1887

Abstract

Primary infection by human parvovirus B19 is often accompanied by arthropathy of varying duration, of which the most severe cases can be indistinguishable from rheumatoid arthritis (RA). While this might seem to imply a role in RA pathogenesis, recent studies have verified long-term persistence of B19 DNA in synovial tissue not only in patients with rheumatoid or juvenile arthritis, but also in immunocompetent, non-arthritic individuals with a history of prior B19 infection. However, the latter data are based on PCR amplification of short segments of DNA, with little sequence information. We determined the nucleotide sequence and examined the integrity of the protein-coding regions of B19 genomes persisting in synovial tissue and compared the results with data from synovial tissues of recently infected patients. In synovium of both previously and recently infected subjects, the viral coding regions were found to be present in an apparently continuous, intact DNA molecule. Comparison with sequences reported from blood or bone marrow showed that the synoviotropism or persistence of the B19 virus DNA was not due to exceptional mutations or particular genotype variants. The synovial retention of full-length viral genomes may represent a physiological process functioning in long-term storage of foreign macromolecules in this tissue.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-4-1017
2000-04-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/4/0811017a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-4-1017&mimeType=html&fmt=ahah

References

  1. Anderson, M. J., Davis, L. R., Hodgson, J., Jones, S. E., Murtaza, L., Pattison, J. R., Stroud, C. E. & White, J. M. ( 1982; ). Occurrence of infection with a parvovirus-like agent in children with sickle cell anaemia during a two-year period. Journal of Clinical Pathology 35, 744-749.[CrossRef]
    [Google Scholar]
  2. Anderson, M. J., Lewis, E., Kidd, I. M., Hall, S. M. & Cohen, B. J. ( 1984; ). An outbreak of erythema infectiosum associated with human parvovirus infection. Journal of Hygiene 93, 85-93.[CrossRef]
    [Google Scholar]
  3. Anderson, L. J., Tsou, C., Parker, R. A., Chorba, T. L., Wulff, H., Tattersall, P. & Mortimer, P. P. ( 1986; ). Detection of antibodies and antigens of human parvovirus B19 by enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 24, 522-526.
    [Google Scholar]
  4. Astell, C. R. & Blundell, M. C. ( 1989; ). Sequence of the right hand terminal palindrome of the human B19 parvovirus genome has the potential to form a ‘stem plus arms’ structure. Nucleic Acids Research 17, 5857.[CrossRef]
    [Google Scholar]
  5. Ball-Goodrich, L. J. & Tattersall, P. ( 1992; ). Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice. Journal of Virology 66, 3415-3423.
    [Google Scholar]
  6. Barland, P., Novikoff, A. B. & Hamerman, D. ( 1962; ). Electron microscopy of the human synovial membrane. Journal of Cell Biology 14, 207-220.[CrossRef]
    [Google Scholar]
  7. Blundell, M. C., Beard, C. & Astell, C. R. ( 1987; ). In vitro identification of a B19 parvovirus promoter. Virology 157, 534-538.[CrossRef]
    [Google Scholar]
  8. Brown, T., Anand, A., Ritchie, L. D., Clewley, J. P. & Reid, T. M. S. (1984). Intrauterine parvovirus infection associated with hydrops fetalis. Lancet ii, 1033–1034.
  9. Brown, K. E., Anderson, S. M. & Young, N. S. ( 1993; ). Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262, 114-117.[CrossRef]
    [Google Scholar]
  10. Burmester, G. R., Dimitriu-Bona, A., Waters, S. J. & Winchester, R. J. ( 1983; ). Identification of three major synovial lining cell populations by monoclonal antibodies directed to Ia antigens and antigens associated with monocytes/macrophages and fibroblasts. Scandinavian Journal of Immunology 17, 69-82.[CrossRef]
    [Google Scholar]
  11. Cassinotti, P., Burtonboy, G., Fopp, M. & Siegl, G. ( 1997; ). Evidence for persistence of human parvovirus B19 DNA in bone marrow. Journal of Medical Virology 53, 229-232.[CrossRef]
    [Google Scholar]
  12. Chang, S.-F., Sgro, J.-Y. & Parrish, C. R. ( 1992; ). Multiple amino acids in the capsid structure of canine parvovirus coordinately determine the canine host range and specific antigenic and hemagglutination properties. Journal of Virology 66, 6858-6867.
    [Google Scholar]
  13. Cooling, L. L. W., Koerner, T. A. W. & Naides, S. J. ( 1995; ). Multiple glycosphingolipids determine the tissue tropism of parvovirus B19. Journal of Infectious Diseases 172, 1198-1205.[CrossRef]
    [Google Scholar]
  14. Cossart, Y. E., Field, A. M., Cant, B. & Widdows, D. (1975). Parvovirus-like particles in human sera. Lancet i, 72–73.
  15. Cotmore, S. F., McKie, V. C., Anderson, L. J., Astell, C. R. & Tattersall, P. ( 1986; ). Identification of the major structural and nonstructural proteins encoded by human parvovirus B19 and mapping of their genes by procaryotic expression of isolated genomic fragments. Journal of Virology 60, 548-557.
    [Google Scholar]
  16. Deiss, V., Tratschin, J.-D., Weitz, M. & Siegl, G. ( 1990; ). Cloning of the human parvovirus B19 genome and structural analysis of its palindromic termini. Virology 175, 247-254.[CrossRef]
    [Google Scholar]
  17. Doerig, C., Hirt, B., Antonietti, J.-P. & Beard, P. ( 1990; ). Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription. Journal of Virology 64, 387-396.
    [Google Scholar]
  18. Edwards, J. W. C. & Willoughby, D. A. ( 1982; ). Demonstration of bone marrow derived cells in synovial lining by means of giant intracellular granules as genetic markers. Annals of the Rheumatic Diseases 41, 177-182.[CrossRef]
    [Google Scholar]
  19. Erdman, D. D., Durigon, E. L., Wang, Q.-Y. & Anderson, L. J. ( 1996; ). Genetic diversity of human parvovirus B19: sequence analysis of the VP1/VP2 gene from multiple isolates. Journal of General Virology 77, 2767-2774.[CrossRef]
    [Google Scholar]
  20. Felsenstein, J. ( 1989; ). PHYLIP – Phylogeny inference package. (version 3.2). Cladistics 5, 164-166.
    [Google Scholar]
  21. Franssila, R., Söderlund, M., Brown, C. S., Spaan, W. J. M., Seppälä, I. & Hedman, K. ( 1996; ). IgG subclass response to human parvovirus B19 infection. Clinical and Diagnostic Virology 6, 41-49.[CrossRef]
    [Google Scholar]
  22. Fraser, J. R., Clarris, B. J. & Baxter, E. ( 1979; ). Patterns of induced variation in the morphology, hyaluronic acid secretion, and lysosomal enzyme activity of cultured human synovial cells. Annals of the Rheumatic Diseases 38, 287-294.[CrossRef]
    [Google Scholar]
  23. Haseyama, K., Kudoh, T., Yoto, Y., Suzuki, N. & Chiba, S. ( 1998; ). Analysis of genetic diversity in the VP1 unique region gene of human parvovirus B19 using the mismatch detection method and direct nucleotide sequencing. Journal of Medical Virology 56, 205-209.[CrossRef]
    [Google Scholar]
  24. Hemauer, A., von Poblotzki, A., Gigler, A., Cassinotti, P., Siegl, G., Wolf, H. & Modrow, S. ( 1996; ). Sequence variability among different parvovirus B19 isolates. Journal of General Virology 77, 1781-1785.[CrossRef]
    [Google Scholar]
  25. Kaikkonen, L., Lankinen, H., Harjunpää, I., Hokynar, K., Söderlund-Venermo, M., Oker-Blom, C., Hedman, L. & Hedman, K. ( 1999; ). Acute-phase-specific heptapeptide epitope for diagnosis of parvovirus B19 infection. Journal of Clinical Microbiology 37, 3952-3956.
    [Google Scholar]
  26. Kerr, J. R., Cartron, J. P., Curran, M. D., Moore, J. E., Elliott, J. R. & Mollan, R. A. ( 1995; ). A study of the role of parvovirus B19 in rheumatoid arthritis. British Journal of Rheumatology 34, 809-813.[CrossRef]
    [Google Scholar]
  27. Kurtzman, G. J., Cohen, B., Meyers, P., Amunullah, A. & Young, N. S. (1988). Persistent B19 parvovirus infection as a cause of severe chronic anaemia in children with acute lymphocytic leukaemia. Lancet ii, 1159–1162.
  28. Leruez, M., Pallier, C., Vassias, I., Elouet, J. F., Romeo, P. & Morinet, F. ( 1994; ). Differential transcription, without replication, of non-structural and structural genes of human parvovirus B19 in the UT7/EPO cell line as demonstrated by in situ hybridization. Journal of General Virology 75, 1475-1478.[CrossRef]
    [Google Scholar]
  29. Liu, J. M., Green, S. W., Shimada, T. & Young, N. S. ( 1992; ). A block in full-length transcript maturation in cells nonpermissive for B19 parvovirus. Journal of Virology 66, 4686-4692.
    [Google Scholar]
  30. Lundqvist, A., Tolfvenstam, T., Brytting, M., Stolt, C. M., Hedman, K. & Broliden, K. ( 1999; ). Prevalence of parvovirus B19 DNA in bone marrow of patients with haematological disorders. Scandinavian Journal of Infectious Diseases 31, 119-122.[CrossRef]
    [Google Scholar]
  31. Miller, E., Fairley, C. K., Cohen, B. J. & Seng, C. ( 1998; ). Immediate and long term outcome of human parvovirus B19 infection in pregnancy. British Journal of Obstetrics & Gynaecology 105, 174-178.[CrossRef]
    [Google Scholar]
  32. Mori, J., Beattie, P., Melton, D. W., Cohen, B. J. & Clewley, J. P. ( 1987; ). Structure and mapping of the DNA of human parvovirus B19. Journal of General Virology 68, 2797-2806.[CrossRef]
    [Google Scholar]
  33. Morinet, F., Tratschin, J. D., Perol, Y. & Siegl, G. ( 1986; ). Comparison of 17 isolates of the human parvovirus B19 by restriction enzyme analysis. Archives of Virology 90, 165-172.[CrossRef]
    [Google Scholar]
  34. Naides, S. J. ( 1993; ). Parvovirus B19 infection. Rheumatic Disease Clinics of North America 19, 457-475.
    [Google Scholar]
  35. Nguyen, Q. T., Sifer, C., Schneider, V., Bernaudin, F., Auguste, V. & Garbarg-Chenon, A. ( 1998; ). Detection of an erythrovirus sequence distinct from B19 in a child with acute anaemia. Lancet 352, 1524.
    [Google Scholar]
  36. Nguyen, Q. T., Sifer, C., Schneider, V., Allaume, X., Servant, A., Bernaudin, F., Auguste, V. & Garbarg-Chenon, A. ( 1999; ). Novel human erythrovirus associated with transient aplastic anemia. Journal of Clinical Microbiology 37, 2483-2487.
    [Google Scholar]
  37. Nikkari, S., Roivainen, A., Hannonen, P., Möttönen, T., Luukkainen, R., Yli-Jama, T. & Toivanen, P. ( 1995; ). Persistence of parvovirus B19 in synovial fluid and bone marrow. Annals of the Rheumatic Diseases 54, 597-600.[CrossRef]
    [Google Scholar]
  38. Ozawa, K., Kurtzman, G. & Young, N. ( 1986; ). Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233, 883-886.[CrossRef]
    [Google Scholar]
  39. Ozawa, K., Ayub, J., Hao, Y.-S., Kurtzman, G., Shimada, T. & Young, N. ( 1987; ). Novel transcription map for the B19 (human) pathogenic parvovirus. Journal of Virology 61, 2395-2406.
    [Google Scholar]
  40. Pattison, J. R., Jones, S. E., Hodgson, J., Davis, L. R., White, J. M., Stroud, C. E. & Murtaza, L. (1981). Parvovirus infections and hypoplastic crisis in sickle-cell anaemia. Lancet i, 664–665.
  41. Reid, D. M., Reid, T. M. S., Brown, T., Rennie, R. A. N. & Eastmond, C. J. (1985). Human parvovirus-associated arthritis: a clinical and laboratory description. Lancet i, 422–425.
  42. Saal, J. G., Steidle, M., Einsele, H., Muller, C. A., Fritz, P. & Zacher, J. ( 1992; ). Persistence of B19 parvovirus in synovial membranes of patients with rheumatoid arthritis. Rheumatology International 12, 147-151.[CrossRef]
    [Google Scholar]
  43. Serjeant, G. R., Topley, J. M., Mason, K., Serjeant, B. E., Pattison, J. R., Jones, S. E. & Mohamed, R. (1981). Outbreak of aplastic crises in sickle-cell anaemia associated with parvovirus-like agent. Lancet ii, 595–597.
  44. Shade, R. O., Blundell, M. C., Cotmore, S. F., Tattersall, P. & Astell, C. R. ( 1986; ). Nucleotide sequence and genome organization of human parvovirus B19 isolated from the serum of a child during aplastic crisis. Journal of Virology 58, 921-936.
    [Google Scholar]
  45. Söderlund, M., Brown, C. S., Spaan, W. J. M., Hedman, L. & Hedman, K. ( 1995; ). Epitope type-specific IgG responses to capsid proteins VP1 and VP2 of human parvovirus B19. Journal of Infectious Diseases 172, 1431-1436.[CrossRef]
    [Google Scholar]
  46. Söderlund, M., von Essen, R., Haapasaari, J., Kiistala, U., Kiviluoto, O. & Hedman, K. ( 1997; ). Persistence of parvovirus B19 DNA in synovial membranes of young patients with and without chronic arthropathy. Lancet 349, 1063-1065.[CrossRef]
    [Google Scholar]
  47. Srivastava, A. & Lu, L. ( 1988; ). Replication of B19 parvovirus in highly enriched hematopoietic progenitor cells from normal human bone marrow. Journal of Virology 62, 3059-3063.
    [Google Scholar]
  48. Takahashi, Y., Murai, C., Shibata, S., Munakata, Y., Ishii, T., Ishii, K., Saitoh, T., Sawai, T., Sugamura, K. & Sasaki, T. ( 1998; ). Human parvovirus B19 as a causative agent for rheumatoid arthritis. Proceedings of the National Academy of Sciences, USA 95, 8227-8232.[CrossRef]
    [Google Scholar]
  49. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673-4680.[CrossRef]
    [Google Scholar]
  50. Umene, K. & Nunoue, T. ( 1993; ). Partial nucleotide sequencing and characterization of human parvovirus B19 genome DNAs from damaged human fetuses and from patients with leukemia. Journal of Medical Virology 39, 333-339.[CrossRef]
    [Google Scholar]
  51. Umene, K. & Nunoue, T. ( 1995; ). A new genome type of human parvovirus B19 present in sera of patients with encephalopathy. Journal of General Virology 76, 2645-2651.[CrossRef]
    [Google Scholar]
  52. White, D. G., Woolf, A. D., Mortimer, P. P., Cohen, B. J., Blake, D. R. & Bacon, P. A. (1985). Human parvovirus arthropathy. Lancet i, 419–421.
  53. Wilkinson, L. S., Worrall, J. G., Sinclair, H. D. & Edwards, J. C. ( 1990; ). Immunohistological reassessment of accessory cell populations in normal and diseased human synovium. British Journal of Rheumatology 29, 259-263.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-4-1017
Loading
/content/journal/jgv/10.1099/0022-1317-81-4-1017
Loading

Data & Media loading...

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