Skip to main content

Advertisement

SpringerLink
Log in

Molecular characteristics and prevalence of small ruminant lentiviruses in goats in Japan

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Small ruminant lentiviruses (SRLVs), which comprise caprine arthritis-encephalitis virus (CAEV) and maedi-visna virus (MVV), are prevalent in goats and sheep worldwide, including in Japan. However, little is known about the molecular characteristics of goat lentiviruses in Japan. In this study, a molecular and phylogenetic analysis of the long gag region was performed. The phylogenic tree demonstrated that all samples belonged to SRLV subtype B1. Two clusters were identified, with one cluster distinct from previously reported strains of subtype B1. In addition, several alterations in the amino acid sequence were detected in immunodominant epitopes of the gag region. To gain a deeper understanding of the genetic diversity of SRLVs in Japan, it will be necessary to increase the sample size and conduct a broader survey. The present report is important for establishing baseline information on the prevalence of SRLV in Japan and providing data to develop a new, more sensitive diagnostic test for effective control of SRLV.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Ramírez H, Reina R, Amorena B et al (2013) Small ruminant lentiviruses: genetic variability, tropism and diagnosis. Viruses 5:1175–1207. doi:10.3390/v5041175

    Article  PubMed  PubMed Central  Google Scholar 

  2. Minardi da Cruz J, Singh D, Lamara A, Chebloune Y (2013) Small Ruminant Lentiviruses (SRLVs) break the species barrier to acquire new host range. Viruses 5:1867–1884. doi:10.3390/v5071867

    Article  PubMed  PubMed Central  Google Scholar 

  3. Leroux C, Cruz JCM, Mornex J-F (2010) SRLVs: a genetic continuum of lentiviral species in sheep and goats with cumulative evidence of cross species transmission. Curr HIV Res 8:94–100

    Article  PubMed  Google Scholar 

  4. Shah C, Böni J, Huder JB et al (2004) Phylogenetic analysis and reclassification of caprine and ovine lentiviruses based on 104 new isolates: evidence for regular sheep-to-goat transmission and worldwide propagation through livestock trade. Virology 319:12–26. doi:10.1016/j.virol.2003.09.047

    Article  CAS  PubMed  Google Scholar 

  5. Li Y, Zhou F, Li X et al (2013) Development of TaqMan-based qPCR method for detection of caprine arthritis–encephalitis virus (CAEV) infection. Arch Virol 158:2135–2141. doi:10.1007/s00705-013-1728-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Konishi M, Tsuduku S, Haritani M et al (2004) An epidemic of caprine arthritis encephalitis in Japan: isolation of the virus. J Vet Med Sci Jpn Soc Vet Sci 66:911–917

    Article  Google Scholar 

  7. Oguma K, Tanaka C, Harasawa R et al (2014) Isolation of maedi/visna virus from a sheep in Japan. J Vet Med Sci Jpn Soc Vet Sci 76:211–218

    Article  CAS  Google Scholar 

  8. Konishi M, Hiratani M, Kimura K et al (2007) Epidemiological survey and pathological studies on Caprine arthritis-encephalitis (CAE) in Japan. Bull Natl Inst Anim Health 113:23–30

    Google Scholar 

  9. Konishi M, Hayama Y, Shirafuji H et al (2016) Serological survey of caprine arthritis-encephalitis virus infection in Japan. J Vet Med Sci Jpn Soc Vet Sci 78:447–450. doi:10.1292/jvms.15-0357

    Article  CAS  Google Scholar 

  10. Reina R, Berriatua E, Luján L et al (2009) Prevention strategies against small ruminant lentiviruses: an update. Vet J 182:31–37. doi:10.1016/j.tvjl.2008.05.008

    Article  PubMed  Google Scholar 

  11. Peterhans E, Greenland T, Badiola J et al (2004) Routes of transmission and consequences of small ruminant lentiviruses (SRLVs) infection and eradication schemes. Vet Res 35:257–274. doi:10.1051/vetres:2004014

    Article  PubMed  Google Scholar 

  12. de Andrés D, Klein D, Watt NJ et al (2005) Diagnostic tests for small ruminant lentiviruses. Vet Microbiol 107:49–62. doi:10.1016/j.vetmic.2005.01.012

    Article  PubMed  Google Scholar 

  13. Brinkhof J, van Maanen C (2007) Evaluation of five enzyme-linked immunosorbent assays and an agar gel immunodiffusion test for detection of antibodies to small ruminant lentiviruses. Clin Vaccine Immunol 14:1210–1214. doi:10.1128/CVI.00282-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Giangaspero M, Osawa T, Orusa R et al (2011) Epidemiological survey for visna-maedi among sheep in northern prefectures of Japan. Vet Ital 47:437–451

    PubMed  Google Scholar 

  15. Brajon G, Daniela M, Manuele L et al (2012) Development and field testing of a real-time PCR assay for caprine arthritis-encephalitis-virus (CAEV). Open Virol J 6:82–90. doi:10.2174/1874357901206010082

    Article  CAS  PubMed  Google Scholar 

  16. de Andrés X, Ramírez H, Bertolotti L et al (2013) An insight into a combination of ELISA strategies to diagnose small ruminant lentivirus infections. Vet Immunol Immunopathol 152:277–288. doi:10.1016/j.vetimm.2012.12.017

    Article  PubMed  Google Scholar 

  17. González B, Reina R, García I et al (2005) Mucosal immunization of sheep with a Maedi-Visna virus (MVV) env DNA vaccine protects against early MVV productive infection. Vaccine 23:4342–4352. doi:10.1016/j.vaccine.2005.03.032

    Article  PubMed  Google Scholar 

  18. Padiernos RBC, Balbin MM, Parayao AM, Mingala CN (2015) Molecular characterization of the gag gene of caprine arthritis encephalitis virus from goats in the Philippines. Arch Virol 160:969–978. doi:10.1007/s00705-015-2359-5

    Article  CAS  PubMed  Google Scholar 

  19. Leroux C, Vuillermoz S, Mornex J-F, Greenland T (1995) Genomic heterogeneity in the pol region of ovine lentiviruses obtained from bronchoalveolar cells of infected sheep from France. J Gen Virol 76:1533–1537. doi:10.1099/0022-1317-76-6-1533

    Article  CAS  PubMed  Google Scholar 

  20. Leroux C, Chastang J, Greenland T, Mornex JF (1997) Genomic heterogeneity of small ruminant lentiviruses: existence of heterogeneous populations in sheep and of the same lentiviral genotypes in sheep and goats. Arch Virol 142:1125–1137

    Article  CAS  PubMed  Google Scholar 

  21. Zanoni RG (1998) Phylogenetic analysis of small ruminant lentiviruses. J Gen Virol 79:1951–1961. doi:10.1099/0022-1317-79-8-1951

    Article  CAS  PubMed  Google Scholar 

  22. Narayan O, Wolinsky JS, Clements JE et al (1982) Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. J Gen Virol 59:345–356. doi:10.1099/0022-1317-59-2-345

    Article  CAS  PubMed  Google Scholar 

  23. Narayan O, Kennedy-Stoskopf S, Sheffer D et al (1983) Activation of caprine arthritis-encephalitis virus expression during maturation of monocytes to macrophages. Infect Immun 41:67–73

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Gorrell MD, Brandon MR, Sheffer D et al (1992) Ovine lentivirus is macrophagetropic and does not replicate productively in T lymphocyte. J Virol 66:2679–2688

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Guiguen F, Mselli-Lakhal L, Durand J et al (2000) Experimental infection of Mouflon-domestic sheep hybrids with caprine arthritis-encephalitis virus. Am J Vet Res 61:456–461

    Article  CAS  PubMed  Google Scholar 

  26. Larruskain A, Jugo B (2013) Retroviral infections in sheep and goats: small ruminant lentiviruses and host interaction. Viruses 5:2043–2061. doi:10.3390/v5082043

    Article  PubMed  PubMed Central  Google Scholar 

  27. L’Homme Y, Ouardani M, Lévesque V et al (2011) Molecular characterization and phylogenetic analysis of small ruminant lentiviruses isolated from Canadian sheep and goats. Virol J 8:271. doi:10.1186/1743-422X-8-271

    Article  PubMed  PubMed Central  Google Scholar 

  28. Shah C, Huder JB, Boni J et al (2004) Direct evidence for natural transmission of small-ruminant lentiviruses of subtype A4 from goats to sheep and vice versa. J Virol 78:7518–7522. doi:10.1128/JVI.78.14.7518-7522.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fras M, Leboeuf A, Labrie F-M et al (2013) Phylogenetic analysis of small ruminant lentiviruses in mixed flocks: multiple evidence of dual infection and natural transmission of types A2 and B1 between sheep and goats. Infect Genet Evol 19:97–104. doi:10.1016/j.meegid.2013.06.019

    Article  PubMed  Google Scholar 

  30. Santry LA, de Jong J, Gold AC et al (2013) Genetic characterization of small ruminant lentiviruses circulating in naturally infected sheep and goats in Ontario, Canada. Virus Res 175:30–44. doi:10.1016/j.virusres.2013.03.019

    Article  CAS  PubMed  Google Scholar 

  31. Grego E, Profiti M, Giammarioli M et al (2002) Genetic heterogeneity of small ruminant lentiviruses involves immunodominant epitope of capsid antigen and affects sensitivity of single-strain-based immunoassay. Clin Diagn Lab Immunol 9:828–832

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Rosati S, Mannelli A, Merlo T, Ponti N (1999) Characterization of the immunodominant cross-reacting epitope of visna maedi virus and caprine arthritis-encephalitis virus capsid antigen. Virus Res 61:177–183

    Article  CAS  PubMed  Google Scholar 

  33. Tang S, Zhao J, Wang A et al (2010) Characterization of immune responses to capsid protein p24 of human immunodeficiency virus type 1 and implications for detection. Clin Vaccine Immunol CVI 17:1244–1251. doi:10.1128/CVI.00066-10

    Article  CAS  PubMed  Google Scholar 

  34. Mammano F, Ohagen A, Höglund S, Göttlinger HG (1994) Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J Virol 68:4927–4936

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Freed EO (1998) HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251:1–15. doi:10.1006/viro.1998.9398

    Article  CAS  PubMed  Google Scholar 

  36. Provitera P, Goff A, Harenberg A et al (2001) Role of the major homology region in assembly of HIV-1 Gag. Biochemistry (Mosc) 40:5565–5572

    Article  CAS  Google Scholar 

  37. Purdy JG, Flanagan JM, Ropson IJ et al (2008) Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J Virol 82:5951–5961. doi:10.1128/JVI.00214-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Chang Y-F, Wang S-M, Huang K-J, Wang C-T (2007) Mutations in capsid major homology region affect assembly and membrane affinity of HIV-1 Gag. J Mol Biol 370:585–597. doi:10.1016/j.jmb.2007.05.020

    Article  CAS  PubMed  Google Scholar 

  39. Fluri A, Nenci C, Zahno M-L et al (2006) The MHC-haplotype influences primary, but not memory, immune responses to an immunodominant peptide containing T- and B-cell epitopes of the caprine arthritis encephalitis virus Gag protein. Vaccine 24:597–606. doi:10.1016/j.vaccine.2005.08.043

    Article  CAS  PubMed  Google Scholar 

  40. Gamble TR, Vajdos FF, Yoo S et al (1996) Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285–1294

    Article  CAS  PubMed  Google Scholar 

  41. Gamble TR, Yoo S, Vajdos FF et al (1997) Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849–853

    Article  CAS  PubMed  Google Scholar 

  42. Wernike K, Hoffmann B, Kalthoff D et al (2011) Development and validation of a triplex real-time PCR assay for the rapid detection and differentiation of wild-type and glycoprotein E-deleted vaccine strains of Bovine herpesvirus type 1. J Virol Methods 174:77–84. doi:10.1016/j.jviromet.2011.03.028

    Article  CAS  PubMed  Google Scholar 

  43. Fieni F, Rowe J, Van Hoosear K et al (2002) Presence of caprine arthritis-encephalitis virus (CAEV) infected cells in flushing media following oviductal-stage embryo collection. Theriogenology 57:931–940

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

This study was supported by the Research Project for Improving Food Safety and Animal Health of the Ministry of Agriculture, Forestry, and Fisheries of Japan.

Author information

Author notes

  1. Saki Kokawa and Mami Oba contributed equally to this work.

Authors and Affiliations

  1. Faculty of Agriculture, Research and Education Center for Prevention of Global Infectious Diseases of Animals, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo, 183-8509, Japan

    Saki Kokawa, Mami Oba, Miki Omura, Shinobu Tsuchiaka, Tsutomu Omatsu & Tetsuya Mizutani

  2. Faculty of Engineering, University of the Ryukyus, 1 Senbaru, Nishihara-cho, Nakagami District, Okinawa, 903-0129, Japan

    Teppei Hirata & Shiro Tamaki

  3. Department of Bioproduction Science, Ishikawa Prefectural University, Nonoichi, Ishikawa, 921-8836, Japan

    Makoto Nagai

Authors
  1. Saki Kokawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mami Oba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Teppei Hirata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shiro Tamaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miki Omura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shinobu Tsuchiaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Makoto Nagai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tsutomu Omatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tetsuya Mizutani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tsutomu Omatsu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The procedures for blood sample collection from goats were carried out based on the guidelines for animal care and use of Tokyo University of Agriculture and Technology.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kokawa, S., Oba, M., Hirata, T. et al. Molecular characteristics and prevalence of small ruminant lentiviruses in goats in Japan. Arch Virol 162, 3007–3015 (2017). https://doi.org/10.1007/s00705-017-3447-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3447-5

Search

Navigation