The role of the N-terminal segment of CCR5 in HIV-1 Env-mediated membrane fusion and the mechanism of virus adaptation to CCR5 lacking this segment

Retrovirology

Volumn 4, Issue , 2007, Pages

  Melikyan, Gregory B ^a   Platt, Emily J ^b   Kabat, David ^b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PORTLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD5 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 41; SYNTHETIC PEPTIDE; VIRUS ENVELOPE PROTEIN; 4 ((4 BROMOPHENYL) (ETHOXYIMINO)METHYL) 1' ((2,4 DIMETHYL 3 PYRIDINYL)CARBONYL) 4' METHYL 1,4' BIPIPERIDINE N OXIDE; 4-((4-BROMOPHENYL)-(ETHOXYIMINO)METHYL)-1'-((2,4-DIMETHYL-3-PYRIDINYL)CARBONYL)-4'-METHYL-1,4'-BIPIPERIDINE N-OXIDE; AMINE OXIDE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; PIPERIDINE DERIVATIVE; PYRIDINE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL FUSION; COMPLEX FORMATION; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INCUBATION TIME; MEMBRANE FUSION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; QUANTITATIVE ANALYSIS; RECEPTOR AFFINITY; RECEPTOR BINDING; TARGET CELL; THERMOREGULATION; WILD TYPE; AMINO ACID SEQUENCE; CHEMISTRY; DRUG ANTAGONISM; GENE DELETION; GENETICS; HELA CELL; KINETICS; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; TEMPERATURE; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; ANTI-HIV AGENTS; CYCLIC N-OXIDES; HELA CELLS; HIV ENVELOPE PROTEIN GP120; HIV FUSION INHIBITORS; HIV-1; HUMANS; KINETICS; MEMBRANE FUSION; MUTATION; PIPERIDINES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PYRIDINES; RECEPTORS, CCR5; SEQUENCE DELETION; TEMPERATURE; VIRUS INTERNALIZATION;

EID: 34848915403     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-4-55     Document Type: Article

References (64)

1. Berger EA Murphy PM Farber JM Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease Annu Rev Immunol 1999, 17:657-700. 10.1146/annurev.immunol.17.1.657 10358771
2. Wyatt R Sodroski J The HIV-1 envelope glycoproteins: Fusogens, antigens, and immunogens Science 1998, 280(5371):1884-1888. 10.1126/ science.280.5371.1884 9632381
3. Earp LJ Delos SE Park HE White JM The many mechanisms of viral membrane fusion proteins Curr Top Microbiol Immunol 2005, 285:25-66. 15609500
4. Eckert DM Kim PS Mechanisms of Viral Membrane Fusion and Its Inhibition Annu Rev Biochem 2001, 70:777-810. 10.1146/annurev.biochem.70.1.777 11395423
5. Gallo SA Finnegan CM Viard M Raviv Y Dimitrov A Rawat SS Puri A Durell S Blumenthal R The HIV Env-mediated fusion reaction Biochim Biophys Acta 2003, 1614(1):36-50. 10.1016/S0005-2736(03)00161-5 12873764
6. Carr CM Kim PS A spring-loaded mechanism for the conformational change of influenza hemagglutinin Cell 1993, 73(4):823-832. 10.1016/ 0092-8674(93)90260-W 8500173
7. Brelot A Heveker N Montes M Alizon M Identification of residues of CXCR4 critical for human immunodeficiency virus coreceptor and chemokine receptor activities J Biol Chem 2000, 275(31):23736-23744. 10.1074/ jbc.M000776200 10825158
8. Cormier EG Tran DN Yukhayeva L Olson WC Dragic T Mapping the determinants of the CCR5 amino-terminal sulfopeptide interaction with soluble human immunodeficiency virus type 1 gp120-CD4 complexes. J Virol 2001, 75(12):5541-5549. 114266 11356961 10.1128/JVI.75.12.5541-5549.2001
9. Chabot DJ Zhang PF Quinnan GV Broder CC Mutagenesis of CXCR4 identifies important domains for human immunodeficiency virus type 1 X4 isolate envelope-mediated membrane fusion and virus entry and reveals cryptic coreceptor activity for R5 isolates. J Virol 1999, 73(8):6598-6609. 112744 10400757
10. Doranz BJ Orsini MJ Turner JD Hoffman TL Berson JF Hoxie JA Peiper SC Brass LF Doms RW Identification of CXCR4 domains that support coreceptor and chemokine receptor functions. J Virol 1999, 73(4):2752-2761. 104032 10074122
11. Lee B Sharron M Blanpain C Doranz BJ Vakili J Setoh P Berg E Liu G Guy HR Durell SR Parmentier M Chang CN Price K Tsang M Doms RW Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J Biol Chem 1999, 274(14):9617-9626. 10.1074/jbc.274.14.9617 10092648
12. Lin G Baribaud F Romano J Doms RW Hoxie JA Identification of gp120 binding sites on CXCR4 by using CD4-independent human immunodeficiency virus type 2 Env proteins. J Virol 2003, 77(2):931-942. 140809 12502809 10.1128/JVI.77.2.931-942.2003
13. Pontow S Ratner L Evidence for common structural determinants of human immunodeficiency virus type 1 coreceptor activity provided through functional analysis of CCR5/CXCR4 chimeric coreceptors. J Virol 2001, 75(23):11503-11514. 114737 11689632 10.1128/JVI.75.23.11503-11514.2001
14. Safarian D Carnec X Tsamis F Kajumo F Dragic T An anti-CCR5 monoclonal antibody and small molecule CCR5 antagonists synergize by inhibiting different stages of human immunodeficiency virus type 1 entry. Virology 2006, 352(2):477-484. 10.1016/j.virol.2006.05.016 16777164
15. Bieniasz PD Fridell RA Aramori I Ferguson SS Caron MG Cullen BR HIV-1-induced cell fusion is mediated by multiple regions within both the viral envelope and the CCR-5 co-receptor. Embo J 1997, 16(10):2599-2609. 1169871 9184207 10.1093/emboj/16.10.2599
16. Huang CC Tang M Zhang MY Majeed S Montabana E Stanfield RL Dimitrov DS Korber B Sodroski J Wilson IA Wyatt R Kwong PD Structure of a V3-containing HIV-1 gp120 core. Science 2005, 310(5750):1025-1028. 10.1126/science.1118398 16284180
17. Zhou N Luo Z Luo J Liu D Hall JW Pomerantz RJ Huang Z Structural and functional characterization of human CXCR4 as a chemokine receptor and HIV-1 co-receptor by mutagenesis and molecular modeling studies. J Biol Chem 2001, 276(46):42826-42833. 10.1074/jbc.M106582200 11551942
18. Blanpain C Doranz BJ Vakili J Rucker J Govaerts C Baik SS Lorthioir O Migeotte I Libert F Baleux F Vassart G Doms RW Parmentier M Multiple charged and aromatic residues in CCR5 amino-terminal domain are involved in high affinity binding of both chemokines and HIV-1 Env protein. J Biol Chem 1999, 274(49):34719-34727. 10.1074/jbc.274.49.34719 10574939
19. Doranz BJ Lu ZH Rucker J Zhang TY Sharron M Cen YH Wang ZX Guo HH Du JG Accavitti MA Doms RW Peiper SC Two distinct CCR5 domains can mediate coreceptor usage by human immunodeficiency virus type 1. J Virol 1997, 71(9):6305-6314. 191903 9261347
20. Dragic T An overview of the determinants of CCR5 and CXCR4 co-receptor function. J Gen Virol 2001, 82(Pt 8):1807-1814. 11457985
21. Kuhmann SE Platt EJ Kozak SL Kabat D Polymorphisms in the CCR5 genes of African green monkeys and mice implicate specific amino acids in infections by simian and human immunodeficiency viruses. J Virol 1997, 71(11):8642-8656. 192328 9343222
22. Siciliano SJ Kuhmann SE Weng Y Madani N Springer MS Lineberger JE Danzeisen R Miller MD Kavanaugh MP DeMartino JA Kabat D A critical site in the core of the CCR5 chemokine receptor required for binding and infectivity of human immunodeficiency virus type 1. J Biol Chem 1999, 274(4):1905-1913. 10.1074/jbc.274.4.1905 9890944
23. Cormier EG Dragic T The crown and stem of the V3 loop play distinct roles in human immunodeficiency virus type 1 envelope glycoprotein interactions with the CCR5 coreceptor. J Virol 2002, 76(17):8953-8957. 136967 12163614 10.1128/JVI.76.17.8953-8957.2002
24. Liu S Fan S Sun Z Structural and functional characterization of the human CCR5 receptor in complex with HIV gp120 envelope glycoprotein and CD4 receptor by molecular modeling studies. J Mol Model 2003, 9(5):329-336. 10.1007/s00894-003-0154-9 14517611
25. Biscone MJ Miamidian JL Muchiri JM Baik SS Lee FH Doms RW Reeves JD Functional impact of HIV coreceptor-binding site mutations. Virology 2006, 351(1):226-236. 16631222
26. Kwong PD Wyatt R Robinson J Sweet RW Sodroski J Hendrickson WA Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody [see comments]. Nature 1998, 393(6686):648-659. 10.1038/31405 9641677
27. Reeves JD Gallo SA Ahmad N Miamidian JL Harvey PE Sharron M Pohlmann S Sfakianos JN Derdeyn CA Blumenthal R Hunter E Doms RW Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc Natl Acad Sci U S A 2002, 99(25):16249-16254. 138597 12444251 10.1073/pnas.252469399
28. Reeves JD Miamidian JL Biscone MJ Lee FH Ahmad N Pierson TC Doms RW Impact of mutations in the coreceptor binding site on human immunodeficiency virus type 1 fusion, infection, and entry inhibitor sensitivity. J Virol 2004, 78(10):5476-5485. 400359 15113926 10.1128/ JVI.78.10.5476-5485.2004
29. Dragic T Trkola A Lin SW Nagashima KA Kajumo F Zhao L Olson WC Wu L Mackay CR Allaway GP Sakmar TP Moore JP Maddon PJ Amino-terminal substitutions in the CCR5 coreceptor impair gp120 binding and human immunodeficiency virus type 1 entry. J Virol 1998, 729(1):279-285. 109374 9420225
30. Farzan M Choe H Vaca L Martin K Sun Y Desjardins E Ruffing N Wu L Wyatt R Gerard N Gerard C Sodroski J A tyrosine-rich region in the N terminus of CCR5 is important for human immunodeficiency virus type 1 entry and mediates an association between gp120 and CCR5. J Virol 1998, 72(2):1160-1164. 124591 9445013
31. Ross TM Bieniasz PD Cullen BR Multiple residues contribute to the inability of murine CCR-5 to function as a coreceptor for macrophage-tropic human immunodeficiency virus type 1 isolates. J Virol 1998, 72(3):1918-1924. 109483 9499044
32. Farzan M Chung S Li W Vasilieva N Wright PL Schnitzler CE Marchione RJ Gerard C Gerard NP Sodroski J Choe H Tyrosine-sulfated peptides functionally reconstitute a CCR5 variant lacking a critical amino-terminal region. J Biol Chem 2002, 277(43):40397-40402. 10.1074/ jbc.M206784200 12183462
33. Cormier EG Persuh M Thompson DA Lin SW Sakmar TP Olson WC Dragic T Specific interaction of CCR5 amino-terminal domain peptides containing sulfotyrosines with HIV-1 envelope glycoprotein gp120. Proc Natl Acad Sci U S A 2000, 97(11):5762-5767. 18507 10823934 10.1073/pnas.97.11.5762
34. Farzan M Vasilieva N Schnitzler CE Chung S Robinson J Gerard NP Gerard C Choe H Sodroski J A tyrosine-sulfated peptide based on the N terminus of CCR5 interacts with a CD4-enhanced epitope of the HIV-1 gp120 envelope glycoprotein and inhibits HIV-1 entry. J Biol Chem 2000, 275(43):33516-33521. 10.1074/jbc.M007228200 10938094
35. Brelot A Heveker N Pleskoff O Sol N Alizon M Role of the first and third extracellular domains of CXCR-4 in human immunodeficiency virus coreceptor activity. J Virol 1997, 71(6):4744-4751. 191696 9151868
36. Platt EJ Shea DM Rose PP Kabat D Variants of human immunodeficiency virus type 1 that efficiently use CCR5 lacking the tyrosine-sulfated amino terminus have adaptive mutations in gp120, including loss of a functional N-glycan. J Virol 2005, 79(7):4357-4368. 1061536 15767436 10.1128/JVI.79.7.4357-4368.2005
37. Olson WC Rabut GE Nagashima KA Tran DN Anselma DJ Monard SP Segal JP Thompson DA Kajumo F Guo Y Moore JP Maddon PJ Dragic T Differential inhibition of human immunodeficiency virus type 1 fusion, gp120 binding, and CC-chemokine activity by monoclonal antibodies to CCR5. J Virol 1999, 73(5):4145-4155. 104194 10196311
38. Wu L Paxton WA Kassam N Ruffing N Rottman JB Sullivan N Choe H Sodroski J Newman W Koup RA Mackay CR CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J Exp Med 1997, 185(9):1681-1691. 10.1084/jem.185.9.1681 9151905
39. Farzan M Mirzabekov T Kolchinsky P Wyatt R Cayabyab M Gerard NP Gerard C Sodroski J Choe H Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 1999, 96(5):667-676. 10.1016/ S0092-8674(00)80577-2 10089882
40. Martin KA Wyatt R Farzan M Choe H Marcon L Desjardins E Robinson J Sodroski J Gerard C Gerard NP CD4-independent binding of SIV gp120 to rhesus CCR5. Science 1997, 278(5342):1470-1473. 10.1126/ science.278.5342.1470 9367961
41. Deng Y Zheng Q Ketas TJ Moore JP Lu M Protein design of a bacterially expressed HIV-1 gp41 fusion inhibitor. Biochemistry 2007, 46(14):4360-4369. 10.1021/bi7001289 17371053
42. Frey S Marsh M Gunther S Pelchen-Matthews A Stephens P Ortlepp S Stegmann T Temperature dependence of cell-cell fusion induced by the envelope glycoprotein of human immunodeficiency virus type 1. J Virol 1995, 69(3):1462-1472. 188734 7853478
43. Gallo SA Puri A Blumenthal R HIV-1 gp41 six-helix bundle formation occurs rapidly after the engagement of gp120 by CXCR4 in the HIV-1 Env-mediated fusion process. Biochemistry 2001, 40(41):12231-12236. 10.1021/bi0155596 11591141
44. Golding H Zaitseva M de Rosny E King LR Manischewitz J Sidorov I Gorny MK Zolla-Pazner S Dimitrov DS Weiss CD Dissection of human immunodeficiency virus type 1 entry with neutralizing antibodies to gp41 fusion intermediates. J Virol 2002, 76(13):6780-6790. 136262 12050391 10.1128/JVI.76.13.6780-6790.2002
45. Melikyan GB Markosyan RM Hemmati H Delmedico MK Lambert DM Cohen FS Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion [In Process Citation]. J Cell Biol 2000, 151(2):413-424. 10.1083/jcb.151.2.413 11038187
46. Mkrtchyan SR Markosyan RM Eadon MT Moore JP Melikyan GB Cohen FS Ternary complex formation of human immunodeficiency virus type 1 Env, CD4, and chemokine receptor captured as an intermediate of membrane fusion. J Virol 2005, 79(17):11161-11169. 1193594 16103167 10.1128/ JVI.79.17.11161-11169.2005
47. Abrahamyan LG Mkrtchyan SR Binley J Lu M Melikyan GB Cohen FS The cytoplasmic tail slows the folding of human immunodeficiency virus type 1 Env from a late prebundle configuration into the six-helix bundle. J Virol 2005, 79(1):106-115. 538707 15596806 10.1128/JVI.79.1.106-115.2005
48. Strizki JM Xu S Wagner NE Wojcik L Liu J Hou Y Endres M Palani A Shapiro S Clader JW Greenlee WJ Tagat JR McCombie S Cox K Fawzi AB Chou CC Pugliese-Sivo C Davies L Moreno ME Ho DD Trkola A Stoddart CA Moore JP Reyes GR Baroudy BM SCH-C (SCH 351125), an orally bioavailable, small molecule antagonist of the chemokine receptor CCR5, is a potent inhibitor of HIV-1 infection in vitro and in vivo. Proc Natl Acad Sci U S A 2001, 98(22):12718-12723. 60120 11606733 10.1073/pnas.221375398
49. Abrahamyan LG Markosyan RM Moore JP Cohen FS Melikyan GB Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion. J Virol 2003, 77(10):5829-5836. 154041 12719576 10.1128/ JVI.77.10.5829-5836.2003
50. Kuhmann SE Platt EJ Kozak SL Kabat D Cooperation of multiple CCR5 coreceptors is required for infections by human immunodeficiency virus type 1. J Virol 2000, 74(15):7005-7015. 112217 10888639 10.1128/ JVI.74.15.7005-7015.2000
51. Furuta RA Wild CT Weng Y Weiss CD Capture of an early fusion-active conformation of HIV-1 gp41. Nat Struct Biol 1998, 5(4):276-279. 10.1038/ nsb0498-276 9546217
52. He Y Vassell R Zaitseva M Nguyen N Yang Z Weng Y Weiss CD Peptides trap the human immunodeficiency virus type 1 envelope glycoprotein fusion intermediate at two sites. J Virol 2003, 77(3):1666-1671. 140873 12525600 10.1128/JVI.77.3.1666-1671.2003
53. Kilgore NR Salzwedel K Reddick M Allaway GP Wild CT Direct evidence that C-peptide inhibitors of human immunodeficiency virus type 1 entry bind to the gp41 N-helical domain in receptor-activated viral envelope. J Virol 2003, 77(13):7669-7672. 164814 12805467 10.1128/ JVI.77.13.7669-7672.2003
54. Baik SS Doms RW Doranz BJ HIV and SIV gp120 binding does not predict coreceptor function. Virology 1999, 259(2):267-273. 10.1006/ viro.1999.9779 10388651
55. Doranz BJ Baik SS Doms RW Use of a gp120 binding assay to dissect the requirements and kinetics of human immunodeficiency virus fusion events. J Virol 1999, 73(12):10346-10358. 113090 10559353
56. Hwang SS Boyle TJ Lyerly HK Cullen BR Identification of envelope V3 loop as the major determinant of CD4 neutralization sensitivity of HIV-1. Science 1992, 257(5069):535-537. 10.1126/science.1636088 1636088
57. Babcock GJ Mirzabekov T Wojtowicz W Sodroski J Ligand binding characteristics of CXCR4 incorporated into paramagnetic proteoliposomes. J Biol Chem 2001, 276(42):38433-38440. 10.1074/jbc.M106229200 11489906
58. Hoffman TL Canziani G Jia L Rucker J Doms RW A biosensor assay for studying ligand-membrane receptor interactions: Binding of antibodies and HIV-1 Env to chemokine receptors. Proc Natl Acad Sci U S A 2000, 97(21):11215-11220. 17180 11005830 10.1073/pnas.190274097
59. Wu L Gerard NP Wyatt R Choe H Parolin C Ruffing N Borsetti A Cardoso AA 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. 10.1038/384179a0 8906795
60. Rucker J Samson M Doranz BJ Libert F Berson JF Yi Y Smyth RJ Collman RG Broder CC Vassart G Doms RW Parmentier M Regions in beta-chemokine receptors CCR5 and CCR2b that determine HIV-1 cofactor specificity. Cell 1996, 87(3):437-446. 10.1016/S0092-8674(00)81364-1 8898197
61. Platt EJ Wehrly K Kuhmann SE Chesebro B Kabat D Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 1998, 72(4):2855-2864. 109730 9525605
62. Platt EJ Kuhmann SE Rose PP Kabat D Adaptive mutations in the V3 loop of gp120 enhance fusogenicity of human immunodeficiency virus type 1 and enable use of a CCR5 coreceptor that lacks the amino-terminal sulfated region. J Virol 2001, 75(24):12266-12278. 116123 11711617 10.1128/ JVI.75.24.12266-12278.2001
63. Chesebro B Wehrly K Development of a sensitive quantitative focal assay for human immunodeficiency virus infectivity. J Virol 1988, 62(10):3779-3788. 253522 3047430
64. Chesebro B Wehrly K Metcalf J Griffin DE Use of a new CD4-positive HeLa cell clone for direct quantitation of infectious human immunodeficiency virus from blood cells of AIDS patients. J Infect Dis 1991, 163(1):64-70. 1984477