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Journal of Virology, April 2006, p. 3617-3623, Vol. 80, No. 7
0022-538X/06/$08.00+0     doi:10.1128/JVI.80.7.3617-3623.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Fitness Cost of Escape Mutations in p24 Gag in Association with Control of Human Immunodeficiency Virus Type 1

Javier Martinez-Picado,1 Julia G. Prado,1 Elizabeth E. Fry,2 Katja Pfafferott,3 Alasdair Leslie,3 Senica Chetty,4 Christina Thobakgale,4 Isobel Honeyborne,3 Hayley Crawford,3 Philippa Matthews,3 Tilly Pillay,3 Christine Rousseau,5 James I. Mullins,5 Christian Brander,6 Bruce D. Walker,6 David I. Stuart,2 Photini Kiepiela,4 and Philip Goulder3,6*

irsiCaixa Foundation, University Hospital "Germans Trias i Pujol," Barcelona, Spain,1 Division of Structural Biology, Henry Wellcome Building for Genomic Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7BN, United Kingdom,2 Department of Paediatrics, Nuffield Department of Medicine, Peter Medawar Building for Pathogen Research, South Parks Road, Oxford OX1 3SY, United Kingdom,3 HIV Pathogenesis Programme, The Doris Duke Medical Research Institute, University of Natal, Durban, South Africa,4 Department of Microbiology, University of Washington, Seattle, Washington 98195,5 Partners AIDS Research Center, Massachusetts General Hospital, 13th Street, Building 149, Charlestown, Boston, Massachusetts 021296

Received 15 October 2005/ Accepted 9 December 2005

Mutational escape by human immunodeficiency virus (HIV) from cytotoxic T-lymphocyte (CTL) recognition is a major challenge for vaccine design. However, recent studies suggest that CTL escape may carry a sufficient cost to viral replicative capacity to facilitate subsequent immune control of a now attenuated virus. In order to examine how limitations can be imposed on viral escape, the epitope TSTLQEQIGW (TW10 [Gag residues 240 to 249]), presented by two HLA alleles associated with effective control of HIV, HLA-B*57 and -B*5801, was investigated. The in vitro experiments described here demonstrate that the dominant TW10 escape mutation, T242N, reduces viral replicative capacity. Structural analysis reveals that T242 plays a critical role in defining the start point and in stabilizing helix 6 within p24 Gag, ensuring that escape occurs at a significant cost. A very similar role is played by Thr-180, which is also an escape residue, but within a second p24 Gag epitope associated with immune control. Analysis of HIV type 1 gag in 206 B*57/5801-positive subjects reveals three principle alternative TW10-associated variants, and each is strongly linked to concomitant additional variants within p24 Gag, suggesting that functional constraints operate against their occurrence alone. The extreme conservation of p24 Gag and the predictable nature of escape variation resulting from these tight functional constraints indicate that p24 Gag may be a critical immunogen in vaccine design and suggest novel vaccination strategies to limit viral escape options from such epitopes.

* Corresponding author. Mailing address: Peter Medawar Building, South Parks Rd., Oxford OX1 3SY, United Kingdom. Phone: 44-1865-281884. Fax: 44-1865-281236. E-mail: philip.goulder{at}ndm.ox.ac.uk.

Journal of Virology, April 2006, p. 3617-3623, Vol. 80, No. 7
0022-538X/06/$08.00+0     doi:10.1128/JVI.80.7.3617-3623.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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