Drug-class specific impact of antivirals on the reproductive capacity of HIV

PLoS Computational Biology

Volumn 6, Issue 3, 2010, Pages

  von Kleist, Max ^a,b   Menz, Stephan ^b   Huisinga, Wilhelm ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRALS; CLINICAL OUTCOME; DRUG DEVELOPMENT; DRUG DISCOVERY PROCESS; DRUG EFFICACY; HALF LIVES; IN-VITRO; IN-VIVO; REPRODUCTIVE CAPACITY; VIRAL REPLICATION;

ASSAYS;

ANTIVIRUS AGENT; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; MATURATION INHIBITOR; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; UNCLASSIFIED DRUG; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT;

ANTIVIRAL RESISTANCE; ARTICLE; DRUG CLASSIFICATION; DRUG EFFECT; DRUG HALF LIFE; DRUG MECHANISM; DRUG SPECIFICITY; HUMAN IMMUNODEFICIENCY VIRUS; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; QUANTITATIVE ANALYSIS; SIMULATION; TARGET CELL; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS STRAIN; BIOLOGICAL MODEL; COMPUTER SIMULATION; PHYSIOLOGY;

ANTI-HIV AGENTS; COMPUTER SIMULATION; HIV; MODELS, BIOLOGICAL; VIRUS REPLICATION;

EID: 77950829090     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000720     Document Type: Article

References (76)

1. Hammer SM, Squires KE, Hughes MD, Grimes JM, Demeter LM, et al. (1997) A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. AIDS clinical trials group 320 study team. N Engl J Med 337: 725-733.
2. Hirsch M, Steigbigel R, Staszewski S, Mellors J, Scerpella E, et al. (1999) A randomized, controlled trial of indinavir, zidovudine, and lamivudine in adults with advanced human immunodeficiency virus type 1 infection and prior antiretroviral therapy. J Infect Dis 180: 659-665.
3. Richman DD (2001) HIV chemotherapy. Nature 410: 995-1001.
4. Kulkosky J, Pomerantz RJ (2002) Approaching eradication of highly active antiretroviral therapy-persistent human immunodeficiency virus type 1 reservoirs with immune activation therapy. Clin Infect Dis 35: 1520-1526.
5. Kulkosky J, Nunnari G, Otero M, Calarota S, Dornadula G, et al. (2002) Intensification and stimulation therapy for human immunodeficiency virus type 1 reservoirs in infected persons receiving virally suppressive highly active antiretroviral therapy. J Infect Dis 186: 1403-1411.
6. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, et al. (1997) Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278: 1295-1300.
7. Wong JK, Hezareh M, Günthard HF, Havlir DV, Ignacio CC, et al. (1997) Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278: 1291-1295.
8. Current HIV treatment guidelines: (http://www.aidsinfo.nih.gov/guidelines/). Technical report, National Institute of Health (accessed 15-Feb-2010).
9. Langford SE, Ananworanich J, Cooper DA (2007) Predictors of disease progression in HIV infection: a review. AIDS Res Ther 4: 11.
10. Markowitz M, Morales-Ramirez JO, Nguyen BY, Kovacs CM, Steigbigel RT, et al. (2006) Antiretroviral activity, pharmacokinetics, and tolerability of mk-0518, a novel inhibitor of HIV-1 integrase, dosed as monotherapy for 10 days in treatment-naive HIV-1-infected individuals. J Acquir Immune Defic Syndr 43: 509-515.
11. Fätkenheuer G, Pozniak AL, Johnson MA, Plettenberg A, Staszewski S, et al. (2005) Efficacy of short-term monotherapy with maraviroc, a new CCR5 antagonist, in patients infected with HIV-1. Nat Med 11: 1170-1172.
12. Louie M, Hogan C, Mascio MD, Hurley A, Simon V, et al. (2003) Determining the relative efficacy of highly active antiretroviral therapy. J Infect Dis 187: 896-900.
13. Zhang H, Zhou Y, Alcock C, Kiefer T, Monie D, et al. (2004) Novel single-cell-level phenotypic assay for residual drug susceptibility and reduced replication capacity of drug-resistant human immunodeficiency virus type 1. J Virol 78: 1718-1729.
14. Shen L, Peterson S, Sedaghat AR, McMahon MA, Callender M, et al. (2008) Dose-response curve slope sets class-specific limits on inhibitory potential of anti-HIV drugs. Nat Med 14: 762-766.
15. Petropoulos CJ, Parkin NT, Limoli KL, Lie YS, Wrin T, et al. (2000) A novel phenotypic drug susceptibility assay for human immunodeficiency virus type 1. Antimicrob Agents Chemother 44: 920-928.
16. Hachiya A, Aizawa-Matsuoka S, Tanaka M, Takahashi Y, Ida S, et al. (2001) Rapid and simple phenotypic assay for drug susceptibility of human immunodeficiency virus type 1 using CCR5-expressing HeLa/CD4(+) cell clone 1-10 (magic-5). Antimicrob Agents Chemother 45: 495-501.
17. Dando TM, Perry CM (2003) Enfuvirtide. Drugs 63: 2755-66.
18. Carter NJ, Keating GM (2007) Maraviroc. Drugs 67: 2277-88.
19. Croxtall JD, Lyseng-Williamson KA, Perry CM (2008) Raltegravir. Drugs 68: 131-138.
20. Investigational drugs: (http://www.aidsinfo.nih.gov/). Technical report, National Institute of Health (accessed 15-Feb-2010).
21. Murray JM, Emery S, Kelleher AD, Law M, Chen J, et al. (2007) Antiretroviral therapy with the integrase inhibitor raltegravir alters decay kinetics of HIV, significantly reducing the second phase. AIDS 21: 2315-2321.
22. Grinsztejn B, Nguyen BY, Katlama C, Gatell JM, Lazzarin A, et al. (2007) Safety and efficacy of the HIV-1 integrase inhibitor raltegravir (mk-0518) in treatment-experienced patients with multidrug-resistant virus: a phase II randomised controlled trial. Lancet 369: 1261-1269.
23. Markowitz M, Nguyen BY, Gotuzzo E, Mendo F, Ratanasuwan W, et al. (2007) Rapid and durable antiretroviral effect of the HIV-1 integrase inhibitor raltegravir as part of combination therapy in treatment-naive patients with HIV-1 infection: results of a 48-week controlled study. J Acquir Immune Defic Syndr 46: 125-133.
24. Steigbigel RT, Cooper DA, Kumar PN, Eron JE, Schechter M, et al. (2008) Raltegravir with optimized background therapy for resistant HIV-1 infection. N Engl J Med 359: 339-354.
25. Dayam R, Al-Mawsawi LQ, Neamati N (2007) HIV-1 integrase inhibitors: an emerging clinical reality. Drugs R D 8: 155-168.
26. DeJesus E, Berger D, Markowitz M, Cohen C, Hawkins T, et al. (2006) Antiviral activity, pharmacokinetics, and dose response of the HIV-1 integrase inhibitor gs-9137 (jtk-303) in treatment-naive and treatment-experienced patients. J Acquir Immune Defic Syndr 43: 1-5.
27. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD (1996) HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271: 1582-1586.
28. Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, et al. (1997) Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387: 188-191.
29. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, et al. (1995) Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373: 123-126.
30. Bonhoeffer S, May RM, Shaw GM, Nowak MA (1997) Virus dynamics and drug therapy. Proc Natl Acad Sci U S A 94: 6971-6976.
31. Nowak MA, Bangham CR (1996) Population dynamics of immune responses to persistent viruses. Science 272: 74-79.
32. Sedaghat AR, Dinoso JB, Shen L, Wilke CO, Siliciano RF (2008) Decay dynamics of HIV-1 depend on the inhibited stages of the viral life cycle. Proc Natl Acad Sci U S A 105: 4832-4837.
33. Sedaghat AR, Siliciano RF, Wilke CO (2009) Constraints on the dominant mechanism for HIV viral dynamics in patients on raltegravir. Antivir Ther 14: 263-271.
34. Pettit SC, Lindquist JN, Kaplan AH, Swanstrom R (2005) Processing sites in the human immunodeficiency virus type 1 (HIV-1) Gag-Pro-Pol precursor are cleaved by the viral protease at different rates. Retrovirology 2: 66.
35. Wiegers K, Rutter G, Kottler H, Tessmer U, Hohenberg H, et al. (1998) Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J Virol 72: 2846-2854.
36. Ross J (1995) mRNA stability in mammalian cells. Microbiol Rev 59: 423-450.
37. Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136: 763-776.
38. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, et al. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 99-103.
39. Rosario MC, Poland B, Sullivan J, Westby M, van der Ryst E (2006) A pharmacokinetic-pharmacodynamic model to optimize the phase IIa development program of maraviroc. J Acquir Immune Defic Syndr 42: 183-191.
40. Jacqmin P, McFadyen L, Wade JR (2008) A receptor theory-based semimechanistic PD model for the CCR5 noncompetitive antagonist maraviroc. Br J Clin Pharmacol 65: Suppl 195-106.
41. von Kleist M, Huisinga W (2009) Pharmacokinetic-pharmacodynamic relationship of NRTIs and its connection to viral escape: an example based on zidovudine. Eur J Pharm Sci 36: 532-543.
42. Hazuda DJ, Felock P, Witmer M, Wolfe A, Stillmock K, et al. (2000) Inhibitors of strand transfer that prevent integration and inhibit HIV-1 replication in cells. Science 287: 646-650.
43. Neamati N, Hong H, Owen JM, Sunder S, Winslow HE, et al. (1998) Salicylhydrazine-containing inhibitors of HIV-1 integrase: implication for a selective chelation in the integrase active site. J Med Chem 41: 3202-3209.
44. Grobler JA, Stillmock K, Hu B, Witmer M, Felock P, et al. (2002) Diketo acid inhibitor mechanism and HIV-1 integrase: implications for metal binding in the active site of phosphotransferase enzymes. Proc Natl Acad Sci U S A 99: 6661-6666.
45. Marchand C, Johnson AA, Karki RG, Pais GCG, Zhang X, et al. (2003) Metal-dependent inhibition of HIV-1 integrase by beta-diketo acids and resistance of the soluble double-mutant (f185k/c280s). Mol Pharmacol 64: 600-609.
46. Salzwedel K, Martin DE, Sakalian M (2007) Maturation inhibitors: a new therapeutic class targets the virus structure. AIDS Rev 9: 162-172.
47. Kräusslich HG, Fäcke M, Heuser AM, Konvalinka J, Zentgraf H (1995) The spacer peptide between human immunodeficiency virus capsid and nucleocapsid proteins is essential for ordered assembly and viral infectivity. J Virol 69: 3407-3419.
48. Pettit SC, Moody MD, Wehbie RS, Kaplan AH, Nantermet PV, et al. (1994) The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J Virol 68: 8017-8027.
49. Li F, Goila-Gaur R, Salzwedel K, Kilgore NR, Reddick M, et al. (2003) PA-457: a potent HIV inhibitor that disrupts core condensation by targeting a late step in gag processing. Proc Natl Acad Sci U S A 100: 13555-13560.
50. Mansky LM, Temin HM (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.
51. Alfonsi A, Cancès E, Turinici G, Ventura B, Huisinga W (2005) Exact simulation of hybrid stochastic and deterministic models for biochemical systems. ESAIM Proc 14: 1-23.
52. Heesterbeek JAP (2002) A brief history of R0 and a recipe for its calculation. Acta Biotheor 50: 189-204.
53. Heffernan JM, Smith RJ, Wahl LM (2005) Perspectives on the basic reproductive ratio. J R Soc Interface 2: 281-293.
54. Ramratnam B, Bonhoeffer S, Binley J, Hurley A, Zhang L, et al. (1999) Rapid production and clearance of HIV-1 and hepatitis C virus assessed by large volume plasma apheresis. Lancet 354: 1782-1785.
55. Nijhuis M, Schuurman R, de Jong D, Erickson J, Gustchina E, et al. (1999) Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy. AIDS 13: 2349-2359.
56. Havlir DV, Eastman S, Gamst A, Richman DD (1996) Nevirapine-resistant human immunodeficiency virus: kinetics of replication and estimated prevalence in untreated patients. J Virol 70: 7894-7899.
57. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EA, et al. (1995) Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373: 117-122.
58. Goffinet C, Allespach I, Oberbremer L, Golden PL, Foster SA, et al. (2009) Pharmacovirological impact of an integrase inhibitor on human immunodeficiency virus type 1 cDNA species in vivo. J Virol 83: 7706-7717.
59. Nicastri E, Sarmati L, d'Ettorre G, Palmisano L, Parisi SG, et al. (2003) Replication capacity, biological phenotype, and drug resistance of hiv strains isolated from patients failing antiretroviral therapy. J Med Virol 69: 1-6.
60. Rong L, Feng Z, Perelson AS (2007) Mathematical analysis of age-structured hiv-1 dynamics with combination antiretroviral therapy. Siam J Appl Math 67: 731-756.
61. Perelson AS, Nelson PW (1999) Mathematical analysis of HIV-1 dynamics in vivo. SIAM Review 41: 3-44.
62. Beerenwinkel N, Rahnenführer J, Däumer M, Hoffmann D, Kaiser R, et al. (2005) Learning multiple evolutionary pathways from cross-sectional data. J Comput Biol 12: 584-598.
63. Beerenwinkel N, Däumer M, Sing T, Rahnenfuhrer J, Lengauer T, et al. (2005) Estimating HIV evolutionary pathways and the genetic barrier to drug resistance. J Infect Dis 191: 1953-1960.
64. Eriksson N, Pachter L, Mitsuya Y, Rhee SY, Wang C, et al. (2008) Viral population estimation using pyrosequencing. PLoS Comput Biol 4: e1000074.
65. Bushman FD, Hoffmann C, Ronen K, Malani N, Minkah N, et al. (2008) Massively parallel pyrosequencing in HIV research. AIDS 22: 1411-1415.
66. Rozera G, Abbate I, Bruselles A, Vlassi C, D'Offizi G, et al. (2009) Massively parallel pyrosequencing highlights minority variants in the HIV-1 Env quasispecies deriving from lymphomonocyte sub-populations. Retrovirology 6: 15.
67. Le T, Chiarella J, Simen BB, Hanczaruk B, Egholm M, et al. (2009) Low-abundance HIV drug-resistant viral variants in treatment-experienced persons correlate with historical antiretroviral use. PLoS One 4: e6079.
68. Klopfenstein R (1971) Numerical differentiation formulas for stiff systems of ordinary differential equations. RCA Review 32: 447-462.
69. Shampine L, Reichelt M (1997) The matlab ode suite. SIAM Journal on Scientific Computing 18: 1-22.
70. Rong L, Perelson AS (2009) Modeling HIV persistence, the latent reservoir, and viral blips. J Theor Biol 260: 308-331.
71. Kawai R, Mathew D, Tanaka C, Rowland M (1998) Physiologically based pharmacokinetics of cyclosporine a: extension to tissue distribution kinetics in rats and scale-up to human. J Pharmacol Exp Ther 287: 457-468.
72. von Kleist M, Huisinga W (2007) Physiologically based pharmacokinetic modelling: a sub-compartmentalized model of tissue distribution. J Pharmacokinet Pharmacodyn 34: 789-806.
73. Markowitz M, Louie M, Hurley A, Sun E, Mascio MD, et al. (2003) A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J Virol 77: 5037-5038.
74. Pierson TC, Zhou Y, Kieffer TL, Ruff CT, Buck C, et al. (2002) Molecular characterization of preintegration latency in human immunodeficiency virus type 1 infection. J Virol 76: 8518-8531.
75. Zhou Y, Zhang H, Siliciano JD, Siliciano RF (2005) Kinetics of human immunodeficiency virus type 1 decay following entry into resting CD4+ T cells. J Virol 79: 2199-2210.
76. Koelsch KK, Liu L, Haubrich R, May S, Havlir D, et al. (2008) Dynamics of total, linear nonintegrated, and integrated HIV-1 DNA in vivo and in vitro. J Infect Dis 197: 411-419.