1887

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Volume 97, Issue 7

Species-specific and individual differences in Nipah virus replication in porcine and human airway epithelial cells Free

Abstract

Highly pathogenic (NiV) causes symptomatic infections in pigs and humans. The severity of respiratory symptoms is much more pronounced in pigs than in humans, suggesting species-specific differences of NiV replication in porcine and human airways. Here, we present a comparative study on productive NiV replication in primary airway epithelial cell cultures of the two species. We reveal that NiV growth substantially differs in primary cells between pigs and humans, with a more rapid spread of infection in human airway epithelia. Increased replication, correlated with higher endogenous expression levels of the main NiV entry receptor ephrin-B2, not only significantly differed between airway cells of the two species but also varied between cells from different human donors. To our knowledge, our study provides the first experimental evidence of species-specific and individual differences in NiV receptor expression and replication kinetics in primary airway epithelial cells. It remains to be determined whether and how these differences contribute to the viral host range and pathogenicity.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Airway epithelial cells , Ephrin-B2 and Nipah virus
© 2016 The Authors
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2016-07-01
2024-04-24
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References

  1. AbuBakar S., Chang L. Y., Ali A. R., Sharifah S. H., Yusoff K., Zamrod Z. 2004; Isolation and molecular identification of Nipah virus from pigs. Emerg Infect Dis 10:2228–2230 [View Article][PubMed]
     [Google Scholar]
  2. Baseler L., de Wit E., Scott D. P., Munster V. J., Feldmann H. 2015; Syrian hamsters (Mesocricetus auratus) oronasally inoculated with a Nipah virus isolate from Bangladesh or Malaysia develop similar respiratory tract lesions. Vet Pathol 52:38–45 [View Article][PubMed]
     [Google Scholar]
  3. Bellini W. J., Harcourt B. H., Bowden N., Rota P. A. 2005; Nipah virus: an emergent paramyxovirus causing severe encephalitis in humans. J Neurovirol 11:481–487 [View Article][PubMed]
     [Google Scholar]
  4. Bonaparte M. I., Dimitrov A. S., Bossart K. N., Crameri G., Mungall B. A., Bishop K. A., Choudhry V., Dimitrov D. S., Wang L. F. et al. 2005; Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci U S A 102:10652–10657 [View Article][PubMed]
     [Google Scholar]
  5. Bossart K. N., Tachedjian M., McEachern J. A., Crameri G., Zhu Z., Dimitrov D. S., Broder C. C., Wang L. F. 2008; Functional studies of host-specific ephrin-B ligands as Henipavirus receptors. Virology 372:357–371 [View Article][PubMed]
     [Google Scholar]
  6. Chua K. B., Goh K. J., Wong K. T., Kamarulzaman A., Tan P. S., Ksiazek T. G., Zaki S. R., Paul G., Lam S. K. et al. 1999; Fatal encephalitis due to Nipah virus among pig-farmers in Malaysia. Lancet 354:1257–1259 [View Article][PubMed]
     [Google Scholar]
  7. Chua K. B., Bellini W. J., Rota P. A., Harcourt B. H., Tamin A., Lam S. K., Ksiazek T. G., Rollin P. E., Zaki S. R. et al. 2000; Nipah virus: a recently emergent deadly paramyxovirus. Science 288:1432–1435 [View Article][PubMed]
     [Google Scholar]
  8. Chua K. B., Lam S. K., Goh K. J., Hooi P. S., Ksiazek T. G., Kamarulzaman A., Olson J., Tan C. T. 2001; The presence of Nipah virus in respiratory secretions and urine of patients during an outbreak of Nipah virus encephalitis in Malaysia. J Infect 42:40–43 [View Article][PubMed]
     [Google Scholar]
  9. Clayton B. A., Wang L. F., Marsh G. A. 2013; Henipaviruses: an updated review focusing on the pteropid reservoir and features of transmission. Zoonoses Public Health 60:69–83 [View Article][PubMed]
     [Google Scholar]
  10. de Swart R. L., Ludlow M., de Witte L., Yanagi Y., van Amerongen G., McQuaid S., Yüksel S., Geijtenbeek T. B., Duprex W. P. et al. 2007; Predominant infection of CD150+ lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog 3:e178 [View Article][PubMed]
     [Google Scholar]
  11. DeBuysscher B. L., de Wit E., Munster V. J., Scott D., Feldmann H., Prescott J. 2013; Comparison of the pathogenicity of Nipah virus isolates from Bangladesh and Malaysia in the Syrian hamster. PLoS Negl Trop Dis 7:e2024 [View Article][PubMed]
     [Google Scholar]
  12. Diederich S., Thiel L., Maisner A. 2008; Role of endocytosis and cathepsin-mediated activation in Nipah virus entry. Virology 375:391–400 [CrossRef]
     [Google Scholar]
  13. Diederich S., Sauerhering L., Weis M., Altmeppen H., Schaschke N., Reinheckel T., Erbar S., Maisner A. 2012; Activation of the Nipah virus fusion protein in MDCK cells is mediated by cathepsin B within the endosome-recycling compartment. J Virol 86:3736–3745 [View Article][PubMed]
     [Google Scholar]
  14. Dietzel E., Kolesnikova L., Sawatsky B., Heiner A., Weis M., Kobinger G. P., Becker S., von Messling V., Maisner A. 2015; Nipah virus matrix protein influences fusogenicity and is essential for particle infectivity and stability. J Virol 90:2514–2522 [View Article][PubMed]
     [Google Scholar]
  15. Erbar S., Diederich S., Maisner A. 2008; Selective receptor expression restricts Nipah virus infection of endothelial cells. Virol J 5:142 [View Article][PubMed]
     [Google Scholar]
  16. Escaffre O., Borisevich V., Carmical J. R., Prusak D., Prescott J., Feldmann H., Rockx B. 2013; Henipavirus pathogenesis in human respiratory epithelial cells. J Virol 87:3284–3294 [View Article][PubMed]
     [Google Scholar]
  17. Escaffre O., Borisevich V., Vergara L. A., Wen J. W., Long D., Rockx B. 2016; Characterization of Nipah virus infection in a model of human airway epithelial cells cultured at an air-liquid interface. J Gen Virol 97:1077–1086 [View Article][PubMed]
     [Google Scholar]
  18. Freitag T. C., Maisner A. 2015; Early activation of primary brain microvascular endothelial cells by Nipah virus glycoprotein-containing particles. J Virol 90:2706–2709 [View Article][PubMed]
     [Google Scholar]
  19. Goris K., Uhlenbruck S., Schwegmann-Wessels C., Köhl W., Niedorf F., Stern M., Hewicker-Trautwein M., Bals R., Taylor G. et al. 2009; Differential sensitivity of differentiated epithelial cells to respiratory viruses reveals different viral strategies of host infection. J Virol 83:1962–1968 [View Article][PubMed]
     [Google Scholar]
  20. Hafner C., Schmitz G., Meyer S., Bataille F., Hau P., Langmann T., Dietmaier W., Landthaler M., Vogt T. 2004; Differential gene expression of Eph receptors and ephrins in benign human tissues and cancers. Clin Chem 50:490–499 [View Article][PubMed]
     [Google Scholar]
  21. Hooper P., Zaki S., Daniels P., Middleton D. 2001; Comparative pathology of the diseases caused by Hendra and Nipah viruses. Microbes Infect 3:315–322 [View Article][PubMed]
     [Google Scholar]
  22. Hossain M. J., Gurley E. S., Montgomery J. M., Bell M., Carroll D. S., Hsu V. P., Formenty P., Croisier A., Bertherat E. et al. 2008; Clinical presentation of nipah virus infection in Bangladesh. Clin Infect Dis 46:977–984 [View Article][PubMed]
     [Google Scholar]
  23. Kullander K., Klein R. 2002; Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3:475–486 [View Article][PubMed]
     [Google Scholar]
  24. Lamp B., Dietzel E., Kolesnikova L., Sauerhering L., Erbar S., Weingartl H., Maisner A. 2013; Nipah virus entry and egress from polarized epithelial cells. J Virol 87:3143–3154 [View Article][PubMed]
     [Google Scholar]
  25. Lemon K., de Vries R. D., Mesman A. W., McQuaid S., van Amerongen G., Yüksel S., Ludlow M., Rennick L. J., Kuiken T. et al. 2011; Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog 7:e1001263 [View Article][PubMed]
     [Google Scholar]
  26. Lo M. K., Rota P. A. 2008; The emergence of Nipah virus, a highly pathogenic paramyxovirus. J Clin Virol 43:396–400 [View Article][PubMed]
     [Google Scholar]
  27. Luby S. P., Gurley E. S., Hossain M. J. 2009; Transmission of human infection with Nipah virus. Clin Infect Dis 49:1743–1748 [View Article][PubMed]
     [Google Scholar]
  28. Maisner A., Neufeld J., Weingartl H. 2009; Organ- and endotheliotropism of Nipah virus infections in vivo and in vitro. Thromb Haemost 102:1014–1023 [View Article][PubMed]
     [Google Scholar]
  29. Middleton D. J., Westbury H. A., Morrissy C. J., van der Heide B. M., Russell G. M., Braun M. A., Hyatt A. D. 2002; Experimental Nipah virus infection in pigs and cats. J Comp Pathol 126:124–136 [View Article][PubMed]
     [Google Scholar]
  30. Mohd Nor M. N., Gan C. H., Ong B. L. 2000; Nipah virus infection of pigs in peninsular Malaysia. Rev Sci Tech 19:160–165[PubMed]
     [Google Scholar]
  31. Moll M., Diederich S., Klenk H. D., Czub M., Maisner A. 2004; Ubiquitous activation of the Nipah virus fusion protein does not require a basic amino acid at the cleavage site. J Virol 78:9705–9712 [View Article][PubMed]
     [Google Scholar]
  32. Negrete O. A., Levroney E. L., Aguilar H. C., Bertolotti-Ciarlet A., Nazarian R., Tajyar S., Lee B. 2005; EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nat New Biol 436:401–405
     [Google Scholar]
  33. Negrete O. A., Wolf M. C., Aguilar H. C., Enterlein S., Wang W., Mühlberger E., Su S. V., Bertolotti-Ciarlet A., Flick R. et al. 2006; Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog 2:e7 [View Article][PubMed]
     [Google Scholar]
  34. Niwa H., Yamamura K., Miyazaki J. 1991; Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–199[PubMed] [CrossRef]
     [Google Scholar]
  35. Pager C. T., Craft W. W., Patch J., Dutch R. E., Craft W. W. Jr 2006; A mature and fusogenic form of the Nipah virus fusion protein requires proteolytic processing by cathepsin L. Virology 346:251–257 [CrossRef]
     [Google Scholar]
  36. Rockx B., Bossart K. N., Feldmann F., Geisbert J. B., Hickey A. C., Brining D., Callison J., Safronetz D., Marzi A. et al. 2010; A novel model of lethal Hendra virus infection in African green monkeys and the effectiveness of ribavirin treatment. J Virol 84:9831–9839 [View Article][PubMed]
     [Google Scholar]
  37. Rockx B., Brining D., Kramer J., Callison J., Ebihara H., Mansfield K., Feldmann H. 2011; Clinical outcome of henipavirus infection in hamsters is determined by the route and dose of infection. J Virol 85:7658–7671 [View Article][PubMed]
     [Google Scholar]
  38. Rudd P. A., Cattaneo R., von Messling V. 2006; Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J Virol 80:9361–9370 [View Article][PubMed]
     [Google Scholar]
  39. Schmittgen T. D., Livak K. J. 2008; Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108[PubMed] [CrossRef]
     [Google Scholar]
  40. Tanimura N., Imada T., Kashiwazaki Y., Shamusudin S., Syed Hassan S., Jamaluddin A., Russell G., White J. 2004; Reactivity of anti-Nipah virus monoclonal antibodies to formalin-fixed, paraffin-embedded lung tissues from experimental Nipah and Hendra virus infections. J Vet Med Sci 66:1263–1266[PubMed] [CrossRef]
     [Google Scholar]
  41. Thiel L., Diederich S., Erbar S., Pfaff D., Augustin H. G., Maisner A. 2008; Ephrin-B2 expression critically influences Nipah virus infection independent of its cytoplasmic tail. Virol J 5:163 [View Article][PubMed]
     [Google Scholar]
  42. Travanty E., Zhou B., Zhang H., Di Y. P., Alcorn J. F., Wentworth D. E., Mason R., Wang J. 2015; Differential susceptibilities of human lung primary cells to H1N1 influenza viruses. J Virol 89:11935–11944 [View Article][PubMed]
     [Google Scholar]
  43. Wang L. F., Yu M., Hansson E., Pritchard L. I., Shiell B., Michalski W. P., Eaton B. T. 2000; The exceptionally large genome of Hendra virus: support for creation of a new genus within the family Paramyxoviridae. J Virol 74:9972–9979[PubMed] [CrossRef]
     [Google Scholar]
  44. Weingartl H., Czub S., Copps J., Berhane Y., Middleton D., Marszal P., Gren J., Smith G., Ganske S. et al. 2005; Invasion of the central nervous system in a porcine host by nipah virus. J Virol 79:7528–7534 [View Article][PubMed]
     [Google Scholar]
  45. Wong K. T., Shieh W. J., Kumar S., Norain K., Abdullah W., Guarner J., Goldsmith C. S., Chua K. B., Lam S. K., Tan C. T. 2002; Nipah virus infection: pathology and pathogenesis of an emerging paramyxoviral zoonosis. Am J Pathol 161:2153–2167 [View Article][PubMed]
     [Google Scholar]
  46. Yob J. M., Field H., Rashdi A. M., Morrissy C., van der Heide B., Rota P., bin Adzhar A., White J., Daniels P. et al. 2001; Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerg Infect Dis 7:439–441 [View Article][PubMed]
     [Google Scholar]
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Species-specific and individual differences in Nipah virus replication in porcine and human airway epithelial cells
J. Gen. Virol. 97, 1511 (2016); https://doi.org/10.1099/jgv.0.000483
/content/journal/jgv/10.1099/jgv.0.000483
/content/journal/jgv/10.1099/jgv.0.000483
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