Mutational pathways and genetic barriers to CXCR4-mediated entry by human immunodeficiency virus type 1

Virology

Volumn 409, Issue 2, 2011, Pages 308-318

  Huang, Wei ^a   Frantzell, Arne ^a   Toma, Jonathan ^a   Fransen, Signe ^a   Whitcomb, Jeannette M ^a   Stawiski, Eric ^a   Petropoulos, Christos J ^a  

^a MONOGRAM BIOSCIENCES   (United States)

Author keywords

CCR5; CCR5 antagonist; Coreceptor; CXCR4; Dual; HIV 1; R5; Tropism; V3; X4

Indexed keywords

CHEMOKINE RECEPTOR CXCR4;

AMINO ACID SUBSTITUTION; ARTICLE; CLONE; CONTROLLED STUDY; GENOTYPE; GLYCOSYLATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; VIRAL GENETICS; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS EXAMINATION; VIRUS INFECTIVITY; VIRUS MUTATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; RECEPTORS, CCR5; RECEPTORS, CXCR4; RECEPTORS, HIV; SEQUENCE ANALYSIS, DNA; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78650285592     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.09.026     Document Type: Article

References (61)

1. Berger E.A., Murphy P.M., Farber J.M. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 1999, 17:657-700.
2. Brumme Z.L., Goodrich J., Mayer H.B., Brumme C.J., Henrick B.M., Wynhoven B., Asselin J.J., Cheung P.K., Hogg R.S., Montaner J.S., Harrigan P.R. Molecular and clinical epidemiology of CXCR4-using HIV-1 in a large population of antiretroviral-naive individuals. J. Infect. Dis. 2005, 192(3):466-474.
3. Cardozo T., Kimura T., Philpott S., Weiser B., Burger H., Zolla-Pazner S. Structural basis for coreceptor selectivity by the HIV type 1 V3 loop. AIDS Res. Hum. Retroviruses 2007, 23(3):415-426.
4. Chesebro B., Wehrly K., Nishio J., Perryman S. Mapping of independent V3 envelope determinants of human immunodeficiency virus type 1 macrophage tropism and syncytium formation in lymphocytes. J. Virol. 1996, 70(12):9055-9059.
5. Coakley E., Benhamida J., Chappey C., Whitcomb J., Goodrich J., van der Ryst E., Westby M., James I., Tressler R., Harrigan P.R., Mayer H. 2nd International Workshop on Targeting HIV Entry, Boston, MA 2006.
6. Cocchi F., DeVico A.L., Garzino-Demo A., Cara A., Gallo R.C., Lusso P. The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nat. Med. 1996, 2(11):1244-1247.
7. Connor R.I., Sheridan K.E., Ceradini D., Choe S., Landau N.R. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 1997, 185(4):621-628.
8. Cooper D.A., Heera J., Goodrich J., Tawadrous M., Saag M., Dejesus E., Clumeck N., Walmsley S., Ting N., Coakley E., Reeves J.D., Reyes-Teran G., Westby M., Van Der Ryst E., Ive P., Mohapi L., Mingrone H., Horban A., Hackman F., Sullivan J., Mayer H. Maraviroc versus efavirenz, both in combination with zidovudine-lamivudine, for the treatment of antiretroviral-naive subjects with CCR5-tropic HIV-1 infection. J. Infect. Dis. 2010, 201(6):803-813.
9. Daar E.S., Kesler K.L., Petropoulos C.J., Huang W., Bates M., Lail A.E., Coakley E.P., Gomperts E.D., Donfield S.M. Baseline HIV type 1 coreceptor tropism predicts disease progression. Clin. Infect. Dis. 2007, 45(5):643-649.
10. De Jong J.J., De Ronde A., Keulen W., Tersmette M., Goudsmit J. Minimal requirements for the human immunodeficiency virus type 1V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J. Virol. 1992, 66(11):6777-6780.
11. Demarest J., Bonny T., Vavaro C., LaBranche C., Kitrinos K., McDanal C., Sparks S., Chavers S., Castillo S., Elrick D., McCarty D., Whitcomb J., Huang W., Petropoulos C., Piscitelli S. 44th Interscience Conference on Antimicrobial Agents and Chemotherapeutics, Washington, DC 2004.
12. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R.E., Hill C.M., Davis C.B., Peiper S.C., Schall T.J., Littman D.R., Landau N.R. Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996, 381(6584):661-666.
13. Eshleman S.H., Husnik M., Hudelson S., Donnell D., Huang Y., Huang W., Hart S., Jackson B., Coates T., Chesney M., Koblin B. Antiretroviral drug resistance, HIV-1 tropism, and HIV-1 subtype among men who have sex with men with recent HIV-1 infection. AIDS 2007, 21(9):1165-1174.
14. Fouchier R.A., Groenink M., Kootstra N.A., Tersmette M., Huisman H.G., Miedema F., Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J. Virol. 1992, 66(5):3183-3187.
15. Fransen S., Bridger G., Whitcomb J.M., Toma J., Stawiski E., Parkin N., Petropoulos C.J., Huang W. Suppression of dualtropic human immunodeficiency virus type 1 by the CXCR4 antagonist AMD3100 is associated with efficiency of CXCR4 use and baseline virus composition. Antimicrob. Agents Chemother. 2008, 52(7):2608-2615.
16. Gulick R.M., Su Z., Flexner C., Hughes M.D., Skolnik P.R., Wilkin T.J., Gross R., Krambrink A., Coakley E., Greaves W.L., Zolopa A., Reichman R., Godfrey C., Hirsch M., Kuritzkes D.R. Phase 2 study of the safety and efficacy of vicriviroc, a CCR5 inhibitor, in HIV-1-Infected, treatment-experienced patients: AIDS clinical trials group 5211. J. Infect. Dis. 2007, 196(2):304-312.
17. Gulick R.M., Lalezari J., Goodrich J., Clumeck N., DeJesus E., Horban A., Nadler J., Clotet B., Karlsson A., Wohlfeiler M., Montana J.B., McHale M., Sullivan J., Ridgway C., Felstead S., Dunne M.W., van der Ryst E., Mayer H. Maraviroc for previously treated patients with R5 HIV-1 infection. N Engl J. Med. 2008, 359(14):1429-1441.
18. Hendrix C.W., Collier A.C., Lederman M.M., Schols D., Pollard R.B., Brown S., Jackson J.B., Coombs R.W., Glesby M.J., Flexner C.W., Bridger G.J., Badel K., MacFarland R.T., Henson G.W., Calandra G. Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. J. Acquir. Immune Defic. Syndr. 2004, 37(2):1253-1262.
19. Hoffman T.L., Doms R.W. HIV-1 envelope determinants for cell tropism and chemokine receptor use. Mol. Membr. Biol. 1999, 16(1):57-65.
20. Huang W., Eshleman S.H., Toma J., Fransen S., Stawiski E., Paxinos E.E., Whitcomb J.M., Young A.M., Donnell D., Mmiro F., Musoke P., Guay L.A., Jackson J.B., Parkin N.T., Petropoulos C.J. Coreceptor tropism in human immunodeficiency virus type 1 subtype D: high prevalence of CXCR4 tropism and heterogeneous composition of viral populations. J. Virol. 2007, 81(15):7885-7893.
21. Huang W., Toma J., Fransen S., Stawiski E., Reeves J.D., Whitcomb J.M., Parkin N., Petropoulos C.J. Coreceptor tropism can be influenced by amino acid substitutions in the gp41 transmembrane subunit of human immunodeficiency virus type 1 envelope protein. J. Virol. 2008, 82(11):5584-5593.
22. Huang W., Toma J., Stawiski E., Fransen S., Wrin T., Parkin N., Whitcomb J.M., Coakley E., Hecht F.M., Deeks S.G., Gandhi R.T., Eshleman S.H., Petropoulos C.J. Characterization of human immunodeficiency virus type 1 populations containing CXCR4-using variants from recently infected individuals. AIDS Res. Hum. Retroviruses 2009, 25(8):795-802.
23. Hung C.S., Vander Heyden N., Ratner L. Analysis of the critical domain in the V3 loop of human immunodeficiency virus type 1 gp120 involved in CCR5 utilization. J. Virol. 1999, 73(10):8216-8226.
24. Hunt P.W., Harrigan P.R., Huang W., Bates M., Williamson D.W., McCune J.M., Price R.W., Spudich S.S., Lampiris H., Hoh R., Leigler T., Martin J.N., Deeks S.G. Prevalence of CXCR4 tropism among antiretroviral-treated HIV-1-infected patients with detectable viremia. J. Infect. Dis. 2006, 194(7):926-930.
25. Hwang S.S., Boyle T.J., Lyerly H.K., Cullen B.R. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 1991, 253(5015):71-74.
26. Jenkinson S., Thomson M., McCoy D., Edelstein M., Danehower S., Lawrence W., Wheelan P., Spaltenstein A., Gudmundsson K. Blockade of X4-tropic HIV-1 cellular entry by GSK812397, a potent noncompetitive CXCR4 receptor antagonist. Antimicrob. Agents Chemother. 2010, 54(2):817-824.
27. Jensen M.A., Li F.S., van 't Wout A.B., Nickle D.C., Shriner D., He H.X., McLaughlin S., Shankarappa R., Margolick J.B., Mullins J.I. Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J. Virol. 2003, 77(24):13376-13388.
28. + cell depletion and progression to AIDS. Ann. Intern. Med. 1993, 118(9):681-688.
29. Lewis M., Simpson P., Fransen S., Huang W., Whitcomb J., Mosley M., Robertson D.L., Mansfield R., Ciaramella G., Westby M. CXCR4-using virus detected in patients receiving maraviroc in the phase III studies MOTIVATE 1 and 2 originates from a pre-existing minority of CXCR4-using virus. Antivir. Ther. 2007, 12:S65.
30. Low A.J., Marchant D., Brumme C.J., Brumme Z.L., Dong W., Sing T., Hogg R.S., Montaner J.S., Gill V., Cheung P.K., Harrigan P.R. CD4-dependent characteristics of coreceptor use and HIV type 1 V3 sequence in a large population of therapy-naive individuals. AIDS Res. Hum. Retroviruses 2008, 24(2):219-228.
31. Markowitz M., Mohri H., Mehandru S., Shet A., Berry L., Kalyanaraman R., Kim A., Chung C., Jean-Pierre P., Horowitz A., La Mar M., Wrin T., Parkin N., Poles M., Petropoulos C., Mullen M., Boden D., Ho D.D. Infection with multidrug resistant, dual-tropic HIV-1 and rapid progression to AIDS: a case report. Lancet 2005, 365(9464):1031-1038.
32. Masquelier B., Capdepont S., Neau D., Peuchant O., Taupin J.L., Coakley E., Lie Y., Carpentier W., Dabis F., Fleury H.J. Virological characterization of an infection with a dual-tropic, multidrug-resistant HIV-1 and further evolution on antiretroviral therapy. AIDS 2007, 21(1):103-106.
33. Melby T., Despirito M., Demasi R., Heilek-Snyder G., Greenberg M.L., Graham N. HIV-1 coreceptor use in triple-class treatment-experienced patients: baseline prevalence, correlates, and relationship to enfuvirtide response. J. Infect. Dis. 2006, 194(2):238-246.
34. Mosier D.E., Picchio G.R., Gulizia R.J., Sabbe R., Poignard P., Picard L., Offord R.E., Thompson D.A., Wilken J. Highly potent RANTES analogues either prevent CCR5-using human immunodeficiency virus type 1 infection in vivo or rapidly select for CXCR4-using variants. J. Virol. 1999, 73(5):3544-3550.
35. Moyle G.J., Wildfire A., Mandalia S., Mayer H., Goodrich J., Whitcomb J., Gazzard B.G. Epidemiology and predictive factors for chemokine receptor use in HIV-1 infection. J. Infect. Dis. 2005, 191(6):866-872.
36. Moyle G., DeJesus E., Boffito M., Wong R.S., Gibney C., Badel K., MacFarland R., Calandra G., Bridger G., Becker S. Proof of activity with AMD11070, an orally bioavailable inhibitor of CXCR4-tropic HIV type 1. Clin. Infect. Dis. 2009, 48(6):798-805.
37. Murakami T., Kumakura S., Yamazaki T., Tanaka R., Hamatake M., Okuma K., Huang W., Toma J., Komano J., Yanaka M., Tanaka Y., Yamamoto N. The novel CXCR4 antagonist KRH-3955 is an orally bioavailable and extremely potent inhibitor of human immunodeficiency virus type 1 infection: comparative studies with AMD3100. Antimicrob. Agents Chemother. 2009, 53(7):2940-2948.
38. O'Brien W.A., Koyanagi Y., Namazie A., Zhao J.Q., Diagne A., Idler K., Zack J.A., Chen I.S. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 1990, 348(6296):69-73.
39. Pastore C., Nedellec R., Ramos A., Pontow S., Ratner L., Mosier D.E. Human immunodeficiency virus type 1 coreceptor switching: V1/V2 gain-of-fitness mutations compensate for V3 loss-of-fitness mutations. J. Virol. 2006, 80(2):750-758.
40. Pollakis G., Kang S., Kliphuis A., Chalaby M.I., Goudsmit J., Paxton W.A. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 2001, 276(16):13433-13441.
41. Resch W., Hoffman N., Swanstrom R. Improved success of phenotype prediction of the human immunodeficiency virus type 1 from envelope variable loop 3 sequence using neural networks. Virology 2001, 288(1):51-62.
42. Richman D.D., Bozzette S.A. The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J. Infect. Dis. 1994, 169(5):968-974.
43. Saag M., Goodrich J., Fatkenheuer G., Clotet B., Clumeck N., Sullivan J., Westby M., van der Ryst E., Mayer H. A double-blind, placebo-controlled trial of maraviroc in treatment-experienced patients infected with non-R5 HIV-1. J. Infect. Dis. 2009, 199(11):1638-1647.
44. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993, 234(3):779-815.
45. Sarkar G., Sommer S.S. The "megaprimer" method of site-directed mutagenesis. Biotechniques 1990, 8:404-407.
46. Schuitemaker H., Koot M., Kootstra N.A., Dercksen M.W., de Goede R.E., van Steenwijk R.P., Lange J.M., Schattenkerk J.K., Miedema F., Tersmette M. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J. Virol. 1992, 66(3):1354-1360.
47. Shepherd J.C., Jacobson L.P., Qiao W., Jamieson B.D., Phair J.P., Piazza P., Quinn T.C., Margolick J.B. Emergence and persistence of CXCR4-tropic HIV-1 in a population of men from the multicenter AIDS cohort study. J. Infect. Dis. 2008, 198(8):1104-1112.
48. Shioda T., Levy J.A., Cheng-Mayer C. Macrophage and T cell-line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene. Nature 1991, 349(6305):167-169.
49. Speck R.F., Wehrly K., Platt E.J., Atchison R.E., Charo I.F., Kabat D., Chesebro B., Goldsmith M.A. Selective employment of chemokine receptors as human immunodeficiency virus type 1 coreceptors determined by individual amino acids within the envelope V3 loop. J. Virol. 1997, 71(9):7136-7139.
50. Su Z., Gulick R.M., Krambrink A., Coakley E., Hughes M.D., Han D., Flexner C., Wilkin T.J., Skolnik P.R., Greaves W.L., Kuritzkes D.R., Reeves J.D. Response to vicriviroc in treatment-experienced subjects, as determined by an enhanced-sensitivity coreceptor tropism assay: reanalysis of AIDS clinical trials group A5211. J. Infect. Dis. 2009, 200(11):1724-1728.
51. Suleiman J., Zingman B.S., Diaz R.S., Madruga J.V., DeJesus E., Slim J., Mak C., Lee E., McCarthy M.C., Dunkle L.M., Walmsley S. Vicriviroc in combination therapy with an optimized regimen for treatment-experienced subjects: 48-week results of the VICTOR-E1 phase 2 trial. J. Infect. Dis. 2010, 201(4):590-599.
52. Tersmette M., Gruters R.A., de Wolf F., de Goede R.E., Lange J.M., Schellekens P.T., Goudsmit J., Huisman H.G., Miedema F. Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. J. Virol. 1989, 63(5):2118-2125.
53. Trkola A., Dragic T., Arthos J., Binley J.M., Olson W.C., Allaway G.P., Cheng-Mayer C., Robinson J., Maddon P.J., Moore J.P. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 1996, 384(6605):184-187.
54. Troyer R.M., Collins K.R., Abraha A., Fraundorf E., Moore D.M., Krizan R.W., Toossi Z., Colebunders R.L., Jensen M.A., Mullins J.I., Vanham G., Arts E.J. Changes in human immunodeficiency virus type 1 fitness and genetic diversity during disease progression. J. Virol. 2005, 79(14):9006-9018.
55. Trujillo J.R., Wang W.K., Lee T.H., Essex M. Identification of the envelope V3 loop as a determinant of a CD4-negative neuronal cell tropism for HIV-1. Virology 1996, 217(2):613-617.
56. Tsibris A.M., Korber B., Arnaout R., Russ C., Lo C.C., Leitner T., Gaschen B., Theiler J., Paredes R., Su Z., Hughes M.D., Gulick R.M., Greaves W., Coakley E., Flexner C., Nusbaum C., Kuritzkes D.R. Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoS ONE 2009, 4(5):e5683.
57. Westby M., Lewis M., Whitcomb J., Youle M., Pozniak A.L., James I.T., Jenkins T.M., Perros M., van der Ryst E. Emergence of CXCR4-using human immunodeficiency virus type 1 (HIV-1) variants in a minority of HIV-1-infected patients following treatment with the CCR5 antagonist maraviroc is from a pretreatment CXCR4-using virus reservoir. J. Virol. 2006, 80(10):4909-4920.
58. Westervelt P., Trowbridge D.B., Epstein L.G., Blumberg B.M., Li Y., Hahn B.H., Shaw G.M., Price R.W., Ratner L. Macrophage tropism determinants of human immunodeficiency virus type 1 in vivo. J. Virol. 1992, 66(4):2577-2582.
59. Whitcomb J.M., Huang W., Fransen S., Limoli K., Toma J., Wrin T., Chappey C., Kiss L.D., Paxinos E.E., Petropoulos C.J. Development and characterization of a novel single-cycle recombinant-virus assay to determine human immunodeficiency virus type 1 coreceptor tropism. Antimicrob. Agents Chemother. 2007, 51(2):566-575.
60. Wilkin T.J., Su Z., Kuritzkes D.R., Hughes M., Flexner C., Gross R., Coakley E., Greaves W., Godfrey C., Skolnik P.R., Timpone J., Rodriguez B., Gulick R.M. HIV type 1 chemokine coreceptor use among antiretroviral-experienced patients screened for a clinical trial of a CCR5 inhibitor: AIDS Clinical Trial Group A5211. Clin. Infect. Dis. 2007, 44(4):591-595.
61. Wu L., Gerard N.P., Wyatt R., Choe H., Parolin C., Ruffing N., Borsetti A., Cardoso A.A., Desjardin E., Newman W., Gerard C., Sodroski J. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 1996, 384(6605):179-183.