1887

Abstract

Human bocavirus (HBoV) 1 is a widespread parvovirus causing acute respiratory disease in young children. In contrast, HBoV2 occurs in the gastrointestinal tract and is potentially associated with gastroenteritis, whilst HBoV3 and -4 infections are less frequent and have not yet been linked with human disease. Due to HBoV1 DNA persistence in the nasopharynx, serology has been advocated as a better alternative for diagnosing acute infections. In constitutionally healthy children, we previously noted that pre-existing HBoV2 immunity in a subsequent HBoV1 infection typically resulted in low or non-existent HBoV1-specific antibody responses. A phenomenon describing such immunological events among related viruses has been known since the 1950s as ‘original antigenic sin’ (OAS). The aim of this study was to characterize this putative OAS phenomenon in a more controlled setting. Follow-up sera of 10 rabbit pairs, inoculated twice with HBoV1–4 virus-like particles (VLPs) or control antigens, in various combinations, were analysed with HBoV1–4 IgG enzyme immunoassays with and without depletion of heterotypic HBoV antibodies. There were no significant IgG boosts after the second inoculation in either the heterologously or the homologously HBoV-inoculated rabbits, but a clear increase in cross-reactivity was seen with time. We could, however, distinguish a distinct OAS pattern from plain cross-reactivity: half of the heterologously inoculated rabbits showed IgG patterns representative of the OAS hypothesis, in line with our prior results with naturally infected children. HBoVs are the first parvoviruses to show the possible existence of OAS. Our findings provide new information on HBoV1–4 immunity and emphasize the complexity of human bocavirus diagnosis.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000253
2015-10-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/10/3099.html?itemId=/content/journal/jgv/10.1099/jgv.0.000253&mimeType=html&fmt=ahah

References

  1. Allander T. , Tammi M.T. , Eriksson M. , Bjerkner A. , Tiveljung-Lindell A. , Andersson B. . ( 2005;). Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci U S A 102: 12891–12896 [CrossRef] [PubMed].
    [Google Scholar]
  2. Allander T. , Jartti T. , Gupta S. , Niesters H.G.M. , Lehtinen P. , Osterback R. , Vuorinen T. , Waris M. , Bjerkner A. , other authors . ( 2007;). Human bocavirus and acute wheezing in children. Clin Infect Dis 44: 904–910 [CrossRef] [PubMed].
    [Google Scholar]
  3. Alvarez M. , Rodriguez-Roche R. , Bernardo L. , Vázquez S. , Morier L. , Gonzalez D. , Castro O. , Kouri G. , Halstead S.B. , Guzman M.G. . ( 2006;). Dengue hemorrhagic fever caused by sequential dengue 1–3 virus infections over a long time interval: Havana epidemic, 2001–2002. Am J Trop Med Hyg 75: 1113–1117.
    [Google Scholar]
  4. Anderson D.E. , Carlos M.P. , Nguyen L. , Torres J.V. . ( 2001;). Overcoming original (antigenic) sin. Clin Immunol 101: 152–157 [CrossRef] [PubMed].
    [Google Scholar]
  5. Angelova L.A. , Shvartsman Y.A.S. . ( 1982;). Original antigenic sin to influenza in rats. Immunology 46: 183–188.
    [Google Scholar]
  6. Arthur J.L. , Higgins G.D. , Davidson G.P. , Givney R.C. , Ratcliff R.M. . ( 2009;). A novel bocavirus associated with acute gastroenteritis in Australian children. PLoS Pathog 5: e1000391 [CrossRef] [PubMed].
    [Google Scholar]
  7. Bastien N. , Brandt K. , Dust K. , Ward D. , Li Y. . ( 2006;). Human Bocavirus infection, Canada. Emerg Infect Dis 12: 848–850 [CrossRef] [PubMed].
    [Google Scholar]
  8. Berzofsky J.A. , Schechter A.N. , Kon H. . ( 1976;). Does Freund's adjuvant denature protein antigens? EPR studies of emulsified hemoglobin. J Immunol 116: 270–272 [CrossRef] [PubMed].
    [Google Scholar]
  9. Blessing K. , Neske F. , Herre U. , Kreth H.W. , Weissbrich B. . ( 2009;). Prolonged detection of human bocavirus DNA in nasopharyngeal aspirates of children with respiratory tract disease. Pediatr Infect Dis J 28: 1018–1019 [CrossRef] [PubMed].
    [Google Scholar]
  10. Brebion A. , Vanlieferinghen P. , Déchelotte P. , Boutry M. , Peigue-Lafeuille H. , Henquell C. . ( 2014;). Fatal subacute myocarditis associated with human bocavirus 2 in a 13-month-old child. J Clin Microbiol 52: 1006–1008 [CrossRef] [PubMed].
    [Google Scholar]
  11. Brieu N. , Guyon G. , Rodière M. , Segondy M. , Foulongne V. . ( 2008;). Human bocavirus infection in children with respiratory tract disease. Pediatr Infect Dis J 27: 969–973 [CrossRef] [PubMed].
    [Google Scholar]
  12. Chieochansin T. , Kapoor A. , Delwart E. , Poovorawan Y. , Simmonds P. . ( 2009;). Absence of detectable replication of human bocavirus species 2 in respiratory tract. Emerg Infect Dis 15: 1503–1505 [CrossRef] [PubMed].
    [Google Scholar]
  13. Christensen A. , Døllner H. , Skanke L.H. , Krokstad S. , Moe N. , Nordbø S.A. . ( 2013;). Detection of spliced mRNA from human bocavirus 1 in clinical samples from children with respiratory tract infections. Emerg Infect Dis 19: 574–580 [CrossRef] [PubMed].
    [Google Scholar]
  14. Davenport F.M. , Hennessy A.V. , Francis T. Jr . ( 1953;). Epidemiologic and immunologic significance of age distribution of antibody to antigenic variants of influenza virus. J Exp Med 98: 641–656 [CrossRef] [PubMed].
    [Google Scholar]
  15. Edner N. , Castillo-Rodas P. , Falk L. , Hedman K. , Söderlund-Venermo M. , Allander T. . ( 2012;). Life-threatening respiratory tract disease with human bocavirus-1 infection in a 4-year-old child. J Clin Microbiol 50: 531–532 [CrossRef] [PubMed].
    [Google Scholar]
  16. Fazekas de St Groth S. , Webster R.G. . ( 1966;). Disquisitions on original antigenic sin. II. Proof in lower creatures. J Exp Med 124: 347–361 [CrossRef] [PubMed].
    [Google Scholar]
  17. Francis T. Jr . ( 1953;). Influenza: the new acquayantance. Ann Intern Med 39: 203–221 [CrossRef] [PubMed].
    [Google Scholar]
  18. Francis T., Jr . ( 1960;). On the doctrine of original antigenic sin. Proc Am Philos Soc 104: 572–578.
    [Google Scholar]
  19. Fry A.M. , Lu X. , Chittaganpitch M. , Peret T. , Fischer J. , Dowell S.F. , Anderson L.J. , Erdman D. , Olsen S.J. . ( 2007;). Human bocavirus: a novel parvovirus epidemiologically associated with pneumonia requiring hospitalization in Thailand. J Infect Dis 195: 1038–1045 [CrossRef] [PubMed].
    [Google Scholar]
  20. Gulati U. , Kumari K. , Wu W. , Keitel W.A. , Air G.M. . ( 2005;). Amount and avidity of serum antibodies against native glycoproteins and denatured virus after repeated influenza whole-virus vaccination. Vaccine 23: 1414–1425 [CrossRef] [PubMed].
    [Google Scholar]
  21. Guo L. , Wang Y. , Zhou H. , Wu C. , Song J. , Li J. , Paranhos-Baccalà G. , Vernet G. , Wang J. , Hung T. . ( 2012;). Differential seroprevalence of human bocavirus species 1–4 in Beijing, China. PLoS One 7: e39644 [CrossRef] [PubMed].
    [Google Scholar]
  22. Guzmán M.G. , Kouri G. , Valdes L. , Bravo J. , Alvarez M. , Vazques S. , Delgado I. , Halstead S.B. . ( 2000;). Epidemiologic studies on Dengue in Santiago de Cuba, 1997. Am J Epidemiol 152: 793–799 discussion 804.[CrossRef]
    [Google Scholar]
  23. Halstead S.B. , Rojanasuphot S. , Sangkawibha N. . ( 1983;). Original antigenic sin in dengue. Am J Trop Med Hyg 32: 154–156.
    [Google Scholar]
  24. Hedman L. , Söderlund-Venermo M. , Jartti T. , Ruuskanen O. , Hedman K. . ( 2010;). Dating of human bocavirus infection with protein-denaturing IgG-avidity assays – secondary immune activations are ubiquitous in immunocompetent adults. J Clin Virol 48: 44–48 [CrossRef] [PubMed].
    [Google Scholar]
  25. Jartti T. , Hedman K. , Jartti L. , Ruuskanen O. , Allander T. , Söderlund-Venermo M. . ( 2012;). Human bocavirus – the first 5 years. Rev Med Virol 22: 46–64 [CrossRef] [PubMed].
    [Google Scholar]
  26. Jensen K.E. , Davenport F.M. , Hennessy A.V. , Francis T. Jr . ( 1956;). Characterization of influenza antibodies by serum absorption. J Exp Med 104: 199–209 [CrossRef] [PubMed].
    [Google Scholar]
  27. Jula A. , Waris M. , Kantola K. , Peltola V. , Söderlund-Venermo M. , Hedman K. , Ruuskanen O. . ( 2013;). Primary and secondary human bocavirus 1 infections in a family, Finland. Emerg Infect Dis 19: 1328–1331 [CrossRef] [PubMed].
    [Google Scholar]
  28. Kantola K. , Hedman L. , Allander T. , Jartti T. , Lehtinen P. , Ruuskanen O. , Hedman K. , Söderlund-Venermo M. . ( 2008;). Serodiagnosis of human bocavirus infection. Clin Infect Dis 46: 540–546 [CrossRef] [PubMed].
    [Google Scholar]
  29. Kantola K. , Hedman L. , Arthur J. , Alibeto A. , Delwart E. , Jartti T. , Ruuskanen O. , Hedman K. , Söderlund-Venermo M. . ( 2011;). Seroepidemiology of human bocaviruses 1–4. J Infect Dis 204: 1403–1412 [CrossRef] [PubMed].
    [Google Scholar]
  30. Kantola K. , Hedman L. , Tanner L. , Simell V. , Mäkinen M. , Partanen J. , Sadegh M. , Veijola R. , Knip M. , Ilonen J. , Hyöty H. , Toppari J. , Simell O. , Hedman K. , Söderlund-Venermo M. . ( 2015; B-Cell Responses to Human Bocaviruses 1–4: New Insights from a Childhood Follow-Up Study. PLoS One.
  31. Kapoor A. , Slikas E. , Simmonds P. , Chieochansin T. , Naeem A. , Shaukat S. , Alam M.M. , Sharif S. , Angez M. , other authors . ( 2009;). A newly identified bocavirus species in human stool. J Infect Dis 199: 196–200 [CrossRef] [PubMed].
    [Google Scholar]
  32. Kapoor A. , Simmonds P. , Slikas E. , Li L. , Bodhidatta L. , Sethabutr O. , Triki H. , Bahri O. , Oderinde B.S. , other authors . ( 2010;). Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J Infect Dis 201: 1633–1643 [CrossRef] [PubMed].
    [Google Scholar]
  33. Kesebir D. , Vazquez M. , Weibel C. , Shapiro E.D. , Ferguson D. , Landry M.L. , Kahn J.S. . ( 2006;). Human bocavirus infection in young children in the United States: molecular epidemiological profile and clinical characteristics of a newly emerging respiratory virus. J Infect Dis 194: 1276–1282 [CrossRef] [PubMed].
    [Google Scholar]
  34. Kim J.H. , Skountzou I. , Compans R. , Jacob J. . ( 2009;). Original antigenic sin responses to influenza viruses. J Immunol 183: 3294–3301 [CrossRef] [PubMed].
    [Google Scholar]
  35. Kim J.H. , Davis W.G. , Sambhara S. , Jacob J. . ( 2012;). Strategies to alleviate original antigenic sin responses to influenza viruses. Proc Natl Acad Sci U S A 109: 13751–13756 [CrossRef] [PubMed].
    [Google Scholar]
  36. Körner R.W. , Söderlund-Venermo M. , van Koningsbruggen-Rietschel S. , Kaiser R. , Malecki M. , Schildgen O. . ( 2011;). Severe human bocavirus infection, Germany. Emerg Infect Dis 17: 2303–2305 [CrossRef] [PubMed].
    [Google Scholar]
  37. Kundu S.K. , Dupuis M. , Sette A. , Celis E. , Dorner F. , Eibl M. , Merigan T.C. . ( 1998;). Role of preimmunization virus sequences in cellular immunity in HIV-infected patients during HIV type 1 MN recombinant gp160 immunization. AIDS Res Hum Retroviruses 14: 1669–1678 [CrossRef] [PubMed].
    [Google Scholar]
  38. Lehtoranta L. , Söderlund-Venermo M. , Nokso-Koivisto J. , Toivola H. , Blomgren K. , Hatakka K. , Poussa T. , Korpela R. , Pitkäranta A. . ( 2012;). Human bocavirus in the nasopharynx of otitis-prone children. Int J Pediatr Otorhinolaryngol 76: 206–211 [CrossRef] [PubMed].
    [Google Scholar]
  39. Lindner J. , Modrow S. . ( 2008;). Human bocavirus – a novel parvovirus to infect humans. Intervirology 51: 116–122 [CrossRef] [PubMed].
    [Google Scholar]
  40. Martin E.T. , Kuypers J. , McRoberts J.P. , Englund J.A. , Zerr D.M. . ( 2015;). Human bocavirus 1 primary infection and shedding in infants. J Infect Dis 212: 516–524 [CrossRef] [PubMed].
    [Google Scholar]
  41. Midgley C.M. , Bajwa-Joseph M. , Vasanawathana S. , Limpitikul W. , Wills B. , Flanagan A. , Waiyaiya E. , Tran H.B. , Cowper A.E. , other authors . ( 2011;). An in-depth analysis of original antigenic sin in dengue virus infection. J Virol 85: 410–421 [CrossRef] [PubMed].
    [Google Scholar]
  42. Mitui M.T. , Shahnawaz Bin Tabib S.M. , Matsumoto T. , Khanam W. , Ahmed S. , Mori D. , Akhter N. , Yamada K. , Kabir L. , other authors . ( 2012;). Detection of human bocavirus in the cerebrospinal fluid of children with encephalitis. Clin Infect Dis 54: 964–967 [CrossRef] [PubMed].
    [Google Scholar]
  43. Mongkolsapaya J. , Dejnirattisai W. , Xu X.N. , Vasanawathana S. , Tangthawornchaikul N. , Chairunsri A. , Sawasdivorn S. , Duangchinda T. , Dong T. , other authors . ( 2003;). Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9: 921–927 [CrossRef] [PubMed].
    [Google Scholar]
  44. Muller S. . ( 2004;). Avoiding deceptive imprinting of the immune response to HIV-1 infection in vaccine development. Int Rev Immunol 23: 423–436 [CrossRef] [PubMed].
    [Google Scholar]
  45. Oxford J.S. , Frezza P. , Race E. . ( 1993;). Challenges and strategies for AIDS vaccine development. Vaccine 11: 612–614 [CrossRef] [PubMed].
    [Google Scholar]
  46. Paloniemi M. , Lappalainen S. , Salminen M. , Kätkä M. , Kantola K. , Hedman L. , Hedman K. , Söderlund-Venermo M. , Vesikari T. . ( 2014;). Human bocaviruses are commonly found in stools of hospitalized children without causal association to acute gastroenteritis. Eur J Pediatr 173: 1051–1057 [CrossRef] [PubMed].
    [Google Scholar]
  47. Proença-Modena J.L. , Gagliardi T.B. , Escremim de Paula F. , Iwamoto M.A. , Criado M.F. , Camara A.A. , Acrani G.O. , Cintra O.A.L. , Cervi M.C. , other authors . ( 2011;). Detection of human bocavirus mRNA in respiratory secretions correlates with high viral load and concurrent diarrhea. PLoS One 6: e21083 [CrossRef] [PubMed].
    [Google Scholar]
  48. Schildgen O. , Müller A. , Allander T. , Mackay I.M. , Völz S. , Kupfer B. , Simon A. . ( 2008;). Human bocavirus: passenger or pathogen in acute respiratory tract infections?. Clin Microbiol Rev 21: 291–304 [CrossRef] [PubMed].
    [Google Scholar]
  49. Shen J. , Zhu Q. , Zeng M. , Yu H. . ( 2013;). Detection and genome analysis of human bocavirus 1–4 from hospitalized children with acute lower respiratory tract infection and symptoms of wheezing in Shanghai. Int J Mol Med 32: 1415–1420.
    [Google Scholar]
  50. Söderlund-Venermo M. , Lahtinen A. , Jartti T. , Hedman L. , Kemppainen K. , Lehtinen P. , Allander T. , Ruuskanen O. , Hedman K. . ( 2009;). Clinical assessment and improved diagnosis of bocavirus-induced wheezing in children, Finland. Emerg Infect Dis 15: 1423–1430 [CrossRef] [PubMed].
    [Google Scholar]
  51. Tsuchiya H. , Furukawa M. , Matsui M. , Katsuki K. , Inouye S. . ( 2000;). ‘Original antigenic sin’ phenomenon in neutralizing antibody responses in children with enterovirus meningitis. J Clin Virol 19: 205–207 [CrossRef] [PubMed].
    [Google Scholar]
  52. Uršič T. , Steyer A. , Kopriva S. , Kalan G. , Krivec U. , Petrovec M. . ( 2011;). Human bocavirus as the cause of a life-threatening infection. J Clin Microbiol 49: 1179–1181 [CrossRef] [PubMed].
    [Google Scholar]
  53. Uršič T. , Krivec U. , Kalan G. , Petrovec M. . ( 2014;). [PubMed] Fatal human bocavirus infection in an 18-month-old child with chronic lung disease of prematurity. Pediatr Infect Dis J 34: 111–112.[CrossRef]
    [Google Scholar]
  54. Virelizier J.L. , Allison A.C. , Schild G.C. . ( 1974;). Antibody responses to antigenic determinants of influenza virus hemagglutinin. II. Original antigenic sin: a bone marrow-derived lymphocyte memory phenomenon modulated by thymus-derived lymphocytes. J Exp Med 140: 1571–1578 [CrossRef] [PubMed].
    [Google Scholar]
  55. Webster R.G. . ( 1966;). Original antigenic sin in ferrets: the response to sequential infections with influenza viruses. J Immunol 97: 177–183.
    [Google Scholar]
  56. Webster R.G. , Kasel J.A. , Couch R.B. , Laver W.G. . ( 1976;). Influenza virus subunit vaccines. II. Immunogenicity and original antigenic sin in humans. J Infect Dis 134: 48–58 [CrossRef] [PubMed].
    [Google Scholar]
  57. Wyrzucki A. , Bianchi M. , Kohler I. , Steck M. , Hangartner L. . ( 2015;). Heterosubtypic antibodies to influenza A virus have limited activity against cell-bound virus but are not impaired by strain-specific serum antibodies. J Virol 89: 3136–3144 [CrossRef] [PubMed].
    [Google Scholar]
  58. Zhou Z. , Gao X. , Wang Y. , Zhou H. , Wu C. , Paranhos-Baccalà G. , Vernet G. , Guo L. , Wang J. . ( 2014;). Conserved B-cell epitopes among human bocavirus species indicate potential diagnostic targets. PLoS One 9: e86960 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000253
Loading
/content/journal/jgv/10.1099/jgv.0.000253
Loading

Data & Media loading...

Supplements

Supplementary Data



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error