High viral fitness during acute HIV-1 infection

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-12

  Arnott, Alicia ^a,b,g   Jardine, Darren ^a,h   Wilson, Kim ^a   Gorry, Paul R ^b,c,d   Merlin, Kate ^e   Grey, Patricia ^e   Law, Matthew G ^e   Dax, Elizabeth M ^a,d   Kelleher, Anthony D ^e,f   Smith, Don E ^e,i   McPhee, Dale A ^a,b,d  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c BURNET INSTITUTE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f St Vincent's Centre for Applied Medical Research   (Australia)

^g INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^h ST VINCENT S HOSPITAL   (Australia)

ⁱ Albion Street Centre   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; INDINAVIR; LAMIVUDINE; RITONAVIR; STAVUDINE; VIRUS DNA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT;

ACUTE DISEASE; ARTICLE; CLINICAL STUDY; CONTROLLED STUDY; DISEASE MARKER; DNA SYNTHESIS; DRUG INTERMITTENT THERAPY; EVIDENCE BASED MEDICINE; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NONHUMAN; PATIENT MONITORING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RELIABILITY; SENSITIVITY ANALYSIS; SEROCONVERSION; VIRUS DETECTION; VIRUS ISOLATION; VIRUS LOAD; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; WILD TYPE; COHORT ANALYSIS; DRUG EFFECT; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; ISOLATION AND PURIFICATION; PHYSIOLOGY; REPRODUCTIVE FITNESS; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTI-HIV AGENTS; COHORT STUDIES; GENETIC FITNESS; HIV INFECTIONS; HIV-1; HUMANS; VIRAL LOAD; VIRUS REPLICATION;

EID: 77958566842     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012631     Document Type: Article

References (63)

1. Tebit DM, Nankya I, Arts EJ, Gao Y (2007) HIV diversity, recombination and disease progression: how does fitness "fit" into the puzzle? AIDS Rev 9: 75-87.
2. 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.
3. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, et al. (1997) Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387: 183-188.
4. 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.
5. 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.
6. Troyer RM, Collins KR, Abraha A, Fraundorf E, Moore DM, et al. (2005) Changes in human immunodeficiency virus type 1 fitness and genetic diversity during disease progression. J Virol 79: 9006-9018.
7. Clarke DK, Duarte EA, Elena SF, Moya A, Domingo E, et al. (1994) The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci U S A 91: 4821-4824.
8. Trkola A, Kuster H, Leemann C, Ruprecht C, Joos B, et al. (2003) Human immunodeficiency virus type 1 fitness is a determining factor in viral rebound and set point in chronic infection. J Virol 77: 13146-13155.
9. Verity EE, Zotos D, Wilson K, Chatfield C, Lawson VA, et al. (2007) Viral phenotypes and antibody responses in long-term survivors infected with attenuated human immunodeficiency virus type 1 containing deletions in the nef and long terminal repeat regions. J Virol 81: 9268-9278.
10. Geffin R, Wolf D, Muller R, Hill MD, Stellwag E, et al. (2000) Functional and structural defects in HIV type 1 nef genes derived from pediatric long-term survivors. AIDS Res Hum Retroviruses 16: 1855-1868.
11. Gorry PR, McPhee DA, Verity E, Dyer WB, Wesselingh SL, et al. (2007) Pathogenicity and immunogenicity of attenuated, nef-deleted HIV-1 strains in vivo. Retrovirology 4: 66.
12. Kondo M, Shima T, Nishizawa M, Sudo K, Iwamuro S, et al. (2005) Identification of attenuated variants of HIV-1 circulating recombinant form 01_AE that are associated with slow disease progression due to gross genetic alterations in the nef/long terminal repeat sequences. J Infect Dis 192: 56-61.
13. Mariani R, Kirchhoff F, Greenough TC, Sullivan JL, Desrosiers RC, et al. (1996) High frequency of defective nef alleles in a long-term survivor with nonprogressive human immunodeficiency virus type 1 infection. J Virol 70: 7752-7764.
14. Salvi R, Garbuglia AR, Di Caro A, Pulciani S, Montella F, et al. (1998) Grossly defective nef gene sequences in a human immunodeficiency virus type 1- seropositive long-term nonprogressor. J Virol 72: 3646-3657.
15. Quinones-Mateu ME, Ball SC, Marozsan AJ, Torre VS, Albright JL, et al. (2000) A dual infection/competition assay shows a correlation between ex vivo human immunodeficiency virus type 1 fitness and disease progression. J Virol 74: 9222-9233.
16. Campbell TB, Schneider K, Wrin T, Petropoulos CJ, Connick E (2003) Relationship between in vitro human immunodeficiency virus type 1 replication rate and virus load in plasma. J Virol 77: 12105-12112.
17. Dykes C, Demeter LM (2007) Clinical significance of human immunodeficiency virus type 1 replication fitness. Clin Microbiol Rev 20: 550-578.
18. Derdeyn CA, Hunter E (2008) Viral characteristics of transmitted HIV. Curr Opin HIV AIDS 3: 16-21.
19. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557.
20. Wood N, Bhattacharya T, Keele BF, Giorgi E, Liu M, et al. (2009) HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 5: e1000414.
21. Bloch MT, Smith DE, Quan D, Kaldor JM, Zaunders JJ, et al. (2006) The role of hydroxyurea in enhancing the virologic control achieved through structured treatment interruption in primary HIV infection: final results from a randomized clinical trial (Pulse). J Acquir Immune Defic Syndr 42: 192-202.
22. Falster K, Gelgor L, Shaik A, Zablotska I, Prestage G, et al. (2008) Trends in antiretroviral treatment use and treatment response in three Australian states in the first decade of combination antiretroviral treatment. Sex Health 5: 141-154.
23. Vandegraaff N, Kumar R, Burrell CJ, Li P (2001) Kinetics of human immunodeficiency virus type 1 (HIV) DNA integration in acutely infected cells as determined using a novel assay for detection of integrated HIV DNA. J Virol 75: 11253-11260.
24. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, et al. (2003) Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. Aids 17: 1871-1879.
25. Verity EE, Williams LA, Haddad DN, Choy V, O'Loughlin C, et al. (2006) Broad neutralization and complement-mediated lysis of HIV-1 by PEHRG214, a novel caprine anti-HIV-1 polyclonal antibody. Aids 20: 505-515.
26. Spira AI, Ho DD (1995) Effect of different donor cells on human immunodeficiency virus type 1 replication and selection in vitro. J Virol 69: 422-429.
27. Oelrichs RB, Lawson VA, Coates KM, Chatfield C, Deacon NJ, et al. (2000) Rapid full-length genomic sequencing of two cytopathically heterogeneous Australian primary HIV-1 isolates. J Biomed Sci 7: 128-135.
28. von Briesen H, Grez M, Ruppach H, Raudonat I, Unger RE, et al. (1999) Selection of HIV-1 genotypes by cultivation in different primary cells. Aids 13: 307-315.
29. Navis M, Matas DE, Rachinger A, Koning FA, van Swieten P, et al. (2008) Molecular evolution of human immunodeficiency virus type 1 upon transmission between human leukocyte antigen disparate donor-recipient pairs. PLoS One 3: e2422.
30. Desire N, Dehee A, Schneider V, Jacomet C, Goujon C, et al. (2001) Quantification of human immunodeficiency virus type 1 proviral load by a TaqMan real-time PCR assay. J Clin Microbiol 39: 1303-1310.
31. Yun Z, Fredriksson E, Sonnerborg A (2002) Quantification of human immunodeficiency virus type 1 proviral DNA by the TaqMan real-time PCR assay. J Clin Microbiol 40: 3883-3884.
32. Gray L, Churchill MJ, Sterjovski J, Witlox K, Learmont JC, et al. (2007) Phenotype and envelope gene diversity of nef-deleted HIV-1 isolated from longterm survivors infected from a single source. Virol J 4: 75.
33. Kiernan R, Marshall J, Bowers R, Doherty R, McPhee D (1990) Kinetics of HIV-1 replication and intracellular accumulation of particles in HTLV-Itransformed cells. AIDS Res Hum Retroviruses 6: 743-752.
34. Kim SY, Byrn R, Groopman J, Baltimore D (1989) Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: evidence for differential gene expression. J Virol 63: 3708-3713.
35. Belyakov IM, Berzofsky JA (2004) Immunobiology of mucosal HIV infection and the basis for development of a new generation of mucosal AIDS vaccines. Immunity 20: 247-253.
36. Ferbas J, Daar ES, Grovit-Ferbas K, Lech WJ, Detels R, et al. (1996) Rapid evolution of human immunodeficiency virus strains with increased replicative capacity during the seronegative window of primary infection. J Virol 70: 7285-7289.
37. Frater AJ, Edwards CT, McCarthy N, Fox J, Brown H, et al. (2006) Passive sexual transmission of human immunodeficiency virus type 1 variants and adaptation in new hosts. J Virol 80: 7226-7234.
38. Gottlieb GS, Heath L, Nickle DC, Wong KG, Leach SE, et al. (2008) HIV-1 variation before seroconversion in men who have sex with men: analysis of acute/early HIV infection in the multicenter AIDS cohort study. J Infect Dis 197: 1011-1015.
39. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952-3970.
40. Gali Y, Berkhout B, Vanham G, Bakker M, Back NK, et al. (2007) Survey of the temporal changes in HIV-1 replicative fitness in the Amsterdam Cohort. Virology 364: 140-146.
41. Simmonds P, Zhang LQ, McOmish F, Balfe P, Ludlam CA, et al. (1991) Discontinuous sequence change of human immunodeficiency virus (HIV) type 1 env sequences in plasma viral and lymphocyte-associated proviral populations in vivo: implications for models of HIV pathogenesis. J Virol 65: 6266-6276.
42. Garcia-Perez J, Perez-Olmeda M, Sanchez-Palomino S, Perez-Romero P, Alcami J (2008) A new strategy based on recombinant viruses for assessing the replication capacity of HIV-1. HIV Med 9: 160-171.
43. Rangel HR, Weber J, Chakraborty B, Gutierrez A, Marotta ML, et al. (2003) Role of the human immunodeficiency virus type 1 envelope gene in viral fitness. J Virol 77: 9069-9073.
44. Weber J, Rangel HR, Chakraborty B, Tadele M, Martinez MA, et al. (2003) A novel TaqMan real-time PCR assay to estimate ex vivo human immunodeficiency virus type 1 fitness in the era of multi-target (pol and env) antiretroviral therapy. J Gen Virol 84: 2217-2228.
45. Weber J, Weberova J, Carobene M, Mirza M, Martinez-Picado J, et al. (2006) Use of a novel assay based on intact recombinant viruses expressing green (EGFP) or red (DsRed2) fluorescent proteins to examine the contribution of pol and env genes to overall HIV-1 replicative fitness. J Virol Methods 136: 102-117.
46. Miura T, Brumme ZL, Brockman MA, Rosato P, Sela J, et al. Impaired replication capacity of acute/early viruses in persons who become HIV controllers. J Virol 84: 7581-7591.
47. Kong X, West JT, Zhang H, Shea DM, M'Soka T J, et al. (2008) The human immunodeficiency virus type 1 envelope confers higher rates of replicative fitness to perinatally transmitted viruses than to nontransmitted viruses. J Virol 82: 11609-11618.
48. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, et al. (2009) Genetic identity, biological phenotype, and evolutionary pathways of transmitted/ founder viruses in acute and early HIV-1 infection. J Exp Med 206: 1273-1289.
49. Muller HJ (1932) Some genetic aspects of sex. American Naturalist 66: 118-138.
50. Borderia AV, Lorenzo-Redondo R, Pernas M, Casado C, Alvaro T, et al. Initial fitness recovery of HIV-1 is associated with quasispecies heterogeneity and can occur without modifications in the consensus sequence. PLoS One 5: e10319.
51. Van Valen L (1974) Molecular evolution as predicted by natural selection. J Mol Evol 3: 89-101.
52. Wang YM, Dyer WB, Workman C, Wang B, Peng NK, et al. (2007) Drug resistance and viral evolution in plasma and peripheral blood cells during structured treatment interruption (STI) and non-interrupted HAART. Curr HIV Res 5: 235-250.
53. Loh L, Kent SJ (2008) Quantification of simian immunodeficiency virus cytotoxic T lymphocyte escape mutant viruses. AIDS Res Hum Retroviruses 24: 1067-1072.
54. Koch M, Pancera M, Kwong PD, Kolchinsky P, Grundner C, et al. (2003) Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313: 387-400.
55. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, et al. (2002) HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420: 678-682.
56. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
57. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, et al. (1997) Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 3: 205-211.
58. Sewell AK, Price DA, Oxenius A, Kelleher AD, Phillips RE (2000) Cytotoxic T lymphocyte responses to human immunodeficiency virus: control and escape. Stem Cells 18: 230-244.
59. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, 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.
60. Parisi SG, Boldrin C, Cruciani M, Nicolini G, Cerbaro I, et al. (2007) Both human immunodeficiency virus cellular DNA sequencing and plasma RNA sequencing are useful for detection of drug resistance mutations in blood samples from antiretroviral-drug-naive patients. J Clin Microbiol 45: 1783-1788.
61. Soto-Ramirez LE, Rodriguez-Diaz R, Duran AS, Losso MH, Salomon H, et al. (2008) Antiretroviral resistance among HIV type 1-infected women first exposed to antiretrovirals during pregnancy: plasma versus PBMCs. AIDS Res Hum Retroviruses 24: 797-804.
62. Bernardin F, Kong D, Peddada L, Baxter-Lowe LA, Delwart E (2005) Human immunodeficiency virus mutations during the first month of infection are preferentially found in known cytotoxic T-lymphocyte epitopes. J Virol 79: 11523-11528.
63. Peut V, Kent SJ (2006) Fitness constraints on immune escape from HIV: Implications of envelope as a target for both HIV-specific T cells and antibody. Curr HIV Res 4: 191-197.