Pathogenesis, humoral immune responses, and transmission between cohoused animals in a ferret model of human respiratory syncytial virus infection

Journal of Virology

Volumn 92, Issue 4, 2018, Pages

  Chan, Kok Fei ^a   Carolan, Louise A ^a   Druce, Julian ^a   Chappell, Keith ^b   Watterson, Daniel ^b   Young, Paul ^b   Korenkov, Daniil ^a,e   Subbarao, Kanta ^a   Barr, Ian G ^a,c   Laurie, Karen L ^a,c,d   Reading, Patrick C ^a,d  

^a PETER DOHERTY INSTITUTE FOR INFECTION AND IMMUNITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF BALLARAT   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Russian Federation)

Author keywords

Animal models; Ferret; Respiratory syncytial virus; Respiratory viruses; Transmission

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GRANZYME A; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; TUMOR NECROSIS FACTOR; VIRUS GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL HOUSING; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE MODEL; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HUMORAL IMMUNITY; LOWER RESPIRATORY TRACT; MUSTELA PUTORIUS FURO; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; RESPIRATORY SYNCYTIAL VIRUS INFECTION; UPPER RESPIRATORY TRACT; VIRAL CLEARANCE; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; HELA CELL LINE; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; RESPIRATORY TRACT INFECTION; TRANSMISSION; VIROLOGY; VIRUS LOAD;

ANIMALS; DISEASE MODELS, ANIMAL; FERRETS; HELA CELLS; HUMANS; IMMUNITY, HUMORAL; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; RESPIRATORY TRACT INFECTIONS; VIRAL LOAD; VIRUS REPLICATION;

EID: 85041230240     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01322-17     Document Type: Article

References (37)

1. Afonso CL, Amarasinghe GK, Banyai K, Bao Y, Basler CF, Bavari S, Bejerman N, Blasdell KR, Briand FX, Briese T, Bukreyev A, Calisher CH, Chandran K, Cheng J, Clawson AN, Collins PL, Dietzgen RG, Dolnik O, Domier LL, Durrwald R, Dye JM, Easton AJ, Ebihara H, Farkas SL, Freitas-Astua J, Formenty P, Fouchier RA, Fu Y, Ghedin E, Goodin MM, Hewson R, Horie M, Hyndman TH, Jiang D, Kitajima EW, Kobinger GP, Kondo H, Kurath G, Lamb RA, Lenardon S, Leroy EM, Li CX, Lin XD, Liu L, Longdon B, Marton S, Maisner A, Muhlberger E, Netesov SV, Nowotny N, et al. 2016. Taxonomy of the order Mononegavirales: update 2016. Arch Virol 161: 2351-2360. https://doi.org/10.1007/s00705-016-2880-1
2. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O'Brien KL, Roca A, Wright PF, Bruce N, Chandran A, Theodoratou E, Sutanto A, Sedyaningsih ER, Ngama M, Munywoki PK, Kartasasmita C, Simoes EA, Rudan I, Weber MW, Campbell H. 2010. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 375: 1545-1555. https://doi.org/10.1016/S0140-6736(10)60206-1
3. Scheltema NM, Gentile A, Lucion F, Nokes DJ, Munywoki PK, Madhi SA, Groome MJ, Cohen C, Moyes J, Thorburn K, Thamthitiwat S, Oshitani H, Lupisan SP, Gordon A, Sanchez JF, O'Brien KL, Group PS, Gessner BD, Sutanto A, Mejias A, Ramilo O, Khuri-Bulos N, Halasa N, de-Paris F, Pires MR, Spaeder MC, Paes BA, Simoes EAF, Leung TF, da Costa Oliveira MT, de Freitas Lazaro Emediato CC, Bassat Q, Butt W, Chi H, Aamir UB, Ali A, Lucero MG, Fasce RA, Lopez O, Rath BA, Polack FP, Papenburg J, Roglic S, Ito H, Goka EA, Grobbee DE, Nair H, Bont LJ. 2017. Global respiratory syncytial virus-associated mortality in young children (RSV GOLD): a retrospective case series. Lancet Glob Health 5:e984-e991. https://doi .org/10.1016/S2214-109X(17)30344-3
4. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352:1749-1759. https://doi.org/10.1056/NEJMoa043951
5. Cardenas S, Auais A, Piedimonte G. 2005. Palivizumab in the prophylaxis of respiratory syncytial virus infection. Expert Rev Anti Infect Ther 3:719-726. https://doi.org/10.1586/14787210.3.5.719
6. Neuzil KM. 2016. Progress toward a respiratory syncytial virus vaccine. Clin Vaccine Immunol 23:186-188. https://doi.org/10.1128/CVI.00037-16
7. Rezaee F, Linfield DT, Harford TJ, Piedimonte G. 2017. Ongoing developments in RSV prophylaxis: a clinician's analysis. Curr Opin Virol 24: 70-78. https://doi.org/10.1016/j.coviro.2017.03.015
8. Taylor G. 2017. Animal models of respiratory syncytial virus infection. Vaccine 35:469-480. https://doi.org/10.1016/j.vaccine.2016.11.054
9. Mejias A, Chavez-Bueno S, Rios AM, Saavedra-Lozano J, Fonseca Aten M, Hatfield J, Kapur P, Gomez AM, Jafri HS, Ramilo O. 2004. Anti-respiratory syncytial virus (RSV) neutralizing antibody decreases lung inflammation, airway obstruction, and airway hyperresponsiveness in a murine RSV model. Antimicrob Agents Chemother 48:1811-1822. https://doi.org/10 .1128/AAC.48.5.1811-1822.2004
10. Prince GA, Horswood RL, Chanock RM. 1985. Quantitative aspects of passive immunity to respiratory syncytial virus infection in infant cotton rats. J Virol 55:517-520
11. Enkirch T, von Messling V. 2015. Ferret models of viral pathogenesis. Virology 479-480:259-270
12. Coates HV, Chanock RM. 1962. Experimental infection with respiratory syncytial virus in several species of animals. Am J Hyg (Lond.) 76: 302-312
13. Hsu KH, Lubeck MD, Bhat BM, Bhat RA, Kostek B, Selling BH, Mizutani S, Davis AR, Hung PP. 1994. Efficacy of adenovirus-vectored respiratory syncytial virus vaccines in a new ferret model. Vaccine 12:607-612. https://doi.org/10.1016/0264-410X(94)90264-X
14. Prince GA, Porter DD. 1976. The pathogenesis of respiratory syncytial virus infection in infant ferrets. Am J Pathol 82:339-352
15. Stittelaar KJ, de Waal L, van Amerongen G, Veldhuis Kroeze EJ, Fraaij PL, van Baalen CA, van Kampen JJ, van der Vries E, Osterhaus AD, de Swart RL. 2016. Ferrets as a novel animal model for studying human respiratory syncytial virus infections in immunocompetent and immunocompromised hosts. Viruses 8:E168
16. Boukhvalova MS, Prince GA, Blanco JC. 2007. Respiratory syncytial virus infects and abortively replicates in the lungs in spite of preexisting immunity. J Virol 81:9443-9450. https://doi.org/10.1128/JVI.00102-07
17. Krizanova O, Rathova V. 1969. Serum inhibitors of myxoviruses. Curr Top Microbiol Immunol 47:125-151. https://doi.org/10.1007/978-3-642-46160-6_6
18. Lukacs NW, Moore ML, Rudd BD, Berlin AA, Collins RD, Olson SJ, Ho SB, Peebles RS, Jr. 2006. Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am J Pathol 169:977-986. https://doi.org/10.2353/ajpath .2006.051055
19. Stokes KL, Chi MH, Sakamoto K, Newcomb DC, Currier MG, Huckabee MM, Lee S, Goleniewska K, Pretto C, Williams JV, Hotard A, Sherrill TP, Peebles RS, Jr, Moore ML. 2011. Differential pathogenesis of respiratory syncytial virus clinical isolates in BALB/c mice. J Virol 85:5782-5793. https://doi.org/10.1128/JVI.01693-10
20. Moore IN, Lamirande EW, Paskel M, Donahue D, Kenney H, Qin J, Subbarao K. 2014. Severity of clinical disease and pathology in ferrets experimentally infected with influenza viruses is influenced by inoculum volume. J Virol 88:13879-13891. https://doi.org/10.1128/JVI.02341-14
21. Byrd LG, Prince GA. 1997. Animal models of respiratory syncytial virus infection. Clin Infect Dis 25:1363-1368. https://doi.org/10.1086/516152
22. Prince GA, Jenson AB, Horswood RL, Camargo E, Chanock RM. 1978. The pathogenesis of respiratory syncytial virus infection in cotton rats. Am J Pathol 93:771-791
23. Hall CB, Douglas RG, Jr. 1981. Modes of transmission of respiratory syncytial virus. J Pediatr 99:100-103. https://doi.org/10.1016/S0022-3476(81)80969-9
24. Blount RE, Jr, Morris JA, Savage RE. 1956. Recovery of cytopathogenic agent from chimpanzees with coryza. Proc Soc Exp Biol Med 92: 544-549. https://doi.org/10.3181/00379727-92-22538
25. Belser JA, Eckert AM, Tumpey TM, Maines TR. 2016. Complexities in ferret influenza virus pathogenesis and transmission models. Microbiol Mol Biol Rev 80:733-744. https://doi.org/10.1128/MMBR.00022-16
26. Chen TR. 1988. Re-evaluation of HeLa, HeLa S3, and HEp-2 karyotypes. Cytogenet Cell Genet 48:19-24. https://doi.org/10.1159/000132579
27. McKimm-Breschkin JL. 2004. A simplified plaque assay for respiratory syncytial virus-direct visualization of plaques without immunostaining. J Virol Methods 120:113-117. https://doi.org/10.1016/j.jviromet.2004.02 .020
28. Leung VK, Carolan LA, Worth LJ, Harper SA, Peck H, Tilmanis D, Laurie KL, Slavin MA, Sullivan SG. 2017. Influenza vaccination responses: Evaluating impact of repeat vaccination among health care workers. Vaccine 35: 2558-2568. https://doi.org/10.1016/j.vaccine.2017.03.063
29. van Baalen CA, Jeeninga RE, Penders GH, van Gent B, van Beek R, Koopmans MP, Rimmelzwaan GF. 2017. ViroSpot microneutralization assay for antigenic characterization of human influenza viruses. Vaccine 35:46-52. https://doi.org/10.1016/j.vaccine.2016.11.060
30. McLellan JS, Correia BE, Chen M, Yang Y, Graham BS, Schief WR, Kwong PD. 2011. Design and characterization of epitope-scaffold immunogens that present the motavizumab epitope from respiratory syncytial virus. J Mol Biol 409:853-866. https://doi.org/10.1016/j.jmb.2011.04.044
31. Jones ML, Seldon T, Smede M, Linville A, Chin DY, Barnard R, Mahler SM, Munster D, Hart D, Gray PP, Munro TP. 2010. A method for rapid, ligation-independent reformatting of recombinant monoclonal antibodies. J Immunol Methods 354:85-90. https://doi.org/10.1016/j.jim.2010.02 .001
32. Carolan LA, Rockman S, Borg K, Guarnaccia T, Reading P, Mosse J, Kelso A, Barr I, Laurie KL. 2015. Characterization of the localized immune response in the respiratory tract of ferrets following infection with influenza A and B viruses. J Virol 90:2838-2848. https://doi.org/10.1128/JVI.02797-15
33. Carolan LA, Butler J, Rockman S, Guarnaccia T, Hurt AC, Reading P, Kelso A, Barr I, Laurie KL. 2014. TaqMan real time RT-PCR assays for detecting ferret innate and adaptive immune responses. J Virol Methods 205: 38-52. https://doi.org/10.1016/j.jviromet.2014.04.014
34. Pyankov OV, Setoh YX, Bodnev SA, Edmonds JH, Pyankova OG, Pyankov SA, Pali G, Belford S, Lu L, La M, Lovrecz G, Volchkova VA, Chappell KJ, Watterson D, Marsh G, Young PR, Agafonov AA, Farmer JF, Volchkov VE, Suhrbier A, Khromykh AA. 2017. Successful post-exposure prophylaxis of Ebola infected non-human primates using Ebola glycoprotein-specific equine IgG. Sci Rep 7:41537. https://doi.org/10.1038/srep41537
35. Corti D, Bianchi S, Vanzetta F, Minola A, Perez L, Agatic G, Guarino B, Silacci C, Marcandalli J, Marsland BJ, Piralla A, Percivalle E, Sallusto F, Baldanti F, Lanzavecchia A. 2013. Cross-neutralization of four paramyxoviruses by a human monoclonal antibody. Nature 501:439-443. https://doi.org/10.1038/nature12442
36. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340: 1113-1117. https://doi.org/10.1126/science.1234914
37. Lakdawala SS, Jayaraman A, Halpin RA, Lamirande EW, Shih AR, Stockwell TB, Lin X, Simenauer A, Hanson CT, Vogel L, Paskel M, Minai M, Moore I, Orandle M, Das SR, Wentworth DE, Sasisekharan R, Subbarao K. 2015. The soft palate is an important site of adaptation for transmissible influenza viruses. Nature 526:122-125. https://doi .org/10.1038/nature15379