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Spread of HTLV-I Between Lymphocytes by Virus-Induced Polarization of the Cytoskeleton
Tadahiko Igakura,13Jane C. Stinchcombe,4Peter K. C. Goon,1Graham P. Taylor,2Jonathan N. Weber,2Gillian M. Griffiths,4Yuetsu Tanaka,5Mitsuhiro Osame,3Charles R. M. Bangham1*
Cell contact is required for efficient transmission of human
T cell leukemia virus- type 1 (HTLV-I) between cells and betweenindividuals, because naturally infected lymphocytes produce virtuallyno cell-free infectious HTLV-I particles. However, the mechanismof
cell-to-cell spread of HTLV-I is not understood. We show herethat cell
contact rapidly induces polarization of the cytoskeletonof the
infected cell to the cell-cell junction. HTLV-I core (Gagprotein)
complexes and the HTLV-I genome accumulate at the cell-celljunction
and are then transferred to the uninfected cell. Otherlymphotropic
viruses, such as HIV-1, may similarly subvert normalT cell physiology
to allow efficient propagation between cells.
1 Department of Immunology,
2 Department of Genito-Urinary Medicine and
Communicable Diseases, Imperial College London, St. Mary's Campus,
Norfolk Place, London W2 1PG, UK.
3 The Third
Department of Internal Medicine, Faculty of Medicine, Kagoshima
University, 8-35-1 Sakuragaoka, Kagoshima 890-8520, Japan.
4 Sir William Dunn School of Pathology, University
of Oxford, Oxford OX1 3RE, UK.
5 Department of
Infectious Disease and Immunology, Okinawa-Asia Research Center of
Medical Science, Faculty of Medicine, University of the Ryukyus,
Uehara-cho 207, Nishihara, Okinawa 903-0215, Japan.
*
To whom correspondence should be addressed. E-mail:
c.bangham{at}imperial.ac.uk
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PERSPECTIVES
David Derse and Gisela Heidecker (14 March 2003) Science299 (5613), 1670.
[DOI: 10.1126/science.1083218] |Summary »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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J. Immunol.
172, 1735-1743
|Abstract »|Full Text »|PDF »
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C. Jolly, K. Kashefi, M. Hollinshead, and Q. J. Sattentau (2004)
J. Exp. Med.
199, 283-293
|Abstract »|Full Text »|PDF »
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|Abstract »|Full Text »|PDF »
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