Modeling HIV infection dynamics: The role of recombination in the development of drug resistance

Future HIV Therapy

Volumn 2, Issue 4, 2008, Pages 375-388

  Dixit, Narendra M ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Antiretroviral therapy; Drug resistance; HIV dynamics; Mathematical model; Recombination; Viral evolution

Indexed keywords

ANTIRETROVIRUS AGENT; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; INTEGRASE INHIBITOR; LAMIVUDINE; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; ZIDOVUDINE;

ANTIVIRAL RESISTANCE; CD4+ T LYMPHOCYTE; DRUG TREATMENT FAILURE; EFFECTIVE POPULATION SIZE; EPISTASIS; GENE LINKAGE DISEQUILIBRIUM; GENETIC DRIFT; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MATHEMATICAL MODEL; MIXED INFECTION; MOLECULAR DYNAMICS; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; POINT MUTATION; POPULATION GENETICS; REVIEW; VIRUS GENOME; VIRUS LOAD; VIRUS MUTATION; VIRUS RECOMBINATION; VIRUS STRAIN;

EID: 52349108625     PISSN: 17469600     EISSN: None     Source Type: Journal    
DOI: 10.2217/17469600.2.4.375     Document Type: Review

References (90)

1. Deeks SG: Antiretroviral treatment of HIV-infected adults. Br. Med. J. 332, 1489-1493 (2006).
2. Hammer SM, Saag MS, Schechter M et al.: Treatment for adult HIV infection: 2006 recommendations of the International AIDS Society: USA panel. J. Amer. Med. Assoc. 296, 827-843 (2006).
3. Clavel F, Hance AJ: HIV drug resistance. N. Engl. J. Med. 350, 1023-1035 (2004).
4. Thomson MM, Perez-Alvarez L, Najera R: Molecular epidemiology of HIV-1 genetic forms and its significance for vaccine development and therapy. Lancet Infect. Dis. 2, 461-471 (2002).
5. Simon V, Ho DD, Karim QA: HIV/AIDS epidemiology, pathogenesis, prevention and treatment. Lancet 368, 489-504 (2006).
6. Perno C-F, Moyle G, Tsoukas C, Ratanasuwan W, Gatell J, Schechter M: Overcoming resistance to existing therapies in HIV-infected patients: the role of new antiretroviral drugs. J. Med. Virol. 80, 565-576 (2008).
7. Shet A, Berry L, Mohri H et al.: Tracking the prevalence of transmitted antiretroviral drug-resistant HIV-1: a decade of experience. J. Acq. Immun. Def. Synd. 41, 439-446 (2006).
8. Shankarappa R, Margolick JB, Gange SJ et al.: Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73, 10489-10502 (1999).
9. Hogg RS, Bangsberg DR, Lima VD et al.: Emergence of drug resistance is associated with an increased risk of death among patients first starting HAART. PLoS Med. 3, 1570-1578 (2006).
10. Martinez-Picado J, DePasquale MP, Kartsonis N et al.: Antiretroviral resistance during successful therapy of HIV type 1 infection. Proc. Natl Acad. Sci. USA 97, 10948-10953 (2000).
11. Mansky LM, Temin HM: 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 (1995).
12. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD: HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span and viral generation time. Science 271, 1582-1586 (1996).
13. Kils-Hutten L, Cheynier R, Wain-Hobson S, Meyerhans A: Phylogenetic reconstruction of intrapatient evolution of human immunodeficiency virus type 1: predominance of drift and purifying selection. J. Gen. Virol. 82, 1621-1627 (2001).
14. Shriner D, Shankarappa R, Jensen MA et al.: Influence of random genetic drift on human immunodeficiency virus type I env evolution during chronic infection. Genetics 166, 1155-1164 (2004).
15. Frost SDW, Dumaurier MJ, Wain-Hobson S, Brown AJL: Genetic drift and within-host metapopulation dynamics of HIV-1 infection. Proc. Natl Acad. Sci. USA 98, 6975-6980 (2001).
16. Rouzine IM, Rodrigo A, Coffin JM: Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol. Mol. Biol. Rev. 65, 151-185 (2001).
17. Williamson S, Perry SM, Bustamante CD, Orive ME, Stearns MN, Kelly JK: A statistical characterization of consistent patterns of human immunodeficiency virus evolution within infected patients. Mol. Biol. Evol. 22, 456-468 (2005).
18. Yuste E, Moya A, Lopez-Galindez C: Frequency-dependent selection in human immunodeficiency virus type 1. J. Gen. Virol. 83, 103-106 (2002).
19. Ball CL, Gilchrist MA, Coombs D: Modeling within-host evolution of HIV: mutation, competition and strain replacement. Bull. Math Biol. 69, 2361-2385 (2007).
20. Murray JM, Perelson AS: Human immunodeficiency virus: quast-species and drug resistance. Multiscale Model. Sim. 3, 300-311 (2005).
21. Rong LB, Feng ZL, Perelson AS: Emergence of HIV-1 drug resistance during antiretroviral treatment. Bull. Math. Biol. 69, 2027-2060 (2007).
22. Boerlijst MC, Bonhoeffer S, Nowak MA: viral quasi-species and recombination. Proc. R. Soc. Lond. B. Biol. Sci. 263, 1577-1584 (1996).
23. Otto SP, Lenormand T: Resolving the paradox of sex and recombination. Nat. Rev. Genet. 3, 252-261 (2002).
24. Rice WR: Experimental tests of the adaptive significance of sexual recombination. Nat. Rev. Genet. 3, 241-251 (2002).
25. Bretscher MT, Althaus CL, Muller V, Bonhoeffer S: Recombination in HIV and the evolution of drug resistance: for better or for worse? Bioessays 26, 180-188 (2004).
26. Fraser C: HIV recombination: what is the impact on antiretroviral therapy? J. R. Soc. Interface 2, 489-503 (2005).
27. Temin HM: Sex and recombination in retroviruses. Trends Genet. 7, 71-74 (1991).
28. Blackard JT, Cohen DE, Mayer KH: Human immunodeficiency virus superinfection and recombination: current state of knowledge and potential clinical consequences. Clin. Infect. Dis. 34, 1108-1114 (2002).
29. Galetto R, Negroni M: Mechanistic features of recombination in HIV. AIDS Rev. 7, 92-102 (2005).
30. Moutouh L, Corbeil J, Richman DD: Recombinatton leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proc. Natl Acad. Sci. USA 93, 6106-6111 (1996).
31. Jetzt AE, Yu H, Klarmann GJ, Ron Y, Preston BD, Dougherty JP: High rate of recombination throughout the human immunodeficiency virus type 1 genome. J. Virol. 74, 1234-1240 (2000).
32. Levy DN, Aldrovandi GM, Kutsch O, Shaw GM: Dynamics of HIV-1 recombination in its natural target cells. Proc. Natl Acad. Sci. USA 101, 4204-4209 (2004).
33. Shriner D, Rodrigo AG, Nickle DC, Mullins JI: Pervasive genomic recombination of HIV-1 in vivo. Genetics 167, 1573-1583 (2004).
34. Suryavanshi GW, Dixit NM: Emergence of recombinant forms of HIV: dynamics and scaling. PLoS Comput. Biol. 3, 2003-2010 (2007).
35. Rhodes T, Wargo H, Hu W-S: High rates of human immunodeficiency virus type 1 recombination: near-random segregation of markers one kilobase apart in one round of viral replication. J. Viro1. 77, 11193-11200 (2003).
36. Jung A, Maier R, Vartanian JP et al.: Multiply infected spleen cells in HIV patients. Nature 418, 144-144 (2002).
37. Charpentier C, Nora T, Tenaillon O, Clavel F, Hance AJ: Extensive recombination among human immunodeficiency virus type 1 quasispecies makes an important contribution to viral diversity in individual patients. J. Virol. 80, 2472-2482 (2006).
38. Nora T, Charpentier C, Tenaillon O, Hoede C, Clavel F, Hance AJ: Contribution of recombination to the evolution of human immunodeficiency viruses expressing resistance to antiretroviral treatment. J. Virol. 81, 7620-7628 (2007).
39. Hartl DL, Clark AG: Principles of Population Genetics (4th Edition). Sunderland MA (Ed.). Sinauer Associates, Inc., MA, USA (2007).
40. Kouyos RD, Silander OK, Bonhoeffer S: Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol. Evol. 22, 308-315 (2007).
41. Chen J, Dang Q, Unutmaz D et al.: Mechanisms of nonrandom human immunodeficiency virus type 1 infection and double infection: preference in virus entry is important but is not the sole factor. J. Virol. 79, 4140-4149 (2005).
42. Chen J, Rhodes TD, Hu W-S: Comparison of the genetic recombination rates of human immunodeficiency virus type 1 in macrophages and T cells. J. Virol. 79, 9337-9340 (2005).
43. Dang Q, Chen JB, Unutmaz D et al.: Nonrandom HIV-1 infection and double infection via direct and cell-mediated pathways. Proc. Natl Acad. Sci. USA 101, 632-637 (2004).
44. Rhodes TD, Nlkolaitchik O, Chen JB, Powell D, Hu WS: Genetic recombination of human immunodeficiency virus type 1 in one round of viral replication: effects of genetic distance, target cells, accessory genes and lack of high negative interference in crossover events. J. Virol. 79, 1666-1677 (2005).
45. Mild M, Esbjornsson J, Fenyo EM, Medstrand P: Frequent intrapatient recombination between human immunodeficiency virus type 1 R5 and X4 envelopes: implications for coreceptor switch. J. Virol. 81, 3369-3376 (2007).
46. Nowak MA, May RM: Virus Dynamics: Mathematical Principles of Immunology and Virology. Oxford University Press, New York, USA (2000).
47. Wei XP, Ghosh SK, Taylor ME et al.: viral dynamics in human-immunodeficiency-virus type-1 infection. Nature 373, 117-122 (1995).
48. Perelson AS: Modelling viral and Immune system dynamics. Nat. Rev. Immunol. 2, 28-36 (2002).
49. Perelson AS, Essunger P, Cao YZ et al.: Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387, 188-191 (1997).
50. Bonhoeffer S, May RM, Shaw GM, Nowak MA: virus dynamics and drug therapy. Proc. Natl Acad. Sci. USA 94, 6971-6976 (1997).
51. Ribeiro RM, Bonhoeffer S, Nowak MA: The frequency of resistant mutant virus before antiviral therapy. AIDS 12, 461-465 (1998).
52. Wahl LM, Nowak MA: Adherence and drug resistance: predictions for therapy outcome. Proc. R. Soc. Lond B. Biol. Sci. 267, 835-843 (2000).
53. Wu HL, Huang YX, Acosta EP et al.: Pharmacodynamics of antiretroviral agents in HIV-1-infected patients: using viral dynamic models that incorporate drug susceptibility and adherence. J. Pharmacokinet. Phar. 33, 399-419 (2006).
54. Wu HL, Huang YX, Acosta EP et al.: Modeling long-term HIV dynamics and antiretroviral response: effects of drug potency, pharmacokinetics, adherence and drug resistance. J. Acq. Immun. Def. Synd. 39, 272-283 (2005).
55. Huang YX, Rosenkranz SL, Wu HL: Modeling HIV dynamics and antiviral response with consideration of time-varying drug exposures, adherence and phenotypic sensitivity. Math. Biosci. 184, 165-186 (2003).
56. Kepler TB, Perelson AS: Drug concentration heterogeneity facilitates the evolution of drug resistance. Proc. Natl Acad. Sci. USA 95, 11514-11519 (1998).
57. Dixit NM, Perelson AS: Influence of drug pharmacokinetics on HIV pathogenesis and therapy. In: Deterministic and Stochastic Models on AIDS and HIV with Intervention. Wu H, Tan WY (Eds). World Scientific Press, Singapore, 287-311 (2005).
58. Doyon L, Tremblay S, Bourgon L, Wardrop E, Cordingley MG: Selection and characterization of HIV-1 showing reduced susceptibility to the non-peptidic protease inhibitor tipranavir. Antivir. Res. 68, 27-35 (2005).
59. Eigen M, McCaskill J, Schuster P: Molecular quasi-species. J. Phys. Chem. 92, 6881-6891 (1988).
60. Eigen M, McCaskill J, Schuster P: The molecular quasi-species. Adv. Chem. Phys. 75, 149-263 (1989).
61. Bonhoeffer S, Chappey C, Parkin NT, Whitcomb JM, Petropoulos CJ: Evidence for positive epistasis in HIV-1. Science 306, 1547-1550 (2004).
62. Althaus CL, Bonhoeffer S: Stochastic interplay between mutation and recombination during the acquisition of drug resistance mutations in human immunodeficiency virus type 1. J. Virol. 79, 13572-13578 (2005).
63. Leontiev W, Maury WJ, Hadany L: Drug induced superinfection in HIV and the evolution of drug resistance. Infect. Genet. Evol. 8, 40-50 (2008).
64. Chen BK, Gandhi RT, Baltimore D: CD4 down-modulation during infection of human T cells with human immunodeficiency virus type 1 involves independent activities of Vpu, Env and Nef. J. Viro1. 70, 6044-6053 (1996).
65. Lama J: The physiological relevance of CD4 receptor down-modulation during HIV infection. Curr. HIV Res. 1, 167-184 (2003).
66. Piguet V, Gu F, Foti M et al.: Nef-induced CD4 degradation: a diacidic-based motif in Nef functions as a lysosomal targeting signal through the binding of β-COP in endosomes. Cell 97, 63-73 (1999).
67. Dixit NM, Perelson AS: HIV dynamics with multiple infections of target cells. Proc. Natl Acad. Sci. USA 102, 8198-8203 (2005).
68. Bocharov G, Ford NJ, Edwards J, Breinig T, Wain-Hobson S, Meyerhans A: A genetic algorithm approach to simulating human immunodeficiency virus evolution reveals the strong impact of multiply infected cells and recombinatton. J. Gen. Virol. 86, 3109-3118 (2005).
69. Gilchrist MA, Coombs D: Evolution of virulence: interdependence, constraints and selection using nested models. Theor. Popul. Biol. 69, 145-153 (2006).
70. Ribeiro RM, Bonhoeffer S: Production of resistant HIV mutants during antiretroviral therapy. Proc. Natl Acad. Sci. USA 97, 7681-7686 (2000).
71. Gheorghiu-Svirschevski S, Rouzine IM, Coffin JM: Increasing sequence correlation limits the efficiency of recombination in a multisite evolution model. Mol. Biol. Evol. 24, 574-586 (2007).
72. Rouzine IM, Coffin JM: Evolution of human immunodeficiency virus under selection and weak recombination. Genetics 170, 7-18 (2005).
73. Vijay NN, Vasantika, Ajmani R, Perelson AS, Dixit NM: Recombination increases HIV fitness, but not necessarily diversity. J. Gen. Virol. 89, 1467-1477 (2008).
74. Kouyos RD, Althaus CL, Bonhoeffer S: Stochastic or deterministic: what is the effective population size of HIV-1? Trends Microbiol. 14, 507-511 (2006).
75. Achaz G, Palmer S, Kearney M et al.: A robust measure of HIV-1 population turnover within chronically infected individuals. Mol. Biol. Evol. 21, 1902-1912 (2004).
76. Brown AJL: Analysis of HIV-1 env gene sequences reveals evidence for a low effective number in the viral population. Proc. Natl Acad. Sci. USA 94, 1862-1865 (1997).
77. Nijhuis M, Boucher CAB, Schipper P, Leitner T, Schuurman R, Albert J: Stochastic processes strongly influence HIV-1 evolution during suboptimal protease-inhibitor therapy. Proc. Natl Acad. Sci. USA 95, 14441-14446 (1998).
78. Rodrigo AG, Shpaer EG, Delwart EL et al.: Coalescent estimates of HIV-1 generation time in vivo. Proc. Natl Acad. Sci. USA 96, 2187-2191 (1999).
79. Seo T-K, Thorne JL, Hasegawa M, Kishino H: Estimation of effective population size of HIV-1 within a host: a pseudomaximum-likelihood approach. Genetics 160, 1283-1293 (2002).
80. Rouzine IM, Coffin JM: Linkage disequilibrium test implies a large effective population number for HIV in vivo. Proc. Natl Acad. Sci. USA 96, 10758-10763 (1999).
81. Markham RB, Wang WC, Weisstein AE et al.: Patterns of HIV-1 evolution in individuals with differing rares of CD4 T-cell decline. Proc. Natl Acad. Sci. USA 95, 12568-12573 (1998).
82. Carvajal-Rodriguez A, Crandall KA, Posada D: Recombination favors the evolution of drug resistance in HIV-1 during antiretroviral therapy. Infect. Genet. Evol. 7, 476-483 (2007).
83. Froissart R, Wilke CO, Montville R, Remold SK, Chao L, Turner PE: Co-infection weakens selection against epistatic mutations in RNA viruses. Genetics 168, 9-19 (2004).
84. Christiansen FB, Otto SP, Bergman A, Feldman MW; Waiting with and without recombination: the time to production of a double mutant. Theor. Popul. Biol. 53, 199-215 (1998).
85. Anderson RM, May RM: Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford, UK (1992).
86. Ribeiro RM, Dixit NM, Perelson AS: Modelling the in vivo growth rate of HIV: implications for vaccination. In: Multidisciplinary Approaches to Theory in Medicine. Paton R, McNamara LA (Eds). Elsevier, Amsterdam, The Netherlands, 231-246 (2006).
87. Ewens WJ: Mathematical Population Genetics (2nd Edition). Springer, New York, USA (2004).
88. Eshel I, Feldman MW: On the evolutionary effect of recombination. Theor. Popul. Biol. 1, 88-100 (1970).
89. Hill WG, Robertson A: The effect of linkage on limits to artificial selection. Genet. Res. 8, 269-294 (1966).
90. Kouyos RD, Otto SP, Bonhoeffer S: Effect of varying epistasis on the evolution of recombination. Genetics 173, 589-597 (2006).