Skip to main content

Advertisement

SpringerLink
Log in

Expression of endogenous beta retroviruses and Hyal-2 mRNA in immune organs of fetuses and lambs

  • Published:
Virologica Sinica

Abstract

Endogenous beta retroviruses (enJSRV) are highly homologous with Jaagsiekte sheep retrovirus (exJSRV), this exogenous retrovirus is the aetiological agent of ovine pulmonary adenocarcinoma (OPA). The aim of this study was to clarify the function of enJSRV and the immunological mechanisms of its corresponding antibody, that is undetectable in JSRV-infected ovine serum. The expression of enJSRV envelope protein and Hyal-2 mRNA in immune organs and lungs of ovine fetuses and lambs were analyzed by Real-Time reverse transcription PCR and In Situ Hybridization using specific probes. In Situ Hybridization results indicated that the enJSRV envelope protein and Hyal-2 mRNA were expressed in thymus, spleen, mesenteric lymph nodes and lungs at different times, while no positive signals were detected in the negative controls. On the other hand, results from Real-Time reverse transcription PCR analysis showed that in 130d fetuses and 3d newborn lambs the enJSRV mRNA levels were much higher in organs associated with the immune system than that in lungs, especially in the thymus and spleen, but levels of Hyal-2 mRNA expression was not significantly different in all collected tissue. These results provided evidence from an immunology point of view to understand why the circulating antibodies against exJSRV are undetectable in JSRV-infected ovine, and will help to unravel the pathogenesis of JSRV-infected ovine.

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

Similar content being viewed by others

References

  1. Bai J, Bishop, J V, Carlson, J O, et al. 1999. Sequence comparison of JSRV with endogenous proviruses: envelope genotypes and a novel ORF with similarity to a G-protein-coupled receptor. J Virol, 258: 333–343.

    Article  CAS  Google Scholar 

  2. Bai J, Zhu, R Y, Stedman, K, et al. 1996. Unique long terminal repeat U3 sequences distinguish exogenous jaagsiekte sheep retroviruses associated with ovine pulmonary carcinoma from endogenous loci in the sheep genome. J Virol, 70: 3159–3168.

    PubMed  CAS  Google Scholar 

  3. de Parseval N, Heidmann T. 2005. Human endogenous retroviruses: from infectious elements to human genes. Cytogenetic Genome Res, 110: 318–332.

    Article  Google Scholar 

  4. Feng Y M. 2004. Histogenesis of the Mongolian sheep embryonic liver and spleen. J Inner Mongolia Agric Univ, 3: 132–138.

    Google Scholar 

  5. Golovkina T V, Chervonsky A, Dudley J P, et al. 1992. Transgenic mouse mammary tumor virus super antigen expression prevents viral infection. Cell, 69: 637–645.

    Article  PubMed  CAS  Google Scholar 

  6. Griebel P J. 1998. Sheep Immunology. In: Handbook of Vertebrate Immunology. Pastoret P P, Griebel P, Bazin H, et al. eds. London: Academic Press. p485–554.

    Google Scholar 

  7. Hecht S J, Carlson J O, DeMartini J C. 1994. Analysis of a type D retroviral capsid gene expressed in ovine pulmonary carcinoma and present in both affected and unaffected sheep genomes. J Virol, 202:480–484.

    Article  CAS  Google Scholar 

  8. Hecht S J, Stedman K E, Carlson J O, et al. 1996. Distribution of endogenous type B and type D sheep retrovirus sequences in ungulates and other mammals. Proc Natl Acad Sci USA, 93:3297–302.

    Article  PubMed  CAS  Google Scholar 

  9. Held W, Shakhov A N, Izui S, et al. 1993. Superantigen-reactive CD4+ T cells are required to stimulate B cells after infection with mouse mammary tumor virus. J Exp Med, 177: 359–366.

    Article  PubMed  CAS  Google Scholar 

  10. Mornex J F, Thivolet F, De las Heras M, et al. 2003. Pathology of human bronchioloalveolar carcinoma and its relationship to the ovine disease. Curr Top Microbiol Immunol, 275:225–248.

    Article  PubMed  CAS  Google Scholar 

  11. Nakagawa K, Harrison L C. 1996. The potential roles of endogenous retroviruses in autoimmunity. Immunol Rev, 152:193–236.

    Article  PubMed  CAS  Google Scholar 

  12. Ortin A, Minguijon E, Dewar P, et al. 1998. Lack of a specific immune response against a recombinant capsid protein of Jaagsiekte sheep retrovirus in sheep and goats naturally affected by enzootic nasal tumor or sheep pulmonary adenomatosis. Vet Immunol Immunopathol, 61: 229–237.

    Article  PubMed  CAS  Google Scholar 

  13. Palmarini M, Cousens C, Dalziel R G, et al. 1996a. The exogenous form of Jaagsiekte retrovirus is specifically associated with a contagious lung cancer of sheep. J Virol, 70:1618–1623.

    PubMed  CAS  Google Scholar 

  14. Palmarini M, Datta S, Omid R, et al. 2000a. The long terminal repeat of jaagsiekte sheep retrovirus is preferentially active in differential epithelial cells of the lungs. J Virol, 74:5776–5787.

    Article  PubMed  CAS  Google Scholar 

  15. Palmarini M, Dewar P, De las Heras M, et al. 1995. Epithelial tumor cells in the lungs of sheep with pulmonary adenomatosis are major sites of replication for Jaagsiekte retrovirus. J Gen Virol, 76:2731–2737.

    Article  PubMed  CAS  Google Scholar 

  16. Palmarini M, Gray C A, Carpenter K, et al. 2001. Expression of endogenous betaretroviruses in the ovine uterus: effects of neonatal age, estrous cycle, pregnancy, and progesterone. J Virol, 75:11319–11327.

    Article  PubMed  CAS  Google Scholar 

  17. Palmarini M, Hallwirth C, York D, et al. 2000b. Molecular cloning and functional analysis of three type D endogenous retroviruses of sheep reveals a different cell tropism from that of the highly related exogenous jaagsiekte sheep retrovirus. J Virol, 74: 8065–8076.

    Article  PubMed  CAS  Google Scholar 

  18. Palmarini M, Holland M J, Cousens C, et al. 1996b. Jaagsiekte retrovirus establishes a disseminated infection of the lymphoid tissues of sheep affected by pulmonary adenomatosis. J Gen Virol, 77: 2991–2998.

    Article  PubMed  CAS  Google Scholar 

  19. Palmarini M, Mura M, Spencer T E. 2004. Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation. J Gen Virol, 85:1–13.

    Article  PubMed  CAS  Google Scholar 

  20. Rai S K, Demartini J C, Miller A D. 2000. Retrovirus vector bearing jaagsiekte sheep retrovirus Env transduce human cells by using a new receptor localized to chromosome 3p21.3. J Virol, 74:4698–4704.

    Article  PubMed  CAS  Google Scholar 

  21. Rosati S, Pittau M, Alberti A, et al. 2000. An accessory open reading frame (orf-x) of jaagsiekte sheep retrovirus is conserved between different virus isolates. Virus Res, 66:109–116.

    Article  PubMed  CAS  Google Scholar 

  22. Ruprecht K, Gronen F, Sauter M, et al. 2008. Lack of immune responses against multiple sclerosis-associated retrovirus/human endogenous retrovirus W in patients with multiple sclerosis. J Neurovirol, 14:143–151.

    Article  PubMed  CAS  Google Scholar 

  23. Sharp J M, Herring A J. 1983. Sheep pulmonary adenomatosis: demonstration of a protein which cross-reacts with the major core proteins of Mason-Pfizer monkey virus and mouse mammary tumor virus. J Gen Virol, 64: 2323–2327.

    Article  PubMed  CAS  Google Scholar 

  24. Summers C, Neill W, Dewar P, et al. 2002. Systemic immune responses following infection with Jaagsiekte sheep retrovirus and in the terminal stages of ovine pulmonary adenocarcinoma. J Gen Virol, 83:1753–1757.

    PubMed  CAS  Google Scholar 

  25. Spencer T E, Mura M, Gray C A, et al. 2003. Receptor usage and fetal expression of ovine endogenous betaretroviruses: implications for coevolution of endogenous and exogenous retroviruses. J Virol, 77: 749–753.

    Article  PubMed  CAS  Google Scholar 

  26. Spencer T E, Stagg A G, Joyce M M, et al. 1999. Discovery and characterization of endometrial epithelial messenger ribonucleic acids using the ovine uterine gland knockout model. Endocrinology, 140 (9):4070–4080.

    Article  Google Scholar 

  27. York D F, Vigne R, Verwoerd D W, et al. 1992. Nucleotide sequence of the jaagsiekte retrovirus, an exogenous and endogenous type D and B retrovirus of sheep and goats. J Virol, 66:4930–4939.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Animal Science and Veterinary Medicine, Inner Mongolia Agricultural University, Huhhot, 010018, China

    Jing-wei Qi, Xiao-li Wu, Shu-ying Liu & Gui-fang Cao

  2. Key Laboratory of Clinical Diagnosis and Treatment Technology in Animal Disease, Ministry of Agriculture, Huhhot, 010018, China

    Shu-ying Liu

Authors
  1. Jing-wei Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-li Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shu-ying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gui-fang Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shu-ying Liu.

Additional information

Foundation items: The Chinese National Natural Science Foundation (No. 30960271 and No.31160493), Inner Mongolia technological innovation fund (20101808) and the Fund of innovation research team (NDPYTD2010-6).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qi, Jw., Wu, Xl., Liu, Sy. et al. Expression of endogenous beta retroviruses and Hyal-2 mRNA in immune organs of fetuses and lambs. Virol. Sin. 27, 83–92 (2012). https://doi.org/10.1007/s12250-012-3222-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12250-012-3222-4

Key words

Search

Navigation