Impaired immune evasion in HIV through intracellular delays and multiple infection of cells

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1740, 2012, Pages 3003-3010

  Althaus, Christian L ^a,b   De Boer, Rob J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Cytotoxic T lymphocytes; HIV; Immune escape; Intracellular delay; Mathematical model; Multiple infection

Indexed keywords

CLONE; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE SYSTEM; IMMUNITY; LIFE CYCLE; MUTATION; NUMERICAL MODEL; PUBLIC HEALTH;

EID: 84863088953     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0328     Document Type: Article

References (54)

1. Phillips, R. et al. 1991 Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354, 453-459. (doi:10.1038/354453a0)
2. Goulder, P. & Watkins, D. 2004 HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4, 630-640. (doi:10.1038/nri1417)
3. Kawashima, Y. et al. 2009 Adaptation of HIV-1 to human leukocyte antigen class I. Nature 458, 641-645. (doi:10. 1038/nature07746)
4. Goonetilleke, N. et al. 2009 The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J. Exp. Med. 206, 1253-1272. (doi:10.1084/jem.20090365)
5. Fischer, W. et al. 2010 Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS ONE 5, e12303. (doi:10. 1371/journal.pone.0012303)
6. Ganusov, V. V., Goonetilleke, N., Liu, M. K. P., Ferrari, G., Shaw, G. M., McMichael, A. J., Borrow, P., Korber, B. T. & Perelson, A. S. 2011 Fitness costs and diversity of the cytotoxic T lymphocyte (CTL) response determine the rate of CTL escape during acute and chronic phases of HIV infection. J. Virol. 85, 10 518-10 528. (doi:10.1128/JVI.00655-11)
7. Asquith, B., Edwards, C., Lipsitch, M. & McLean, A. 2006 Inefficient cytotoxic T lymphocyte-mediated killing of HIV-1-infected cells in vivo. PLoS Biol. 4, e90. (doi:10. 1371/journal.pbio.0040090)
8. Ganusov, V. & De Boer, R. 2006 Estimating costs and benefits of CTL escape mutations in SIV/HIV infection. PLoS Comput. Biol. 2, e24. (doi:10.1371/journal.pcbi. 0020024)
9. Althaus, C. L. & De Boer, R. J. 2008 Dynamics of immune escape during HIV/SIV infection. PLoS Comput. Biol. 4, e1000103. (doi:10.1371/journal.pcbi. 1000103)
10. Kadolsky, U. D. & Asquith, B. 2010 Quantifying the impact of human immunodeficiency virus-1 escape from cytotoxic T-lymphocytes. PLoS Comput. Biol. 6, e1000981. (doi:10.1371/journal.pcbi.1000981)
11. Jung, A., Maier, R., Vartanian, J., Bocharov, G., Jung, V., Fischer, U., Meese, E., Wain-Hobson, S. & Meyerhans, A. 2002 Multiply infected spleen cells in HIV patients. Nature 418, 144. (doi:10.1038/418144a)
12. Bretscher, M. T., Althaus, C. L., Muller, V. & Bonhoeffer, S. 2004 Recombination in HIV and the evolution of drug resistance: for better or for worse? Bioessays 26, 180-188. (doi:10.1002/bies.10386)
13. Fraser, C. 2005 HIV recombination: what is the impact on antiretroviral therapy? J. R. Soc. Interface 2, 489-503. (doi:10.1098/rsif.2005.0064)
14. Althaus, C. L. & Bonhoeffer, S. 2005 Stochastic interplay between mutation and recombination during the acquisition of drug resistance mutations in human immunodeficiency virus type 1. J. Virol. 79, 13 572-13 578. (doi:10.1128/JVI.79.21.13572-13578.2005)
15. Kouyos, R. D., Fouchet, D. & Bonhoeffer, S. 2009 Recombination and drug resistance in HIV: population dynamics and stochasticity. Epidemics 1, 58-69. (doi:10.1016/j.epidem.2008.11.001)
16. Dixit, N. & Perelson, A. 2004 Multiplicity of human immunodeficiency virus infections in lymphoid tissue. J. Virol. 78, 8942-8945. (doi:10.1128/JVI.78.16.8942-945.2004)
17. Dixit, N. M. & Perelson, A. S. 2005 HIV dynamics with multiple infections of target cells. Proc. Natl Acad. Sci. USA 102, 8198-8203. (doi:10.1073/pnas.040749 8102)
18. Wodarz, D. & Levy, D. N. 2011 Effect of different modes of viral spread on the dynamics of multiply infected cells in human immunodeficiency virus infection. J. R. Soc. Interface 8, 289-300. (doi:10.1098/rsif.2010.0266)
19. Josefsson, L. et al. 2011 Majority of CD{thorn}4 T cells from peripheral blood of HIV-1-infected individuals contain only one HIV DNA molecule. Proc. Natl Acad. Sci. USA 108, 11 199-11 204. (doi:10.1073/pnas.1107729108)
20. Neher, R. A. & Leitner, T. 2010 Recombination rate and selection strength in HIV intra-patient evolution. PLoS Comput. Biol. 6, e1000660. (doi:10.1371/journal.pcbi. 1000660)
21. Batorsky, R., Kearney, M. F., Palmer, S. E., Maldarelli, F., Rouzine, I. M. & Coffin, J. M. 2011 Estimate of effective recombination rate and average selection coefficient for HIV in chronic infection. Proc. Natl Acad. Sci. USA 108, 5661-5666. (doi:10.1073/pnas.1102036108)
22. Wodarz, D. & Levy, D. N. 2009 Multiple HIV-1 infection of cells and the evolutionary dynamics of cytotoxic T lymphocyte escape mutants. Evolution 63, 2326-2339. (doi:10.1111/j.1558-5646.2009.00727.x)
23. Dixit, N. M., Markowitz, M., Ho, D. D. & Perelson, A. S. 2004 Estimates of intracellular delay and average drug efficacy from viral load data of HIV-infected individuals under antiretroviral therapy. Antivir. Ther. 9, 237-246.
24. Althaus, C. L., De Vos, A. S. & De Boer, R. J. 2009 Reassessing the human immunodeficiency virus type 1 life cycle through age-structured modeling: life span of infected cells, viral generation time, and basic reproductive number, R0. J. Virol. 83, 7659-7667. (doi:10. 1128/JVI.01799-08)
25. Nowak, M. & May, R. 2000 Virus dynamics: mathematical principles of immunology and virology. Oxford, UK: Oxford University Press.
26. Perelson, A. 2002 Modelling viral and immune system dynamics. Nat. Rev. Immunol. 2, 28-36. (doi:10.1038/nri700)
27. Haase, A. et al. 1996 Quantitative image analysis of HIV-1 infection in lymphoid tissue. Science 274, 985-989. (doi:10.1126/science.274.5289.985)
28. Kouyos, R., Althaus, C. & Bonhoeffer, S. 2006 Stochastic or deterministic: what is the effective population size of HIV-1? Trends Microbiol. 14, 507-511. (doi:10.1016/j.tim.2006.10.001)
29. Mattapallil, J., Douek, D., Hill, B., Nishimura, Y., Martin, M. & Roederer, M. 2005 Massive infection and loss of memory CD4{thorn} T cells in multiple tissues during acute SIV infection. Nature 434, 1093-1097. (doi:10.1038/nature03501)
30. Althaus, C. L. & De Boer, R. J. 2010 Intracellular transactivation of HIV can account for the decelerating decay of virus load during drug therapy. Mol. Syst. Biol. 6, 348. (doi:10.1038/msb.2010.4)
31. De Boer, R. J., Ribeiro, R. M. & Perelson, A. S. 2010 Current estimates for HIV-1 production imply rapid viral clearance in lymphoid tissues. PLoS Comput. Biol. 6, e1000906. (doi:10.1371/journal.pcbi.1000906)
32. Ramratnam, B. et al. 1999 Rapid production and clearance of HIV-1 and hepatitis C virus assessed by large volume plasma apheresis. Lancet 354, 1782-1785. (doi:10.1016/S0140-6736(99)02035-8)
33. Mansky, L. & Temin, H. 1995 Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J. Virol. 69, 5087-5094.
34. De Boer, R. 2007 Understanding the failure of CD8{thorn} T-cell vaccination against simian/human immunodeficiency virus. J. Virol. 81, 2838-2848. (doi:10.1128/JVI. 01914-06)
35. Allee, W. C. 1949 Principles of animal ecology. Philadelphia, PA: Saunders Co.
36. Courchamp, F., Clutton-Brock, T. & Grenfell, B. 1999 Inverse density dependence and the Allee effect. Trends Ecol. Evol. 14, 405-410. (doi:10.1016/S0169-5347(99) 01683-3)
37. van Baalen, C., Guillon, C., van Baalen, M., Verschuren, E., Boers, P., Osterhaus, A. & Gruters, R. 2002 Impact of antigen expression kinetics on the effectiveness of HIVspecific cytotoxic T lymphocytes. Eur. J. Immunol. 32, 2644-2652. (doi:10.1002/1521-4141(200209)32:9,26 44::AID-IMMU2644.3.0.CO;2-R)
38. Sacha, J. et al. 2007 Gag-specific CD8{thorn} T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178, 2746-2754.
39. Sacha, J. B et al. 2007 Pol-specific CD8{thorn} T cells recognize simian immunodeficiency virus-infected cells prior to Nef-mediated major histocompatibility complex class I downregulation. J. Virol. 81, 11 703-11 712. (doi:10. 1128/JVI.00926-07)
40. Sacha, J. B., Buechler, M. B., Newman, L. P., Reed, J., Wallace, L. T., Loffredo, J. T., Wilson, N. A. & Watkins, D. I. 2010 Simian immunodeficiency virus-specific CD8{thorn} T cells recognize Vpr-and Rev-derived epitopes early after infection. J. Virol. 84, 10 907-10 912. (doi:10.1128/JVI.01357-10)
41. Wick, W. D., Gilbert, P. B. & Yang, O. O. 2009 Predicting the impact of blocking human immunodeficiency virus type 1 Nef in vivo. J. Virol. 83, 2349-2356. (doi:10. 1128/JVI.00821-08)
42. Klatt, N. R et al. 2010 CD8{thorn} lymphocytes control viral replication in SIVmac239-infected Rhesus macaques without decreasing the lifespan of productively infected cells. PLoS Pathog. 6, e1000747. (doi:10.1371/journal.ppat. 1000747)
43. Wong, J. K et al. 2010 In vivo CD8{thorn} T-cell suppression of SIV viremia is not mediated by CTL clearance of productively infected cells. PLoS Pathog. 6, e1000748. (doi:10.1371/journal.ppat.1000748)
44. Althaus, C. L. & De Boer, R. J. 2011 Implications of CTL-mediated killing of HIV-infected cells during the non-productive stage of infection. PLoS ONE 6, e16468. (doi:10.1371/journal.pone.0016468)
45. Mandl, J. N., Regoes, R. R., Garber, D. A. & Feinberg, M. B. 2007 Estimating the effectiveness of simian immunodeficiency virus-specific CD8{thorn} T cells from the dynamics of viral immune escape. J. Virol. 81, 11 982-11 991. (doi:10.1128/JVI.00946-07)
46. Davenport, M. P. & Petravic, J. 2010 CD8{thorn} T cell control of HIV-A known unknown. PLoS Pathog. 6, e1000728. (doi:10.1371/journal.ppat.1000728)
47. Balamurali, M., Petravic, J., Loh, L., Alcantara, S., Kent, S. J. & Davenport, M. P. 2010 Does cytolysis by CD8{thorn} T cells drive immune escape in HIV infection? J. Immunol. 185, 5093-5101. (doi:10.4049/jimmunol.1002204)
48. Elemans, M., Seich Al Basatena, N.-K., Klatt, N. R., Gkekas, C., Silvestri, G. & Asquith, B. 2011 Why don't CD8{thorn} T cells reduce the lifespan of SIV-infected cells in vivo? PLoS Comput. Biol. 7, e1002200. (doi:10.1371/journal.pcbi.1002200)
49. Ganusov, V. V. & De Boer, R. J. 2007 Do most lymphocytes in humans really reside in the gut? Trends Immunol. 28, 514-518. (doi:10.1016/j.it.2007.08.009)
50. Delassus, S., Cheynier, R. & Wain-Hobson, S. 1992 Nonhomogeneous distribution of human immunodeficiency virus type 1 proviruses in the spleen. J. Virol. 66, 5642-5645.
51. Frost, S. D., Dumaurier, M. J., Wain-Hobson, S. & Brown, A. J. 2001 Genetic drift and within-host metapopulation dynamics of HIV-1 infection. Proc. Natl Acad. Sci. USA 98, 6975-6980. (doi:10.1073/pnas. 131056998)
52. Funk, G. A., Jansen, V. A.A., Bonhoeffer, S. &Killingback, T. 2005 Spatialmodels of virus-immune dynamics. J Theor. Biol. 233, 221-236. (doi:10.1016/j.jtbi.2004.10.004)
53. Sato, H., Orenstein, J., Dimitrov, D. & Martin, M. 1992 Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles. Virology 186, 712-724. (doi:10.1016/0042-6822(92)90038-Q)
54. Sykulev, Y., Joo, M., Vturina, I., Tsomides, T. J. & Eisen, H. N. 1996 Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4, 565-571. (doi:10.1016/S1074-7613(00)80483-5)