1887

Abstract

A recent study reported the detection of a bat-derived virus (BatPV/Epo_spe/AR1/DCR/2009, batMuV) with phylogenetic relatedness to human mumps virus (hMuV). Since all efforts to isolate infectious batMuV have reportedly failed, we generated recombinant mumps viruses (rMuVs) in which the open reading frames (ORFs) of the fusion (F) and haemagglutinin-neuraminidase (HN) glycoproteins of an hMuV strain were replaced by the corresponding ORFs of batMuV. The batMuV F and HN proteins were successfully incorporated into viral particles and the resultant chimeric virus was able to mediate infection of Vero cells. Distinct differences were observed between the fusogenicity of rMuVs expressing one or both batMuV glycoproteins: viruses expressing batMuV F were highly fusogenic, regardless of the origin of HN. In contrast, rMuVs expressing human F and bat-derived HN proteins were less fusogenic compared to hMuV. The growth kinetics of chimeric MuVs expressing batMuV HN in combination with either hMuV or batMuV F were similar to that of the backbone virus, whereas a delay in virus replication was obtained for rMuVs harbouring batMuV F and hMuV HN. Replacement of the hMuV F and HN genes or the HN gene alone by the corresponding batMuV genes led to a slight reduction in neurovirulence of the highly neurovirulent backbone strain. Neutralizing antibodies inhibited infection mediated by all recombinant viruses generated. Furthermore, group IV anti-MuV antibodies inhibited the neuraminidase activity of bat-derived HN. Our study reports the successful generation of chimeric MuVs expressing the F and HN proteins of batMuV, providing a means for further examination of this novel batMuV.

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2016-11-10
2022-01-19
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References

  1. Aguilar H. C., Matreyek K. A., Filone C. M., Hashimi S. T., Levroney E. L., Negrete O. A., Bertolotti-Ciarlet A., Choi D. Y., McHardy I. et al. 2006; N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J Virol 80:4878–4889 [View Article][PubMed]
    [Google Scholar]
  2. Amexis G., Rubin S., Chatterjee N., Carbone K., Chumakov K. 2003; Identification of a new genotype H wild-type mumps virus strain and its molecular relatedness to other virulent and attenuated strains. J Med Virol 70:284–286 [View Article][PubMed]
    [Google Scholar]
  3. Bagai S., Lamb R. A. 1995; Individual roles of N-linked oligosaccharide chains in intracellular transport of the paramyxovirus SV5 fusion protein. Virology 209:250–256 [View Article][PubMed]
    [Google Scholar]
  4. Beard C. M., Benson R. C., Kelalis P. P., Elveback L. R., Kurland L. T. 1977; The incidence and outcome of mumps orchitis in Rochester, Minnesota, 1935 to 1974. Mayo Clin Proc 52:3–7[PubMed]
    [Google Scholar]
  5. Brostrom M. A., Bruening G., Bankowski R. A. 1971; Comparison of neuraminidases of paramyxoviruses with immunologically dissimilar hemagglutinins. Virology 46:856–865 [View Article][PubMed]
    [Google Scholar]
  6. Buchholz U. J., Finke S., Conzelmann K. K. 1999; Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251–259[PubMed]
    [Google Scholar]
  7. Calain P., Roux L. 1993; The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol 67:4822–4830[PubMed]
    [Google Scholar]
  8. Cdc 2015; Mumps. In Epidemiology and Prevention of Vaccine-Preventable Diseases: The Pink Book: Course Textbook. 13 Edited by Hamborsky J., Kroger A., Wolfe C. Washington, DC: Public Health Foundation;
    [Google Scholar]
  9. Chang A., Dutch R. E. 2012; Paramyxovirus fusion and entry: multiple paths to a common end. Viruses 4:613–636 [View Article][PubMed]
    [Google Scholar]
  10. Cox R., Green T. J., Purushotham S., Deivanayagam C., Bedwell G. J., Prevelige P. E., Luo M. 2013; Structural and functional characterization of the mumps virus phosphoprotein. J Virol 87:7558–7568 [View Article][PubMed]
    [Google Scholar]
  11. Drexler J. F., Corman V. M., Müller M. A., Maganga G. D., Vallo P., Binger T., Gloza-Rausch F., Cottontail V. M., Rasche A. et al. 2012; Bats host major mammalian paramyxoviruses. Nat Commun 3:796 [View Article][PubMed]
    [Google Scholar]
  12. Elango N., Varsanyi T. M., Kövamees J., Norrby E. 1988; Molecular cloning and characterization of six genes, determination of gene order and intergenic sequences and leader sequence of mumps virus. J Gen Virol 69:2893–2900 [View Article][PubMed]
    [Google Scholar]
  13. Gale M. Jr., Tan S. L., Katze M. G. 2000; Translational control of viral gene expression in eukaryotes. Microbiol Mol Biol Rev 64:239–280 [View Article][PubMed]
    [Google Scholar]
  14. Hausmann S., Jacques J. P., Kolakofsky D. 1996; Paramyxovirus RNA editing and the requirement for hexamer genome length. RNA 2:1033–1045[PubMed]
    [Google Scholar]
  15. Hoffmann M., Wu Y. J., Gerber M., Berger-Rentsch M., Heimrich B., Schwemmle M., Zimmer G. 2010; Fusion-active glycoprotein G mediates the cytotoxicity of vesicular stomatitis virus M mutants lacking host shut-off activity. J Gen Virol 91:2782–2793 [View Article][PubMed]
    [Google Scholar]
  16. Hosaka Y., Kuroda K., Ikeura A., Iwamoto T., Suzuki Y. 1998; Binding of influenza and paramyxoviruses to group B streptococcus with the terminal sialyl-galactose linkage. J Electron Microsc 47:169–174 [View Article]
    [Google Scholar]
  17. Katoh H., Kubota T., Ihara T., Maeda K., Takeda M., Kidokoro M. 2016; Cross-neutralization between human and African bat mumps viruses. Emerg Infect Dis 22:703–706 [View Article][PubMed]
    [Google Scholar]
  18. Kolakofsky D., Roux L., Garcin D., Ruigrok R. W. 2005; Paramyxovirus mRNA editing, the ‘rule of six’ and error catastrophe: a hypothesis. J Gen Virol 86:1869–1877 [View Article][PubMed]
    [Google Scholar]
  19. Kövamees J., Rydbeck R., Orvell C., Norrby E. 1990; Hemagglutinin-neuraminidase (HN) amino acid alterations in neutralization escape mutants of Kilham mumps virus. Virus Res 17:119–129 [View Article][PubMed]
    [Google Scholar]
  20. Krüger N., Hoffmann M., Drexler J. F., Müller M. A., Corman V. M., Sauder C., Rubin S., He B., Örvell C. et al. 2015; Functional properties and genetic relatedness of the fusion and hemagglutinin-neuraminidase proteins of a mumps virus-like bat virus. J Virol 89:4539–4548 [View Article][PubMed]
    [Google Scholar]
  21. Leprat R., Aymard M. 1979; Selective inactivation of hemagglutinin and neuraminidase on mumps virus. Arch Virol 61:273–281 [View Article][PubMed]
    [Google Scholar]
  22. Malik T., Sauder C., Wolbert C., Zhang C., Carbone K. M., Rubin S. 2007a; A single nucleotide change in the mumps virus F gene affects virus fusogenicity in vitro and virulence in vivo . J Neurovirol 13:513–521 [View Article]
    [Google Scholar]
  23. Malik T., Wolbert C., Mauldin J., Sauder C., Carbone K. M., Rubin S. A. 2007b; Functional consequences of attenuating mutations in the haemagglutinin neuraminidase, fusion and polymerase proteins of a wild-type mumps virus strain. J Gen Virol 88:2533–2541 [View Article]
    [Google Scholar]
  24. McCarthy M., Johnson R. T. 1980; A comparison of the structural polypeptides of five strains of mumps virus. J Gen Virol 46:15–27 [View Article][PubMed]
    [Google Scholar]
  25. McGinnes L., Sergel T., Reitter J., Morrison T. 2001; Carbohydrate modifications of the NDV fusion protein heptad repeat domains influence maturation and fusion activity. Virology 283:332–342 [View Article][PubMed]
    [Google Scholar]
  26. Merz D. C., Wolinsky J. S. 1981; Biochemical features of mumps virus neuraminidases and their relationship with pathogenicity. Virology 114:218–227 [View Article][PubMed]
    [Google Scholar]
  27. Merz D. C., Server A. C., Waxham M. N., Wolinsky J. S. 1983; Biosynthesis of mumps virus F glycoprotein: non-fusing strains efficiently cleave the F glycoprotein precursor. J Gen Virol 64:1457–1467 [View Article][PubMed]
    [Google Scholar]
  28. Orvell C. 1984; The reactions of monoclonal antibodies with structural proteins of mumps virus. J Immunol 132:2622–2629[PubMed]
    [Google Scholar]
  29. Orvell C., Alsheikhly A. R., Kalantari M., Johansson B. 1997; Characterization of genotype-specific epitopes of the HN protein of mumps virus. J Gen Virol 78:3187–3193 [View Article][PubMed]
    [Google Scholar]
  30. Orvell C., Tecle T., Johansson B., Saito H., Samuelson A. 2002; Antigenic relationships between six genotypes of the small hydrophobic protein gene of mumps virus. J Gen Virol 83:2489–2496 [View Article][PubMed]
    [Google Scholar]
  31. Paterson R. G., Lamb R. A. 1990; RNA editing by G-nucleotide insertion in mumps virus P-gene mRNA transcripts. J Virol 64:4137–4145[PubMed]
    [Google Scholar]
  32. Rubin S., Beeler J. 2013; Mumps vaccines: do we need a new one?. Pediatr Infect Dis J 32:1156–1157 [View Article][PubMed]
    [Google Scholar]
  33. Rubin S. A., Pletnikov M., Taffs R., Snoy P. J., Kobasa D., Brown E. G., Wright K. E., Carbone K. M. 2000; Evaluation of a neonatal rat model for prediction of mumps virus neurovirulence in humans. J Virol 74:5382–5384 [View Article][PubMed]
    [Google Scholar]
  34. Russell R. R., Donald J. C. 1958; The neurological complications of mumps. Br Med J 2:27–30 [View Article][PubMed]
    [Google Scholar]
  35. Samal S. K. 2011 The Biology of Paramyxoviruses Norfolk, UK: Caister Academic Press;
    [Google Scholar]
  36. Santos-López G., Scior T., Borraz-Argüello M. T., Vallejo-Ruiz V., Herrera-Camacho I., Tapia-Ramírez J., Reyes-Leyva J. 2009; Structure-function analysis of two variants of mumps virus hemagglutinin-neuraminidase protein. Braz J Infect Dis 13:24–34 [View Article]
    [Google Scholar]
  37. Sauder C. J., Zhang C. X., Ngo L., Werner K., Lemon K., Duprex W. P., Malik T., Carbone K., Rubin S. A. 2011; Gene-specific contributions to mumps virus neurovirulence and neuroattenuation. J Virol 85:7059–7069 [View Article][PubMed]
    [Google Scholar]
  38. Sauder C. J., Ngo L., Simonyan V., Cong Y., Zhang C., Link M., Malik T., Rubin S. A. 2015; Generation and propagation of recombinant mumps viruses exhibiting an additional U residue in the homopolymeric U tract of the F gene-end signal. Virus Genes 51:12–24 [View Article][PubMed]
    [Google Scholar]
  39. Server A. C., Merz D. C., Waxham M. N., Wolinsky J. S. 1982; Differentiation of mumps virus strains with monoclonal antibody to the HN glycoprotein. Infect Immun 35:179–186[PubMed]
    [Google Scholar]
  40. Sidhu M. S., Menonna J. P., Cook S. D., Dowling P. C., Udem S. A. 1993; Canine distemper virus L gene: sequence and comparison with related viruses. Virology 193:50–65 [View Article][PubMed]
    [Google Scholar]
  41. Takeuchi K., Tanabayashi K., Hishiyama M., Yamada A. 1996; The mumps virus SH protein is a membrane protein and not essential for virus growth. Virology 225:156–162 [View Article][PubMed]
    [Google Scholar]
  42. Tanabayashi K., Takeuchi K., Okazaki K., Hishiyama M., Yamada A. 1993; Identification of an amino acid that defines the fusogenicity of mumps virus. J Virol 67:2928–2931[PubMed]
    [Google Scholar]
  43. von Messling V., Cattaneo R. 2003; N-linked glycans with similar location in the fusion protein head modulate paramyxovirus fusion. J Virol 77:10202–10212 [View Article][PubMed]
    [Google Scholar]
  44. Wolinsky J. S., Stroop W. G. 1978; Virulence and persistence of three prototype strains of mumps virus in newborn hamsters. Arch Virol 57:355–359 [View Article][PubMed]
    [Google Scholar]
  45. Yoshida N., Nakayama T. 2010; Leucine at position 383 of fusion protein is responsible for fusogenicity of wild-type mumps virus in B95a cells. Intervirology 53:193–202 [View Article][PubMed]
    [Google Scholar]
  46. Zimmer G., Trotz I., Herrler G. 2001; N-glycans of F protein differentially affect fusion activity of human respiratory syncytial virus. J Virol 75:4744–4751 [View Article][PubMed]
    [Google Scholar]
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