Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1997 Apr;71(4):2866–2872. doi: 10.1128/jvi.71.4.2866-2872.1997

A novel exogenous retrovirus sequence identified in humans.

D J Griffiths 1, P J Venables 1, R A Weiss 1, M T Boyd 1
PMCID: PMC191412  PMID: 9060643

Abstract

A 932-bp retrovirus sequence was cloned by reverse transcriptase PCR from salivary gland tissue of a patient with Sjögren's syndrome. The sequence is related to that of type B and type D retroviruses and was present in a sucrose density gradient fraction corresponding to that of an enveloped retrovirus particle. Sequences amplified from tissues of eight individuals with or without Sjögren's syndrome had over 90% similarity and were present at a level of less than one copy per 10(3) cells. The sequence was not detectable in human genomic DNA by PCR or by Southern hybridization. These data indicate that the sequence represents an infectiously acquired genome, provisionally called human retrovirus 5.

Full Text

The Full Text of this article is available as a PDF (673.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Achong B. G., Mansell P. W., Epstein M. A., Clifford P. An unusual virus in cultures from a human nasopharyngeal carcinoma. J Natl Cancer Inst. 1971 Feb;46(2):299–307. [PubMed] [Google Scholar]
  2. Ali M., Taylor G. P., Pitman R. J., Parker D., Rethwilm A., Cheingsong-Popov R., Weber J. N., Bieniasz P. D., Bradley J., McClure M. O. No evidence of antibody to human foamy virus in widespread human populations. AIDS Res Hum Retroviruses. 1996 Oct 10;12(15):1473–1483. doi: 10.1089/aid.1996.12.1473. [DOI] [PubMed] [Google Scholar]
  3. Barré-Sinoussi F., Chermann J. C., Rey F., Nugeyre M. T., Chamaret S., Gruest J., Dauguet C., Axler-Blin C., Vézinet-Brun F., Rouzioux C. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983 May 20;220(4599):868–871. doi: 10.1126/science.6189183. [DOI] [PubMed] [Google Scholar]
  4. Bohannon R. C., Donehower L. A., Ford R. J. Isolation of a type D retrovirus from B-cell lymphomas of a patient with AIDS. J Virol. 1991 Nov;65(11):5663–5672. doi: 10.1128/jvi.65.11.5663-5672.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boyd M. T., Maclean N., Oscier D. G. Detection of retrovirus in patients with myeloproliferative disease. Lancet. 1989 Apr 15;1(8642):814–817. doi: 10.1016/s0140-6736(89)92273-3. [DOI] [PubMed] [Google Scholar]
  6. Brookes S. M., Pandolfino Y. A., Mitchell T. J., Venables P. J., Shattles W. G., Clark D. A., Entwistle A., Maini R. N. The immune response to and expression of cross-reactive retroviral gag sequences in autoimmune disease. Br J Rheumatol. 1992 Nov;31(11):735–742. doi: 10.1093/rheumatology/31.11.735. [DOI] [PubMed] [Google Scholar]
  7. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  8. Clavel F., Guétard D., Brun-Vézinet F., Chamaret S., Rey M. A., Santos-Ferreira M. O., Laurent A. G., Dauguet C., Katlama C., Rouzioux C. Isolation of a new human retrovirus from West African patients with AIDS. Science. 1986 Jul 18;233(4761):343–346. doi: 10.1126/science.2425430. [DOI] [PubMed] [Google Scholar]
  9. Cohen M., Powers M., O'Connell C., Kato N. The nucleotide sequence of the env gene from the human provirus ERV3 and isolation and characterization of an ERV3-specific cDNA. Virology. 1985 Dec;147(2):449–458. doi: 10.1016/0042-6822(85)90147-3. [DOI] [PubMed] [Google Scholar]
  10. Delassus S., Sonigo P., Wain-Hobson S. Genetic organization of gibbon ape leukemia virus. Virology. 1989 Nov;173(1):205–213. doi: 10.1016/0042-6822(89)90236-5. [DOI] [PubMed] [Google Scholar]
  11. Donahue P. R., Hoover E. A., Beltz G. A., Riedel N., Hirsch V. M., Overbaugh J., Mullins J. I. Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses. J Virol. 1988 Mar;62(3):722–731. doi: 10.1128/jvi.62.3.722-731.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Doolittle R. F., Feng D. F., Johnson M. S., McClure M. A. Origins and evolutionary relationships of retroviruses. Q Rev Biol. 1989 Mar;64(1):1–30. doi: 10.1086/416128. [DOI] [PubMed] [Google Scholar]
  13. Franchini G., Gurgo C., Guo H. G., Gallo R. C., Collalti E., Fargnoli K. A., Hall L. F., Wong-Staal F., Reitz M. S., Jr Sequence of simian immunodeficiency virus and its relationship to the human immunodeficiency viruses. Nature. 1987 Aug 6;328(6130):539–543. doi: 10.1038/328539a0. [DOI] [PubMed] [Google Scholar]
  14. Garry R. F., Fermin C. D., Hart D. J., Alexander S. S., Donehower L. A., Luo-Zhang H. Detection of a human intracisternal A-type retroviral particle antigenically related to HIV. Science. 1990 Nov 23;250(4984):1127–1129. doi: 10.1126/science.1701273. [DOI] [PubMed] [Google Scholar]
  15. Hatfield D., Oroszlan S. The where, what and how of ribosomal frameshifting in retroviral protein synthesis. Trends Biochem Sci. 1990 May;15(5):186–190. doi: 10.1016/0968-0004(90)90159-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heneine W., Lerche N. W., Woods T., Spira T., Liff J. M., Eley W., Yee J. L., Kaplan J. E., Khabbaz R. F. The search for human infection with simian type D retroviruses. J Acquir Immune Defic Syndr. 1993 Sep;6(9):1062–1066. [PubMed] [Google Scholar]
  17. Itescu S., Winchester R. Diffuse infiltrative lymphocytosis syndrome: a disorder occurring in human immunodeficiency virus-1 infection that may present as a sicca syndrome. Rheum Dis Clin North Am. 1992 Aug;18(3):683–697. [PubMed] [Google Scholar]
  18. Jacks T., Madhani H. D., Masiarz F. R., Varmus H. E. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell. 1988 Nov 4;55(3):447–458. doi: 10.1016/0092-8674(88)90031-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kalyanaraman V. S., Sarngadharan M. G., Robert-Guroff M., Miyoshi I., Golde D., Gallo R. C. A new subtype of human T-cell leukemia virus (HTLV-II) associated with a T-cell variant of hairy cell leukemia. Science. 1982 Nov 5;218(4572):571–573. doi: 10.1126/science.6981847. [DOI] [PubMed] [Google Scholar]
  20. Krieg A. M., Steinberg A. D. Retroviruses and autoimmunity. J Autoimmun. 1990 Apr;3(2):137–166. doi: 10.1016/0896-8411(90)90137-h. [DOI] [PubMed] [Google Scholar]
  21. Kuff E. L., Lueders K. K. The intracisternal A-particle gene family: structure and functional aspects. Adv Cancer Res. 1988;51:183–276. doi: 10.1016/s0065-230x(08)60223-7. [DOI] [PubMed] [Google Scholar]
  22. Lackner A. A., Rodriguez M. H., Bush C. E., Munn R. J., Kwang H. S., Moore P. F., Osborn K. G., Marx P. A., Gardner M. B., Lowenstine L. J. Distribution of a macaque immunosuppressive type D retrovirus in neural, lymphoid, and salivary tissues. J Virol. 1988 Jun;62(6):2134–2142. doi: 10.1128/jvi.62.6.2134-2142.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maurer B., Bannert H., Darai G., Flügel R. M. Analysis of the primary structure of the long terminal repeat and the gag and pol genes of the human spumaretrovirus. J Virol. 1988 May;62(5):1590–1597. doi: 10.1128/jvi.62.5.1590-1597.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Moore R., Dixon M., Smith R., Peters G., Dickson C. Complete nucleotide sequence of a milk-transmitted mouse mammary tumor virus: two frameshift suppression events are required for translation of gag and pol. J Virol. 1987 Feb;61(2):480–490. doi: 10.1128/jvi.61.2.480-490.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. O'Connell C., O'Brien S., Nash W. G., Cohen M. ERV3, a full-length human endogenous provirus: chromosomal localization and evolutionary relationships. Virology. 1984 Oct 30;138(2):225–235. doi: 10.1016/0042-6822(84)90347-7. [DOI] [PubMed] [Google Scholar]
  26. Oda T., Ikeda S., Watanabe S., Hatsushika M., Akiyama K., Mitsunobu F. Molecular cloning, complete nucleotide sequence, and gene structure of the provirus genome of a retrovirus produced in a human lymphoblastoid cell line. Virology. 1988 Dec;167(2):468–476. [PubMed] [Google Scholar]
  27. Ono M., Toh H., Miyata T., Awaya T. Nucleotide sequence of the Syrian hamster intracisternal A-particle gene: close evolutionary relationship of type A particle gene to types B and D oncovirus genes. J Virol. 1985 Aug;55(2):387–394. doi: 10.1128/jvi.55.2.387-394.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ono M., Yasunaga T., Miyata T., Ushikubo H. Nucleotide sequence of human endogenous retrovirus genome related to the mouse mammary tumor virus genome. J Virol. 1986 Nov;60(2):589–598. doi: 10.1128/jvi.60.2.589-598.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Patience C., Simpson G. R., Colletta A. A., Welch H. M., Weiss R. A., Boyd M. T. Human endogenous retrovirus expression and reverse transcriptase activity in the T47D mammary carcinoma cell line. J Virol. 1996 Apr;70(4):2654–2657. doi: 10.1128/jvi.70.4.2654-2657.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Payne S. L., Rausch J., Rushlow K., Montelaro R. C., Issel C., Flaherty M., Perry S., Sellon D., Fuller F. Characterization of infectious molecular clones of equine infectious anaemia virus. J Gen Virol. 1994 Feb;75(Pt 2):425–429. doi: 10.1099/0022-1317-75-2-425. [DOI] [PubMed] [Google Scholar]
  31. Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7415–7419. doi: 10.1073/pnas.77.12.7415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Price E. J., Venables P. J. The etiopathogenesis of Sjögren's syndrome. Semin Arthritis Rheum. 1995 Oct;25(2):117–133. doi: 10.1016/s0049-0172(95)80025-5. [DOI] [PubMed] [Google Scholar]
  33. Querat G., Audoly G., Sonigo P., Vigne R. Nucleotide sequence analysis of SA-OMVV, a visna-related ovine lentivirus: phylogenetic history of lentiviruses. Virology. 1990 Apr;175(2):434–447. doi: 10.1016/0042-6822(90)90428-t. [DOI] [PubMed] [Google Scholar]
  34. Renne R., Mergia A., Renshaw-Gegg L. W., Neumann-Haefelin D., Luciw P. A. Regulatory elements in the long terminal repeat (LTR) of simian foamy virus type 3 (SFV-3). Virology. 1993 Jan;192(1):365–369. doi: 10.1006/viro.1993.1045. [DOI] [PubMed] [Google Scholar]
  35. Sagata N., Yasunaga T., Tsuzuku-Kawamura J., Ohishi K., Ogawa Y., Ikawa Y. Complete nucleotide sequence of the genome of bovine leukemia virus: its evolutionary relationship to other retroviruses. Proc Natl Acad Sci U S A. 1985 Feb;82(3):677–681. doi: 10.1073/pnas.82.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  37. Schweizer M., Turek R., Hahn H., Schliephake A., Netzer K. O., Eder G., Reinhardt M., Rethwilm A., Neumann-Haefelin D. Markers of foamy virus infections in monkeys, apes, and accidentally infected humans: appropriate testing fails to confirm suspected foamy virus prevalence in humans. AIDS Res Hum Retroviruses. 1995 Jan;11(1):161–170. doi: 10.1089/aid.1995.11.161. [DOI] [PubMed] [Google Scholar]
  38. Seiki M., Hattori S., Hirayama Y., Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3618–3622. doi: 10.1073/pnas.80.12.3618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shattles W. G., Brookes S. M., Venables P. J., Clark D. A., Maini R. N. Expression of antigen reactive with a monoclonal antibody to HTLV-1 P19 in salivary glands in Sjögren's syndrome. Clin Exp Immunol. 1992 Jul;89(1):46–51. doi: 10.1111/j.1365-2249.1992.tb06875.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Shih A., Misra R., Rush M. G. Detection of multiple, novel reverse transcriptase coding sequences in human nucleic acids: relation to primate retroviruses. J Virol. 1989 Jan;63(1):64–75. doi: 10.1128/jvi.63.1.64-75.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shimotohno K., Takahashi Y., Shimizu N., Gojobori T., Golde D. W., Chen I. S., Miwa M., Sugimura T. Complete nucleotide sequence of an infectious clone of human T-cell leukemia virus type II: an open reading frame for the protease gene. Proc Natl Acad Sci U S A. 1985 May;82(10):3101–3105. doi: 10.1073/pnas.82.10.3101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  43. Silver J., Maudru T., Fujita K., Repaske R. An RT-PCR assay for the enzyme activity of reverse transcriptase capable of detecting single virions. Nucleic Acids Res. 1993 Jul 25;21(15):3593–3594. doi: 10.1093/nar/21.15.3593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Simpson G. R., Patience C., Löwer R., Tönjes R. R., Moore H. D., Weiss R. A., Boyd M. T. Endogenous D-type (HERV-K) related sequences are packaged into retroviral particles in the placenta and possess open reading frames for reverse transcriptase. Virology. 1996 Aug 15;222(2):451–456. doi: 10.1006/viro.1996.0443. [DOI] [PubMed] [Google Scholar]
  45. Sonigo P., Barker C., Hunter E., Wain-Hobson S. Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus. Cell. 1986 May 9;45(3):375–385. doi: 10.1016/0092-8674(86)90323-5. [DOI] [PubMed] [Google Scholar]
  46. Talal N., Dauphinée M. J., Dang H., Alexander S. S., Hart D. J., Garry R. F. Detection of serum antibodies to retroviral proteins in patients with primary Sjögren's syndrome (autoimmune exocrinopathy). Arthritis Rheum. 1990 Jun;33(6):774–781. doi: 10.1002/art.1780330603. [DOI] [PubMed] [Google Scholar]
  47. Thayer R. M., Power M. D., Bryant M. L., Gardner M. B., Barr P. J., Luciw P. A. Sequence relationships of type D retroviruses which cause simian acquired immunodeficiency syndrome. Virology. 1987 Apr;157(2):317–329. doi: 10.1016/0042-6822(87)90274-1. [DOI] [PubMed] [Google Scholar]
  48. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Venables P. J., Brookes S. M., Griffiths D., Weiss R. A., Boyd M. T. Abundance of an endogenous retroviral envelope protein in placental trophoblasts suggests a biological function. Virology. 1995 Aug 20;211(2):589–592. doi: 10.1006/viro.1995.1442. [DOI] [PubMed] [Google Scholar]
  50. Vernant J. C., Buisson G., Magdeleine J., De Thore J., Jouannelle A., Neisson-Vernant C., Monplaisir N. T-lymphocyte alveolitis, tropical spastic paresis, and Sjögren syndrome. Lancet. 1988 Jan 23;1(8578):177–177. doi: 10.1016/s0140-6736(88)92744-4. [DOI] [PubMed] [Google Scholar]
  51. Wain-Hobson S., Sonigo P., Danos O., Cole S., Alizon M. Nucleotide sequence of the AIDS virus, LAV. Cell. 1985 Jan;40(1):9–17. doi: 10.1016/0092-8674(85)90303-4. [DOI] [PubMed] [Google Scholar]
  52. Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES