Transmission of Multiple HIV-1 Subtype C Transmitted/founder Viruses into the Same Recipients Was not Determined by Modest Phenotypic Differences

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Song, Hongshuo ^a   Hora, Bhavna ^a   Giorgi, Elena E ^b   Kumar, Amit ^a   Cai, Fangping ^a   Bhattacharya, Tanmoy ^b   Perelson, Alan S ^b   Gao, Feng ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c JILIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CCR5 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR5; VIRUS RECEPTOR;

CLASSIFICATION; DRUG EFFECT; GENETIC VARIATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; PHENOTYPE; PHYSIOLOGY; TRANSMISSION; VIRAL TROPISM; VIROLOGY; VIRUS GENOME; VIRUS REPLICATION;

GENETIC VARIATION; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-ALPHA; MALE; PHENOTYPE; RECEPTORS, CCR5; RECEPTORS, HIV; VIRAL TROPISM; VIRUS REPLICATION;

EID: 85003040921     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep38130     Document Type: Article

References (49)

1. Keele, B. F. et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proceedings of the National Academy of Sciences of the United States of America 105, 7552-7557 (2008).
2. Li, H. et al. High Multiplicity Infection by HIV-1 in Men Who Have Sex with Men. PLoS pathogens 6, e1000890 (2010).
3. Haaland, R. E. et al. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS pathogens 5, e1000274, doi: 10.1371/journal.ppat.1000274 (2009).
4. Abrahams, M. R. et al. Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. Journal of virology 83, 3556-3567, doi: 10.1128/JVI.02132-08 (2009).
5. Chen, Y. et al. Comprehensive Characterization of the Transmitted/Founder env Genes From a Single MSM Cohort in China. J Acquir Immune Defic Syndr 69, 403-412, doi: 10.1097/QAI.0000000000000649 (2015).
6. Shaw, G. M. & Hunter, E. HIV transmission. Cold Spring Harbor perspectives in medicine 2, doi: 10.1101/cshperspect.a006965 (2012).
7. Derdeyn, C. A. et al. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science (New York, N.Y.) 303, 2019-2022 (2004).
8. Chohan, B. et al. Selection for human immunodeficiency virus type 1 envelope glycosylation variants with shorter V1-V2 loop sequences occurs during transmission of certain genetic subtypes and may impact viral RNA levels. Journal of virology 79, 6528-6531 (2005).
9. Sagar, M. et al. Selection of HIV variants with signature genotypic characteristics during heterosexual transmission. The Journal of infectious diseases 199, 580-589, doi: 10.1086/596557 (2009).
10. Frost, S. D. et al. Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. Journal of virology 79, 6523-6527 (2005).
11. Wilen, C. B. et al. Phenotypic and immunologic comparison of clade B transmitted/founder and chronic HIV-1 envelope glycoproteins. Journal of virology 85, 8514-8527, doi: 10.1128/JVI.00736-11 (2011).
12. Gnanakaran, S. et al. Recurrent signature patterns in HIV-1 B clade envelope glycoproteins associated with either early or chronic infections. PLoS pathogens 7, e1002209, doi: 10.1371/journal.ppat.1002209 (2011).
13. Asmal, M. et al. A signature in HIV-1 envelope leader peptide associated with transition from acute to chronic infection impacts envelope processing and infectivity. PloS one 6, e23673, doi: 10.1371/journal.pone.0023673 (2011).
14. Salazar-Gonzalez, J. F. et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. The Journal of experimental medicine 206, 1273-1289 (2009).
15. Ochsenbauer, C. et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. Journal of virology 86, 2715-2728, doi: 10.1128/JVI.06157-11 (2012).
16. Parrish, N. F. et al. Phenotypic properties of transmitted founder HIV-1. Proceedings of the National Academy of Sciences of the United States of America 110, 6626-6633, doi: 10.1073/pnas.1304288110 (2013).
17. Fenton-May, A. E. et al. Relative resistance of HIV-1 founder viruses to control by interferon-Alpha. Retrovirology 10, 146, doi: 10.1186/1742-4690-10-146 (2013).
18. Giorgi, E. E. et al. Estimating time since infection in early homogeneous HIV-1 samples using a poisson model. BMC bioinformatics 11, 532, doi: 10.1186/1471-2105-11-532 (2010).
19. Shimizu, N. et al. A formylpeptide receptor, FPRL1, acts as an efficient coreceptor for primary isolates of human immunodeficiency virus. Retrovirology 5, 52, doi: 10.1186/1742-4690-5-52 (2008).
20. Edinger, A. L. et al. An orphan seven-transmembrane domain receptor expressed widely in the brain functions as a coreceptor for human immunodeficiency virus type 1 and simian immunodeficiency virus. Journal of virology 72, 7934-7940 (1998).
21. He, J. et al. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385, 645-649, doi: 10.1038/385645a0 (1997).
22. Choe, H. et al. The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85, 1135-1148 (1996).
23. Parrish, N. F. et al. Phenotypic properties of transmitted founder HIV-1. Proceedings of the National Academy of Sciences of the United States of America 110, 6626-6633, doi: 10.1073/pnas.1304288110 (2013).
24. Deymier, M. J. et al. Heterosexual Transmission of Subtype C HIV-1 Selects Consensus-Like Variants without Increased Replicative Capacity or Interferon-Alpha Resistance. PLoS pathogens 11, e1005154, doi: 10.1371/journal.ppat.1005154 (2015).
25. Jiang, C. et al. Primary infection by a human immunodeficiency virus with atypical coreceptor tropism. Journal of virology 85, 10669-10681, doi: 10.1128/JVI.05249-11 (2011).
26. Ritchie, A. J. et al. Recombination-mediated escape from primary CD8 + T cells in acute HIV-1 infection. Retrovirology 11, 69, doi: 10.1186/s12977-014-0069-9 (2014).
27. Song, H. et al. Impact of immune escape mutations on HIV-1 fitness in the context of the cognate transmitted/founder genome. Retrovirology 9, 89, doi: 10.1186/1742-4690-9-89 (2012).
28. Song, H. et al. Reversion and T cell escape mutations compensate the fitness loss of a CD8 + T cell escape mutant in their cognate transmitted/founder virus. PloS one 9, e102734, doi: 10.1371/journal.pone.0102734 (2014).
29. Cai, F. et al. Detection of minor drug-resistant populations by parallel allele-specific sequencing. Nature methods 4, 123-125, doi: 10.1038/nmeth995 (2007).
30. Liu, D. et al. Preexisting compensatory amino acids compromise fitness costs of a HIV-1 T cell escape mutation. Retrovirology 11, 101, doi: 10.1186/s12977-014-0101-0 (2014).
31. Nedellec, R. et al. Virus entry via the alternative coreceptors CCR3 and FPRL1 differs by human immunodeficiency virus type 1 subtype. Journal of virology 83, 8353-8363 (2009).
32. Isaacman-Beck, J. et al. Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. Journal of virology 83, 8208-8220 (2009).
33. Sandler, N. G. et al. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 511, 601-605, doi: 10.1038/nature13554 (2014).
34. Abel, K., Rocke, D. M., Chohan, B., Fritts, L. & Miller, C. J. Temporal and anatomic relationship between virus replication and cytokine gene expression after vaginal simian immunodeficiency virus infection. Journal of virology 79, 12164-12172, doi: 10.1128/JVI.79.19.12164-12172.2005 (2005).
35. Stacey, A. R. et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. Journal of virology 83, 3719-3733, doi: 10.1128/JVI.01844-08 (2009).
36. Arnott, A. et al. High viral fitness during acute HIV-1 infection. PloS one 5, doi: 10.1371/journal.pone.0012631 (2010).
37. Kong, X. et al. The human immunodeficiency virus type 1 envelope confers higher rates of replicative fitness to perinatally transmitted viruses than to nontransmitted viruses. Journal of virology 82, 11609-11618 (2008).
38. Quinones-Mateu, M. E. et al. A dual infection/competition assay shows a correlation between ex vivo human immunodeficiency virus type 1 fitness and disease progression. Journal of virology 74, 9222-9233 (2000).
39. Wilen, C. B. et al. Phenotypic and immunologic comparison of clade B transmitted/founder and chronic HIV-1 envelope glycoproteins. Journal of virology 85, 8514-8527, doi: 10.1128/JVI.00736-11 (2011).
40. Sanchez, A. M. et al. Development of a contemporary globally diverse HIV viral panel by the EQAPOL program. Journal of immunological methods 409, 117-130, doi: 10.1016/j.jim.2014.01.004 (2014).
41. Kirchherr, J. L. et al. High throughput functional analysis of HIV-1 env genes without cloning. J Virol Methods 143, 104-111 (2007).
42. Shimizu, N. et al. Broad usage spectrum of G protein-coupled receptors as coreceptors by primary isolates of HIV. Aids 23, 761-769 (2009).
43. Steimer, J. L., Mallet, A., Golmard, J. L. & Boisvieux, J. F. Alternative approaches to estimation of population pharmacokinetic parameters: comparison with the nonlinear mixed-effect model. Drug metabolism reviews 15, 265-292, doi: 10.3109/03602538409015066 (1984).
44. Davidian, M. & Giltinan, D. M. Nonlinear models for repeated measurement data. (Chapman & Hall/CRC, 1998).
45. Satterthwaite, F. E. An approximate distribution of estimates of variance components. Biometrics 2, 110-114 (1946).
46. Bonferroni, C. E. Teoria statistica delle classi e calcolo delle probabilitá. (Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commerciali di Firenze, 1936).
47. R: A Language and Environment for Statistical Computing, R Core Team, R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org (2016).
48. subplex: Subplex optimization algorithm. R package version 1.1-3. http://CRAN.R-project.org/package=subplex (2008).
49. ucminf: General-purpose unconstrained non-linear optimization. R package version 1.1-3. http://CRAN.R-project.org/package=ucminf (2012).