turkington HL, Juozapaitis M, Tsolakos N, Corrales-Aguilar E, Schwemmle M, Hale BG. J. Virol. 92 (2018)
  38. Unique Structural Features of Influenza Virus H15 Hemagglutinin. Tzarum N, McBride R, Nycholat CM, Peng W, Paulson JC, Wilson IA. J. Virol. 91 (2017)
  39. ClassyFlu: classification of influenza A viruses with Discriminatively trained profile-HMMs. Van der Auwera S, Bulla I, Ziller M, Pohlmann A, Harder T, Stanke M. PLoS ONE 9 e84558 (2014)
  40. Genetics and biological property analysis of Korea lineage of influenza A H9N2 viruses. Kang M, Jang HK. Vet. Microbiol. 204 96-103 (2017)
  41. Influenza A viruses balance ER stress with host protein synthesis shutoff. Mazel-Sanchez B, Iwaszkiewicz J, Bonifacio JPP, Silva F, Niu C, Strohmeier S, Eletto D, Krammer F, Tan G, Zoete V, Hale BG, Schmolke M. Proc Natl Acad Sci U S A 118 e2024681118 (2021)
  42. Novel insights into bat influenza A viruses. Ciminski K, Thamamongood T, Zimmer G, Schwemmle M. J. Gen. Virol. 98 2393-2400 (2017)
  43. Bats reveal the true power of influenza A virus adaptability. Ciminski K, Pfaff F, Beer M, Schwemmle M. PLoS Pathog. 16 e1008384 (2020)
  44. Carboxymethylated polyethylenimine modified magnetic nanoparticles specifically for purification of His-tagged protein. Chang M, Qin Q, Wang B, Xia T, Lv W, Sun X, Shi X, Xu G. J Sep Sci 42 744-753 (2019)
  45. Characterization of Experimental Oro-Nasal Inoculation of Seba's Short-Tailed Bats (Carollia perspicillata) with Bat Influenza A Virus H18N11. Gorka M, Schinköthe J, Ulrich R, Ciminski K, Schwemmle M, Beer M, Hoffmann D. Viruses 12 (2020)
  46. Evolutionarily conserved residues at an oligomerization interface of the influenza A virus neuraminidase are essential for viral survival. Mok CK, Chen GW, Shih KC, Gong YN, Lin SJ, Horng JT, Hsu JT, Chen CJ, Shih SR. Virology 447 32-44 (2013)
  47. Functional and structural analyses reveal that a dual domain sialidase protects bacteria from complement killing through desialylation of complement factors. Clark ND, Pham C, Kurniyati K, Sze CW, Coleman L, Fu Q, Zhang S, Malkowski MG, Li C. PLoS Pathog 19 e1011674 (2023)
  48. Impact of tetramerization on the ligand recognition of N1 influenza neuraminidase via MMGBSA approach. Bello M. Biopolymers 110 e23251 (2019)
  49. Influenza A (N1-N9) and Influenza B (B/Victoria and B/Yamagata) Neuraminidase Pseudotypes as Tools for Pandemic Preparedness and Improved Influenza Vaccine Design. da Costa KAS, Del Rosario JMM, Ferrari M, Vishwanath S, Asbach B, Kinsley R, Wagner R, Heeney JL, Carnell GW, Temperton NJ. Vaccines (Basel) 10 1520 (2022)
  50. New insights into the neuraminidase-mediated hemagglutination activity of influenza A(H3N2) viruses. Gao R, Pascua PNQ, Nguyen HT, Chesnokov A, Champion C, Mishin VP, Wentworth DE, Gubareva LV. Antiviral Res 218 105719 (2023)
  51. Plasticity of the 340-Loop in Influenza Neuraminidase Offers New Insight for Antiviral Drug Development. Han N, Ng JTY, Li Y, Mu Y, Huang Z. Int J Mol Sci 21 (2020)
  52. Structural Basis of Protection against H7N9 Influenza Virus by Human Anti-N9 Neuraminidase Antibodies. Zhu X, Turner HL, Lang S, McBride R, Bangaru S, Gilchuk IM, Yu W, Paulson JC, Crowe JE, Ward AB, Wilson IA. Cell Host Microbe 26 729-738.e4 (2019)
  53. Structural and inhibitor sensitivity analysis of influenza B-like viral neuraminidases derived from Asiatic toad and spiny eel. Li L, Chai Y, Peng W, Li D, Sun L, Gao GF, Qi J, Xiao H, Liu WJ, von Itzstein M, Gao F. Proc Natl Acad Sci U S A 119 e2210724119 (2022)
  54. Using common spatial distributions of atoms to relate functionally divergent influenza virus N10 and N11 protein structures to functionally characterized neuraminidase structures, toxin cell entry domains, and non-influenza virus cell entry domains. Weininger A, Weininger S. PLoS ONE 10 e0117499 (2015)