1887

Abstract

The biological properties of human T-cell leukemia virus type I (HTLV-I) and HTLV type II (HTLV-II) are not well elucidated as cell-free viruses. We established new assay systems to detect the infectivity of cell-free HTLVs and examined the stability of cell-free HTLVs at different temperatures. HTLVs lost infectivity more rapidly than did bovine leukemia virus (BLV), which is genetically related to HTLVs. The half-lives of three HTLV-I strains (two cosmopolitan strains and one Melanesian strain) at 37 °C were approximately 0.6 h, whereas the half-life of a BLV strain was 8.5 h. HTLV-I rapidly lost infectivity unexpectedly at 0 and 4 °C. We examined the stability of vesicular stomatitis virus pseudotypes with HTLV-I, HTLV-II or BLV Env proteins, and the Env proteins of HTLVs were found to be more unstable at 4 and 25 °C than the Env proteins of the BLV. Over the course of the viral life cycle, heat treatment inhibited HTLV-I infection at the phase of attachment to the host cells, and inhibition was more marked upon entry into the cells. The HTLV-I Env surface (SU) protein (gp46) was easily released from virions during incubation at 37 °C. However, this release was inhibited by pre-treatment of the virions with -ethylmaleimide, suggesting that the inter-subunit bond between gp46 SU and gp21 transmembrane (TM) proteins is rearranged by disulfide bond isomerization. HTLVs are highly unstable over a wide range of temperatures because the disulfide bonds between the SU and TM proteins are labile.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.037622-0
2012-03-01
2020-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/3/608.html?itemId=/content/journal/jgv/10.1099/vir.0.037622-0&mimeType=html&fmt=ahah

References

  1. Bangham C. R. M.. 2003; The immune control and cell-to-cell spread of human T-lymphotropic virus type 1. J Gen Virol84:3177–3189 [CrossRef][PubMed]
    [Google Scholar]
  2. Beer C., Meyer A., Müller K., Wirth M.. 2003; The temperature stability of mouse retroviruses depends on the cholesterol levels of viral lipid shell and cellular plasma membrane. Virology308:137–146 [CrossRef][PubMed]
    [Google Scholar]
  3. Clapham P., Nagy K., Weiss R. A.. 1984; Pseudotypes of human T-cell leukemia virus types 1 and 2: neutralization by patients’ sera. Proc Natl Acad Sci U S A81:2886–2889 [CrossRef][PubMed]
    [Google Scholar]
  4. Delebecque F., Pramberger K., Prévost M. C., Brahic M., Tangy F.. 2002; A chimeric human T-cell lymphotropic virus type 1 with the envelope glycoprotein of Moloney murine leukemia virus is infectious for murine cells. J Virol76:7883–7889 [CrossRef][PubMed]
    [Google Scholar]
  5. Derse D., Hill S. A., Lloyd P. A., Chung H.-k., Morse B. A.. 2001; Examining human T-lymphotropic virus type 1 infection and replication by cell-free infection with recombinant virus vectors. J Virol75:8461–8468 [CrossRef][PubMed]
    [Google Scholar]
  6. Dougherty R. M.. 1961; Heat inactivation of Rous sarcoma virus. Virology14:371–372 [CrossRef][PubMed]
    [Google Scholar]
  7. Fan N., Gavalchin J., Paul B., Wells K. H., Lane M. J., Poiesz B. J.. 1992; Infection of peripheral blood mononuclear cells and cell lines by cell-free human T-cell lymphoma/leukemia virus type I. J Clin Microbiol30:905–910[PubMed]
    [Google Scholar]
  8. Feng R., Kabayama A., Uchida K., Hoshino H., Miwa M.. 2001; Cell-free entry of human T-cell leukemia virus type 1 to mouse cells. Jpn J Cancer Res92:410–416 [CrossRef][PubMed]
    [Google Scholar]
  9. Feuer G., Green P. L.. 2005; Comparative biology of human T-cell lymphotropic virus type 1 (HTLV-1) and HTLV-2. Oncogene24:5996–6004 [CrossRef][PubMed]
    [Google Scholar]
  10. Fischinger P. J., Peebles P. T., Nomura S., Haapala D. K.. 1973; Isolation of RD-114-like oncornavirus from a cat cell line. J Virol11:978–985[PubMed]
    [Google Scholar]
  11. Gessain A., Barin F., Vernant J. C., Gout O., Maurs L., Calender A., de Thé G.. 1985; Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet2:407–410 [CrossRef][PubMed]
    [Google Scholar]
  12. Ghez D., Lepelletier Y., Jones K. S., Pique C., Hermine O.. 2010; Current concepts regarding the HTLV-1 receptor complex. Retrovirology7:99 [CrossRef][PubMed]
    [Google Scholar]
  13. Haapala D. K., Robey W. G., Oroszlan S. D., Tsai W. P.. 1985; Isolation from cats of an endogenous type C virus with a novel envelope glycoprotein. J Virol53:827–833[PubMed]
    [Google Scholar]
  14. Haraguchi Y., Yang D. W., Handa A., Shimizu N., Tanaka Y., Hoshino H.. 1994; Detection of neutralizing antibodies against human T-cell leukemia virus type 1 using a cell-free infection system and polymerase chain reaction. Int J Cancer59:416–421 [CrossRef][PubMed]
    [Google Scholar]
  15. Hinuma Y., Nagata K., Hanaoka M., Nakai M., Matsumoto T., Kinoshita K. I., Shirakawa S., Miyoshi I.. 1981; Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci U S A78:6476–6480 [CrossRef][PubMed]
    [Google Scholar]
  16. Ho D. D.. 1997; Perspectives series: host/pathogen interactions. Dynamics of HIV-1 replication in vivo . J Clin Invest99:2565–2567 [CrossRef][PubMed]
    [Google Scholar]
  17. Hoshino H., Shimoyama M., Miwa M., Sugimura T.. 1983a; Detection of lymphocytes producing a human retrovirus associated with adult T-cell leukemia by syncytia induction assay. Proc Natl Acad Sci U S A80:7337–7341 [CrossRef][PubMed]
    [Google Scholar]
  18. Hoshino H., Esumi H., Miwa M., Shimoyama M., Minato K., Tobinai K., Hirose M., Watanabe S., Inada N.. other authors 1983b; Establishment and characterization of 10 cell lines derived from patients with adult T-cell leukemia. Proc Natl Acad Sci U S A80:6061–6065 [CrossRef][PubMed]
    [Google Scholar]
  19. Hoshino H., Clapham P. R., Weiss R. A., Miyoshi I., Yoshida M., Miwa M.. 1985; Human T-cell leukemia virus type I: pseudotype neutralization of Japanese and American isolates with human and rabbit sera. Int J Cancer36:671–675 [CrossRef][PubMed]
    [Google Scholar]
  20. Jacobson S., Raine C. S., Mingioli E. S., McFarlin D. E.. 1988; Isolation of an HTLV-1-like retrovirus from patients with tropical spastic paraparesis. Nature331:540–543 [CrossRef][PubMed]
    [Google Scholar]
  21. Johnston E. R., Radke K.. 2000; The SU and TM envelope protein subunits of bovine leukemia virus are linked by disulfide bonds, both in cells and in virions. J Virol74:2930–2935 [CrossRef][PubMed]
    [Google Scholar]
  22. Jones K. S., Petrow-Sadowski C., Huang Y. K., Bertolette D. C., Ruscetti F. W.. 2008; Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4+ T cells. Nat Med14:429–436 [CrossRef][PubMed]
    [Google Scholar]
  23. Kalyanaraman V. S., Sarngadharan M. G., Robert-Guroff M., Miyoshi I., Golde D., Gallo R. C.. 1982; A new subtype of human T-cell leukemia virus (HTLV-II) associated with a T-cell variant of hairy cell leukemia. Science218:571–573 [CrossRef][PubMed]
    [Google Scholar]
  24. Li K. J., Zhang S. J., Kronqvist M., Wallin M., Ekström M., Derse D., Garoff H.. 2008; Intersubunit disulfide isomerization controls membrane fusion of human T-cell leukemia virus Env. J Virol82:7135–7143 [CrossRef][PubMed]
    [Google Scholar]
  25. McAllister R. M., Gardner M. B., Greene A. E., Bradt C., Nichols W. W., Landing B. H.. 1971; Cultivation in vitro of cells derived from a human osteosarcoma. Cancer27:397–402 [CrossRef][PubMed]
    [Google Scholar]
  26. Michalski F., Parks N. F., Sokol F., Clark H. F.. 1976; Thermal inactivation of rabies and other rhabdoviruses: stabilization by the chelating agent ethylenediaminetetraacetic acid at physiological temperatures. Infect Immun14:135–143[PubMed]
    [Google Scholar]
  27. Miyoshi I., Kubonishi I., Yoshimoto S., Akagi T., Ohtsuki Y., Shiraishi Y., Nagata K., Hinuma Y.. 1981; Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T cells. Nature294:770–771 [CrossRef][PubMed]
    [Google Scholar]
  28. Miyoshi I., Yoshimoto S., Taguchi H., Kubonishi I., Fujishita M., Ohtsuki Y., Shiraishi Y., Akagi T.. 1983; Transformation of rabbit lymphocytes with T-cell leukemia virus. Gann74:1–4[PubMed]
    [Google Scholar]
  29. Moore J. P., McKeating J. A., Huang Y. X., Ashkenazi A., Ho D. D.. 1992; Virions of primary human immunodeficiency virus type 1 isolates resistant to soluble CD4 (sCD4) neutralization differ in sCD4 binding and glycoprotein gp120 retention from sCD4-sensitive isolates. J Virol66:235–243[PubMed]
    [Google Scholar]
  30. Okochi K., Sato H., Hinuma Y.. 1984; A retrospective study on transmission of adult T cell leukemia virus by blood transfusion: seroconversion in recipients. Vox Sang46:245–253 [CrossRef][PubMed]
    [Google Scholar]
  31. Opstelten D. J., Wallin M., Garoff H.. 1998; Moloney murine leukemia virus envelope protein subunits, gp70 and Pr15E, form a stable disulfide-linked complex. J Virol72:6537–6545[PubMed]
    [Google Scholar]
  32. Osame M., Usuku K., Izumo S., Ijichi N., Amitani H., Igata A., Matsumoto M., Tara M.. 1986; HTLV-I associated myelopathy, a new clinical entity. Lancet1:1031–1032 [CrossRef][PubMed]
    [Google Scholar]
  33. Pinter A., Kopelman R., Li Z., Kayman S. C., Sanders D. A.. 1997; Localization of the labile disulfide bond between SU and TM of the murine leukemia virus envelope protein complex to a highly conserved CWLC motif in SU that resembles the active-site sequence of thiol-disulfide exchange enzymes. J Virol71:8073–8077[PubMed]
    [Google Scholar]
  34. Pique C., Pham D., Tursz T., Dokhélar M. C.. 1992; Human T-cell leukemia virus type I envelope protein maturation process: requirements for syncytium formation. J Virol66:906–913[PubMed]
    [Google Scholar]
  35. Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C.. 1980; 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 A77:7415–7419 [CrossRef][PubMed]
    [Google Scholar]
  36. Shimizu A., Shimizu N., Tanaka A., Jinno-Oue A., Roy B. B., Shinagawa M., Ishikawa O., Hoshino H.. 2004; Human T-cell leukaemia virus type I is highly sensitive to UV-C light. J Gen Virol85:2397–2406 [CrossRef][PubMed]
    [Google Scholar]
  37. Stull H. B., Gazdar A. F.. 1976; Stability of Rauscher leukemia virus under certain laboratory conditions. Proc Soc Exp Biol Med152:554–556[PubMed][CrossRef]
    [Google Scholar]
  38. Takada A., Robison C., Goto H., Sanchez A., Murti K. G., Whitt M. A., Kawaoka Y.. 1997; A system for functional analysis of Ebola virus glycoprotein. Proc Natl Acad Sci U S A94:14764–14769 [CrossRef][PubMed]
    [Google Scholar]
  39. Tanaka Y., Lee B., Inoi T., Tozawa H., Yamamoto N., Hinuma Y.. 1986; Antigens related to three core proteins of HTLV-I (p24, p19 and p15) and their intracellular localizations, as defined by monoclonal antibodies. Int J Cancer37:35–42 [CrossRef][PubMed]
    [Google Scholar]
  40. Van Der Maaten M. J., Miller J. M.. 1975; Replication of bovine leukemia virus in monolayer cell cultures. Bibl Haematol43:360–362[PubMed]
    [Google Scholar]
  41. Vogt V. M.. 1997; Retroviral virions and genomes. In Retroviruses pp.27–69 Edited by John C. M., Stephen H. H., Varmus V. E.. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  42. Wallin M., Ekström M., Garoff H.. 2004; Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J23:54–65 [CrossRef][PubMed]
    [Google Scholar]
  43. Yanagihara R., Nerurkar V. R., Ajdukiewicz A. B.. 1991; Comparison between strains of human T lymphotropic virus type I isolated from inhabitants of the Solomon Islands and Papua New Guinea. J Infect Dis164:443–449 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.037622-0
Loading
/content/journal/jgv/10.1099/vir.0.037622-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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