HIV-1 Tropism Determination Using a Phenotypic Env Recombinant Viral Assay Highlights Overestimation of CXCR4-Usage by Genotypic Prediction Algorithms for CRRF01_AE and CRF02_AG

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Mulinge, Martin ^a   Lemaire, Morgane ^a   Servais, Jean Yves ^a   Rybicki, Arkadiusz ^a   Struck, Daniel ^a   da Silva, Eveline Santos ^a   Verhofstede, Chris ^c   Lie, Yolanda ^d   Seguin Devaux, Carole ^a   Schmit, Jean Claude ^a,b   Bercoff, Danielle Perez ^a  

^a LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^b CENTRE HOSPITALIER DE LUXEMBOURG   (Luxembourg)

^c GHENT UNIVERSITY   (Belgium)

^d MONOGRAM BIOSCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; VIRUS ENVELOPE PROTEIN;

ANALYTIC METHOD; ARTICLE; CONTROLLED STUDY; ENHANCED SENSITIVITY TROPISM ASSAY; GENE SEQUENCE; GENETIC ALGORITHM; GENOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INTERMETHOD COMPARISON; LIMIT OF DETECTION; MAJOR CLINICAL STUDY; MICROBIOLOGICAL EXAMINATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; RECOMBINANT VIRAL ASSAY; VIRAL TROPISM;

ALGORITHMS; CYCLOHEXANES; GENOTYPE; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; LUCIFERASES; PHENOTYPE; RECEPTORS, CXCR4; TRIAZOLES; VIRAL TROPISM; VIRUS INTERNALIZATION;

EID: 84877294446     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060566     Document Type: Article

References (72)

1. Dalgleish AG, (1984) The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312: 763-767.
2. Deng H, Liu R, Ellmeier W, Choe S, Unutmaz D, et al. (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature 381: 661-666.
3. Oberlin E, (1996) The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line adapted HIV-1. Nature 382: 833-835.
4. Feng Y, Broder CC, Kennedy PE, Berger EA, (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane G protein-coupled receptor. Science 272: 872-877.
5. Choe H, (1996) The [beta]-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85: 1135-1148.
6. Dragic T, (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381: 667-673.
7. Alkhatib G, Combadiere C, Broder C, Feng Y, Kennedy P, et al. (1996) CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
8. Weissenhorn W, Dessen A, Harrison S, Skehel J, Wiley D, (1997) Atomic structure of the ectodomain from HIV-1 gp41. Nature 387: 426-430.
9. Cardozo T, (2007) Structural basis of co-receptor selectivity by the HIV-1 V3 loop. AIDS Res Hum Retroviruses 23: 415-426.
10. Shioda T, Levy JA, Cheng-Mayer C, (1992) Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 89: 9434-9438.
11. Berger E, Doms R, Fenyo E, Korber B, Littman D, et al. (1998) A newclassification for HIV-1. Nature 391: 240.
12. Hartley O, Klasse PJ, Sattentau QJ, Moore JP, (2005) V3: HIV's Switch-Hitter. AIDS Research and Human Retroviruses 21: 171-189.
13. Pastore C, Nedellec R, Ramos A, Pontow S, Ratner L, et al. (2006) Human immunodeficiency virus type 1 coreceptor switching: V1/V2 gain-of-fitness mutations compensate for V3 loss-of-fitness mutations. J Virol 80: 750-758.
14. Chalmet K, Dauwe K, Foquet L, Baatz F, Seguin-Devaux C, et al. (2011) Presence of CXCR4-Using HIV-1 in Patients With Recently Diagnosed Infection: Correlates and Evidence for Transmission. Journal of Infectious Diseases.
15. Schuitemaker H, van 't Wout A, Lusso P, (2011) Clinical significance of HIV-1 coreceptor usage. Journal of Translational Medicine 9: 1-17.
16. Bratt G, Karlsson A, Leandersson AC, Albert J, Wahren B, et al. (1998) Treatment history and baseline viral load, but not viral tropism or CCR-5 genotype, influence prolonged antiviral efficacy of highly active antiretroviral treatment. AIDS 12: 2193-2202.
17. Bjorndal A, Deng H, Jansson M, Fiore J, Colognesi C, et al. (1997) Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J Virol 71: 7478-7487.
18. Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR, (1997) Change in coreceptor use correlates with disease progression in HIV-1 infected individuals. J Exp Med 185: 621-628.
19. Esbjornsson J, Mansson F, Martinez-Arias W, Vincic E, Biague A, et al. (2010) Frequent CXCR4 tropism of HIV-1 subtype A and CRF02_AG during late-stage disease- indication of an evolving epidemic in West Africa. Retrovirology 7: 23.
20. Fenyö EM, Esbjörnsson J, Medstrand P, Jansson M, (2011) Human immunodeficiency virus type 1 biological variation and coreceptor use: from concept to clinical significance. Journal of Internal Medicine 270: 520-531.
21. Blaak H, (2000) In vivo HIV-1 infection of CD45RA+CD4+ T cells is established primarily by syncytium-inducing variants and correlates with the rate of CD4+ T cell decline. Proc Natl Acad Sci USA 97: 1269-1274.
22. Fatkenheuer G, Nelson M, Lazzarin A, Konourina I, Hoepelman A, et al. (2008) Subgroup analyses of maraviroc in previously treated R5 HIV-1 infection. N Engl J Med 359: 1442-1455.
23. Gulick R, Lalezari J, Goodrich J, Clumeck N, DeJesus E, et al. (2008) Maraviroc for previously treated patients with R5 HIV-1 infection. N Engl J Med 359: 1429-1441.
24. Harrigan PR, Geretti AM, (2011) Genotypic tropism testing: evidence-based or leap of faith. AIDS 25: 257-264.
25. Kuhmann SE, Hartley O (2008) Targeting chemokine receptors in HIV: A status report. Annual Review of Pharmacology and Toxicology. 425-461.
26. Westby M, Smith-Burchnell C, Mori J, Lewis M, Mosley M, et al. (2007) Reduced maximal inhibition in phenotypic susceptibility assays indicates that viral strains resistant to the CCR5 antagonist maraviroc utilize inhibitor-bound receptor for entry. J Virol 81: 2359-2371.
27. Baatz F, Nijhuis M, Lemaire M, Riedijk M, Wensing AMJ, et al. (2011) Impact of the HIV-1 Genetic Context outside HR1/HR2 on Resistance to the Fusion Inhibitor Enfuvirtide and Viral Infectivity in Clinical Isolates. PLoS ONE 6: e21535.
28. Pugach P, Marozsan AJ, Ketas TJ, Landes EL, Moore JP, et al. (2007) HIV-1 clones resistant to a small molecule CCR5 inhibitor use the inhibitor-bound form of CCR5 for entry. Virology 361: 212-228.
29. Rose JD, Rhea AM, Weber J, Quinones-Mateu ME, (2009) Current tests to evaluate HIV-1 coreceptor tropism. Current Opinion in HIV & AIDS 4: 136-142.
30. Reeves JD, Coakley E, Petropoulos CJ, Whitcomb JM, (2009) An Enhanced-Sensitivity Trofile™ HIV Coreceptor Tropism Assay for Selecting Patients for Therapy with Entry Inhibitors Targeting CCR5: A Review of Analytical and Clinical Studies. The Journal of Viral Entry 3: 94-102.
31. Whitcomb JM, Huang W, Fransen S, Limoli K, Toma J, et al. (2007) Development and characterization of a novel single-cycle recombinant-virus assay to determine human immunodeficiency virus type 1 coreceptor tropism. Antimicrob Agents Chemother 51: 566-575.
32. Van Baelen K, Vandenbroucke I, Rondelez E, Van Eygen V, Vermeiren H, et al. (2007) HIV-1 coreceptor usage determination in clinical isolates using clonal and population-based genotypic and phenotypic assays. J Virol Methods 146: 61-73.
33. Lin NH, Negusse DM, Beroukhim R, Giguel F, Lockman S, et al. (2010) The design and validation of a novel phenotypic assay to determine HIV-1 coreceptor usage of clinical isolates. Journal of Virological Methods 169: 39-46.
34. Trouplin V, Salvatori F, Cappello F, Obry V, Brelot A, et al. (2001) Determination of coreceptor usage of human immunodeficiency virus type 1 from patient plasma samples by using a recombinant phenotypic assay. J Virol 75: 251-259.
35. Raymond S, Delobel P, Mavigner M, Cazabat M, Souyris C, et al. (2010) Development and performance of a new recombinant virus phenotypic entry assay to determine HIV-1 coreceptor usage. Journal of Clinical Virology 47: 126-130.
36. Asboe D, Aitken C, Boffito M, Booth C, Cane P, et al. (2012) British HIV Association guidelines for the routine investigation and monitoring of adult HIV-1-infected individuals 2011. HIV Medicine 13: 1-44.
37. Delobel P, Nugeyre M-T, Cazabat M, Pasquier C, Marchou B, et al. (2007) Population-Based Sequencing of the V3 Region of env for Predicting the Coreceptor Usage of Human Immunodeficiency Virus Type 1 Quasispecies. Journal of Clinical Microbiology 45: 1572-1580.
38. Beerenwinkel N, Däumer M, Oette M, Korn K, Hoffmann D, et al. (2003) Geno2pheno: estimating phenotypic drug resistance from HIV-1 genotypes. Nucleic Acids Research 31: 3850-3855.
39. Jensen M, Li F, van 't Wout A, Nickle D, Shriner D, et al. (2003) Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loopsequences. J Virol 77: 13376-13388.
40. Vandekerckhove LPR, Wensing AMJ, Kaiser R, Brun-Vézinet F, Clotet B, et al. (2011) European guidelines on the clinical management of HIV-1 tropism testing. The Lancet Infectious Diseases 11: 394-407.
41. McGovern RA, Harrigan PR, Swenson LC (2010) Genotypic Inference of HIV-1 Tropism Using Population-based Sequencing of V3. J Vis Exp: e2531.
42. Recordon-Pinson P, Soulie C, Flandre P, (2010) Evaluation of the genotypic prediction of HIV-1 coreceptor use versus a phenotypic assay and correlation with the virological response to maraviroc: the ANRS GenoTropism study. Antimicrob Agents Chemother 54: 3335-3340.
43. Swenson LC, Moores A, Low AJ, Thielen A, Dong W, et al. (2010) Improved detection of CXCR4-using HIV by V3 genotyping: application of population-based and "deep" sequencing to plasma RNA and proviral DNA. J Acquir Immune Defic Syndr 54: 506-510.
44. Garrido C, Roulet V, Chueca N, Poveda E, Aguilera A, et al. (2008) Evaluation of Eight Different Bioinformatics Tools To Predict Viral Tropism in Different Human Immunodeficiency Virus Type 1 Subtypes. Journal of Clinical Microbiology 46: 887-891.
45. Raymond S, Delobel P, Mavigner M, Cazabat M, Souyris C, et al. (2009) Genotypic Prediction of HIV-1 CRF02-AG Tropism. J Clin Microbiol 47: 2292-2294.
46. Raymond S, Delobel P, Chaix ML, Cazabat M, Encinas S, et al. (2011) Genotypic prediction of HIV-1 subtype D tropism. Retrovirology 8: 56.
47. de Oliveira T, Deforche K, Cassol S, Salminen M, Paraskevis D, et al. (2005) An automated genotyping system for analysis of HIV-1 and other microbial sequences. Bioinformatics 21: 3797-3800.
48. Van Laethem K, Schrooten Y, Lemey P, Wijngaerden EV, Wit SD, et al. (2005) A genotypic resistance assay for the detection of drug resistance in the human immunodeficiency virus type 1 envelope gene. Journal of Virological Methods 123: 25-34.
49. Verhofstede C, Brudney D, Reynaerts J, Vaira D, Fransen K, et al. (2011) Concordance between HIV-1 genotypic coreceptor tropism predictions based on plasma RNA and proviral DNA. HIV Medicine 12: 544-552.
50. Batra M, Tien PC, Shafer RW, Contag CH, Katzenstein DA, (2000) HIV type 1 envelope subtype C sequences from recent seroconverters in Zimbabwe. AIDS Res Hum Retroviruses 16: 973-979.
51. Chakrabarti AK, Caruso L, Ding M, Shen C, Buchanan W, et al. (2009) Detection of HIV-1 RNA/DNA and CD4 mRNA in feces and urine from chronic HIV-1 infected subjects with and without anti-retroviral therapy. AIDS Res Ther 6: 20.
52. O'Doherty U, Swiggard WJ, Malim MH, (2000) Human Immunodeficiency Virus Type 1 Spinoculation Enhances Infection through Virus Binding. Journal of virology 74: 10074-10080.
53. Chueca N, Garrido C, Álvarez M, Poveda E, de Dios Luna J, et al. (2009) Improvement in the determination of HIV-1 tropism using the V3 gene sequence and a combination of bioinformatic tools. Journal of Medical Virology 81: 763-767.
54. Seclén E, Garrido C, Gonzalez MdM, Gonzalez-Lahoz J, de Mendoza C, et al. (2010) High sensitivity of specific genotypic tools for detection of X4 variants in antiretroviral-experienced patients suitable to be treated with CCR5 antagonists. Journal of Antimicrobial Chemotherapy 65: 1486-1492.
55. Qu S, Ma L, Yuan L, Xu W, Hong K, et al. (2010) Co-receptor usage and prediction of V3 genotyping algorithms in HIV-1 subtype B' from paid blood donors experienced anti-retroviral therapy in Chinese central province. Virol J 7: 280.
56. Delgado E, Fernandez-Garcia A, Vega Y, Cuevas T, Pinilla M, et al. (2012) Evaluation of genotypic tropism prediction tests compared with in vitro co-receptor usage in HIV-1 primary isolates of diverse subtypes. Journal of Antimicrobial Chemotherapy 67: 25-31.
57. Poveda E, Seclen E, Gonzalez Mdel M, Garcia F, Chueca N, et al. (2009) Design and validation of new genotypic tools for easy and reliable estimation of HIV tropism before using CCR5 antagonists. J Antimicrob Chemother 63: 1006-1010.
58. Poveda E, Briz V, Roulet V, del Mar Gonzalez M, Faudon J-L, et al. (2007) Correlation between a phenotypic assay and three bioinformatic tools for determining HIV co-receptor use. AIDS 21: 1487-1490 1410.1097/QAD.1480b1013e32826fb32741.
59. de Mendoza C, Van Baelen K, Poveda E, Rondelez E, Zahonero N, et al. (2008) Performance of a population-based HIV-1 tropism phenotypic assay and correlation with V3 genotypic prediction tools in recent HIV-1 seroconverters. J Acquir Immune Defic Syndr 48: 241-244.
60. Rodriguez JJ, Seclen E, Poveda E, Varela E, Regueiro B, et al. (2011) [Variability in HIV viral tropism determination using different genotypic algorithms in patients infected with B versus non-B HIV-1 subtypes]. Enferm Infecc Microbiol Clin 29: 4-8.
61. Raymond S, Delobel P, Mavigner M, Cazabat M, Souyris C, et al. (2008) Correlation between genotypic predictions based on V3 sequences and phenotypic determination of HIV-1 tropism. AIDS 22: F11-F16.
62. Raymond S, Delobel P, Rogez S, Encinas S, Bruel P, et al. (2012) Genotypic Prediction of HIV-1 CRF01-AE Tropism. J Clin Microbiol 5: 5.
63. Hoffman NG, Seillier-Moiseiwitsch F, Ahn J, Walker JM, Swanstrom R, (2002) Variability in the Human Immunodeficiency Virus Type 1 gp120 Env Protein Linked to Phenotype-Associated Changes in the V3 Loop. Journal of Virology 76: 3852-3864.
64. Huang CC, (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028.
65. Nabatov AA, Pollakis G, Linnemann T, Kliphius A, Chalaby MIM, et al. (2004) Intrapatient Alterations in the Human Immunodeficiency Virus Type 1 gp120 V1V2 and V3 Regions Differentially Modulate Coreceptor Usage, Virus Inhibition by CC/CXC Chemokines, Soluble CD4, and the b12 and 2G12 Monoclonal Antibodies. Journal of Virology 78: 524-530.
66. Zolla-Pazner S, Cardozo T, (2010) Structure-function relationships of HIV-1 envelope sequence-variable regions refocus vaccine design. Nat Rev Immunol 10: 527-535.
67. Ross TM, Cullen BR, (1998) The ability of HIV type 1 to use CCR-3 as a coreceptor is controlled by envelope V1/V2 sequences acting in conjunction with a CCR-5 tropic V3 loop. Proc Natl Acad Sci U S A 95: 7682-7686.
68. Clevestig P, Maljkovic I, Casper C, Carlenor E, Lindgren S, et al. (2005) The X4 phenotype of HIV type 1 evolves from R5 in two children of mothers, carrying X4, and is not linked to transmission. AIDS Res Hum Retroviruses 21: 371-378.
69. McCaffrey RA, Saunders C, Hensel M, Stamatatos L, (2004) N-Linked Glycosylation of the V3 Loop and the Immunologically Silent Face of gp120 Protects Human Immunodeficiency Virus Type 1 SF162 from Neutralization by Anti-gp120 and Anti-gp41 Antibodies. Journal of Virology 78: 3279-3295.
70. Pollakis G, Kang S, Kliphuis A, Chalaby MIM, Goudsmit J, et al. (2001) N-Linked Glycosylation of the HIV Type-1 gp120 Envelope Glycoprotein as a Major Determinant of CCR5 and CXCR4 Coreceptor Utilization. Journal of Biological Chemistry 276: 13433-13441.
71. Hamy F, Vidal V, Hubert S, Klimkait T (2007) Hybridization-based assay and replicative phenotyping as diagnostic platform for determination of coreceptor tropism. 5th European HIV drug resistance workshop: Abstract 60.
72. Gonzalez N, Perez-Olmeda M, Mateos E, Cascajero A, Alvarez A, et al. (2010) A sensitive phenotypic assay for the determination of human immunodeficiency virus type 1 tropism. J Antimicrob Chemother 65: 2493-2501.