Clustered Mutations in HIV-1 gag Are Consistently Required for Escape from HLA-B27-restricted Cytotoxic T Lymphocyte Responses

doi:10.1084/jem.193.3.375

Published online 5 February 2001.

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© The Rockefeller University Press, 0022-1007/2001/2/375/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 3, February 5, 2001 375-386

Original Article

Clustered Mutations in HIV-1 gag Are Consistently Required for Escape from HLA-B27–restricted Cytotoxic T Lymphocyte Responses

Anthony D. Kelleher^a, Chad Long^b, Edward C. Holmes^c, Rachel L. Allen^a, Jamie Wilson^a, Christopher Conlon^b, Cassy Workman^d, Sunil Shaunak^e, Kara Olson^b, Philip Goulder^b,f, Christian Brander^f, Graham Ogg^a, John S. Sullivan^g, Wayne Dyer^g, Ian Jones^h, Andrew J. McMichael^a, Sarah Rowland-Jones^a, and Rodney E. Phillips^b
^a Medical Research Council Human Immunology Unit, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DS, United Kingdom
^b Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, United Kingdom
^c Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom
^d AIDS Research Initiative, Darlinghurst, New South Wales 2010, Australia
^e Department of Infectious Diseases, Imperial College School of Medicine, Hammersmith Hospital, London W12 ONN, United Kingdom
^f Partners AIDS Research Center, Massachusetts General Hospital, Charlestown, Massachusetts 02129
^g Australian Red Cross Blood Service, Sydney 2000, Australia
^h Virology, School of Animal and Microbial Sciences, University of Reading, Whiteknights, Reading RG6 6AH, United Kingdom

Correspondence to: Anthony D. Kelleher, National Centre in HIV Epidemiology and Clinical Research, University of New South Wales, 376 Victoria St., Sydney, NSW 2010, Australia. Tel:61-293-324-646 Fax:61-293-321-837 E-mail:kelleher{at}worf.molbiol.ox.ac.uk.

The immune response to HIV-1 in patients who carry human histocompatibilityleukocyte antigen (HLA)-B27 is characterized by an immunodominantresponse to an epitope in p24 gag (amino acids 263–272,KRWIILGLNK). Substitution of lysine (K) or glycine (G) for arginine(R) at HIV-1 gag residue 264 (R264K and R264G) results in epitopesthat bind to HLA-B27 poorly_. We have detected a R264K mutationin four patients carrying HLA-B27. In three of these patientsthe mutation occurred late, coinciding with disease progression.In another it occurred within 1 yr of infection and was associatedwith a virus of syncytium-inducing phenotype. In each case,R264K was tightly associated with a leucine to methionine changeat residue 268. After the loss of the cytotoxic T lymphocyte(CTL) response to this epitope and in the presence of high viralload, reversion to wild-type sequence was observed. In a fifthpatient, a R264G mutation was detected when HIV-1 disease progressed.Its occurrence was associated with a glutamic acid to asparticacid mutation at residue 260. Phylogenetic analyses indicatedthat these substitutions emerged under natural selection ratherthan by genetic drift or linkage. Outgrowth of CTL escape virusesrequired high viral loads and additional, possibly compensatory,mutations in the gag protein.

Key Words: human immunodeficiency virus, immune escape, selection, CD8⁺T lymphocyte, phylogenetic analysis

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Novitsky, V., Cao, H., Rybak, N., Gilbert, P., McLane, M. F., Gaolekwe, S., Peter, T., Thior, I., Ndung'u, T., Marlink, R., Lee, T. H., Essex, M. (2002). Magnitude and Frequency of Cytotoxic T-Lymphocyte Responses: Identification of Immunodominant Regions of Human Immunodeficiency Virus Type 1 Subtype C. J. Virol. 76: 10155-10168 [Abstract] [Full Text]
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