Antiviral activity of α-helical stapled peptides designed from the HIV-1 capsid dimerization domain

Retrovirology

Volumn 8, Issue , 2011, Pages

  Zhang, Hongtao ^a   Curreli, Francesca ^a   Zhang, Xihui ^a   Bhattacharya, Shibani ^b   Waheed, Abdul A ^c   Cooper, Alan ^d   Cowburn, David ^e   Freed, Eric O ^c   Debnath, Asim K ^a  

^a NEW YORK BLOOD CENTER   (United States)

^b NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CAPSID PROTEIN; DIMER; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HYDROCARBON; PEPTIDE NYAD 201; PEPTIDE NYAD 202; PEPTIDE NYAD 203; PEPTIDE NYAD 209; PEPTIDE NYAD 215; PEPTIDE NYAD 233; UNCLASSIFIED DRUG; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CYCLOPEPTIDE; GAG PROTEIN;

ALPHA HELIX; ANTIVIRAL ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIMERIZATION; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG PENETRATION; DRUG POTENCY; DRUG SPECIFICITY; DRUG STABILITY; DRUG STRUCTURE; DRUG TARGETING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; INTRACELLULAR TRANSPORT; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN MODIFICATION; SEDIMENTATION; STRUCTURE ACTIVITY RELATION; VIRUS CAPSID; VIRUS INHIBITION; VIRUS ISOLATION; VIRUS PARTICLE; VIRUS STRAIN; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; SYNTHESIS; VIRION; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

AMINO ACID SEQUENCE; ANTI-HIV AGENTS; CELL LINE; CLONING, MOLECULAR; DRUG DESIGN; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENETIC VECTORS; HIV-1; HUMANS; HYDROCARBONS; MAGNETIC RESONANCE IMAGING; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; TRANSFECTION; VIRION; VIRUS ASSEMBLY;

EID: 79955486153     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-8-28     Document Type: Article

References (102)

1. Briggs JA, Wilk T, Welker R, Krausslich HG, Fuller SD. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J 2003, 22:1707-1715. 10.1093/emboj/cdg143, 152888, 12660176.
2. Briggs JA, Grunewald K, Glass B, Forster F, Krausslich HG, Fuller SD. The mechanism of HIV-1 core assembly: insights from three-dimensional reconstructions of authentic virions. Structure 2006, 14:15-20. 10.1016/j.str.2005.09.010, 16407061.
3. Li S, Hill CP, Sundquist WI, Finch JT. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 2000, 407:409-413. 10.1038/35030177, 11014200.
4. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI. Assembly and analysis of conical models for the HIV-1 core. Science 1999, 283:80-83. 10.1126/science.283.5398.80, 9872746.
5. Ganser-Pornillos BK, Cheng A, Yeager M. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 2007, 131:70-79. 10.1016/j.cell.2007.08.018, 17923088.
6. Ganser-Pornillos BK, Yeager M, Sundquist WI. The structural biology of HIV assembly. Curr Opin Struct Biol 2008, 18:203-217. 10.1016/j.sbi.2008.02.001, 2819415, 18406133.
7. Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, Stout CD, Sundquist WI, Hill CP, Yeager M. X-ray structures of the hexameric building block of the HIV capsid. Cell 2009, 137:1282-1292. 10.1016/j.cell.2009.04.063, 2840706, 19523676.
8. Ako-Adjei D, Johnson MC, Vogt VM. The retroviral capsid domain dictates virion size, morphology, and coassembly of gag into virus-like particles. J Virol 2005, 79:13463-13472. 10.1128/JVI.79.21.13463-13472.2005, 1262573, 16227267.
9. Pornillos O, Ganser-Pornillos BK, Yeager M. Atomic-level modelling of the HIV capsid. Nature 2011, 469:424-427. 10.1038/nature09640, 21248851.
10. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J Virol 2003, 77:5439-5450. 10.1128/JVI.77.9.5439-5450.2003, 153941, 12692245.
11. Abdurahman S, Hoglund S, Goobar-Larsson L, Vahlne A. Selected amino acid substitutions in the C-terminal region of human immunodeficiency virus type 1 capsid protein affect virus assembly and release. J Gen Virol 2004, 85:2903-2913. 10.1099/vir.0.80137-0, 15448352.
12. Chien AI, Liao WH, Yang DM, Wang CT. A domain directly C-terminal to the major homology region of human immunodeficiency type 1 capsid protein plays a crucial role in directing both virus assembly and incorporation of Gag-Pol. Virol 2006, 348:84-95.
13. Douglas CC, Thomas D, Lanman J, Prevelige PE. Investigation of N-terminal domain charged residues on the assembly and stability of HIV-1 CA. Biochemistry 2004, 43:10435-10441. 10.1021/bi049359g, 15301542.
14. Forshey BM, von Schwedler UK, Sundquist WI, Aiken C. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J Virol 2002, 76:5667-5677. 10.1128/JVI.76.11.5667-5677.2002, 137032, 11991995.
15. Ganser-Pornillos BK, von Schwedler UK, Stray KM, Aiken C, Sundquist WI. Assembly properties of the human immunodeficiency virus type 1 CA protein. J Virol 2004, 78:2545-2552. 10.1128/JVI.78.5.2545-2552.2004, 369201, 14963157.
16. Joshi A, Nagashima K, Freed EO. Mutation of dileucine-like motifs in the human immunodeficiency virus type 1 capsid disrupts virus assembly, gag-gag interactions, gag-membrane binding, and virion maturation. J Virol 2006, 80:7939-7951. 10.1128/JVI.00355-06, 1563813, 16873251.
17. del Alamo M, Mateu MG. Electrostatic repulsion, compensatory mutations, and long-range non-additive effects at the dimerization interface of the HIV capsid protein. J Mol Biol 2005, 345:893-906. 10.1016/j.jmb.2004.10.086, 15588834.
18. Scholz I, Arvidson B, Huseby D, Barklis E. Virus particle core defects caused by mutations in the human immunodeficiency virus capsid N-terminal domain. J Virol 2005, 79:1470-1479. 10.1128/JVI.79.3.1470-1479.2005, 544128, 15650173.
19. Chang YF, Wang SM, Huang KJ, Wang CT. Mutations in capsid major homology region affect assembly and membrane affinity of HIV-1 Gag. J Mol Biol 2007, 370:585-597. 10.1016/j.jmb.2007.05.020, 17532005.
20. Abdurahman S, Hoglund S, Hoglund A, Vahlne A. Mutation in the loop C-terminal to the cyclophilin A binding site of HIV-1 capsid protein disrupts proper virus assembly and infectivity. Retrovirology 2007, 4:19. 10.1186/1742-4690-4-19, 1832212, 17371591.
21. Abdurahman S, Youssefi M, Hoglund S, Vahlne A. Characterization of the invariable residue 51 mutations of human immunodeficiency virus type 1 capsid protein on in vitro CA assembly and infectivity. Retrovirology 2007, 4:69. 10.1186/1742-4690-4-69, 2064932, 17903253.
22. Vogt VM. Blocking HIV-1 virus assembly. Nat Struct Mol Biol 2005, 12:638-639. 10.1038/nsmb0805-638, 16077724.
23. Li F, Wild C. HIV-1 assembly and budding as targets for drug discovery. Curr Opin Investig Drugs 2005, 6:148-154.
24. Li J, Tang S, Hewlett I, Yang M. HIV-1 capsid protein and cyclophilin a as new targets for anti-AIDS therapeutic agents. Infect Disor Drug Targets 2007, 7:238-244.
25. Adamson CS, Freed EO. Novel approaches to inhibiting HIV-1 replication. Antiviral Res 2010, 85:119-141. 10.1016/j.antiviral.2009.09.009, 2815006, 19782103.
26. Blair WS, Pickford C, Irving SL, Brown DG, Anderson M, Bazin R, Cao J, Ciaramella G, Isaacson J, Jackson L, et al. HIV capsid is a tractable target for small molecule therapeutic intervention. PLoS Pathog 2010, 6:e1001220. 10.1371/journal.ppat.1001220, 3000358, 21170360.
27. Shi J, Zhou J, Shah VB, Aiken C, Whitby K. Small-molecule inhibition of human immunodeficiency virus type 1 infection by virus capsid destabilization. J Virol 2011, 85:542-549. 10.1128/JVI.01406-10, 20962083.
28. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, Hill CP. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 1996, 87:1285-1294. 10.1016/S0092-8674(00)81823-1, 8980234.
29. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 1993, 73:1067-1078. 10.1016/0092-8674(93)90637-6, 8513493.
30. Adamson CS, Jones IM. The molecular basis of HIV capsid assembly--five years of progress. Rev Med Virol 2004, 14:107-121. 10.1002/rmv.418, 15027003.
31. Mammano F, Ohagen A, Hoglund S, Gottlinger HG. Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J Virol 1994, 68:4927-4936. 236433, 8035491.
32. Strambio-de-Castillia C, Hunter E. Mutational analysis of the major homology region of Mason-Pfizer monkey virus by use of saturation mutagenesis. J Virol 1992, 66:7021-7032. 240357, 1279197.
33. Craven RC, Leure-duPree AE, Weldon RA, Wills JW. Genetic analysis of the major homology region of the Rous sarcoma virus Gag protein. J Virol 1995, 69:4213-4227. 189159, 7769681.
34. Willems L, Kerkhofs P, Attenelle L, Burny A, Portetelle D, Kettmann R. The major homology region of bovine leukaemia virus p24gag is required for virus infectivity in vivo. J Gen Virol 1997, 78(Pt 3):637-640.
35. Lokhandwala PM, Nguyen TL, Bowzard JB, Craven RC. Cooperative role of the MHR and the CA dimerization helix in the maturation of the functional retrovirus capsid. Virol 2008, 376:191-198.
36. Purdy JG, Flanagan JM, Ropson IJ, Rennoll-Bankert KE, Craven RC. Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J Virol 2008, 82:5951-5961. 10.1128/JVI.00214-08, 2395126, 18400856.
37. Provitera P, Goff A, Harenberg A, Bouamr F, Carter C, Scarlata S. Role of the major homology region in assembly of HIV-1 Gag. Biochemistry 2001, 40:5565-5572. 10.1021/bi002040l, 11331022.
38. Gamble TR, Yoo S, Vajdos FF, von Schwedler UK, Worthylake DK, Wang H, McCutcheon JP, Sundquist WI, Hill CP. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 1997, 278:849-853. 10.1126/science.278.5339.849, 9346481.
39. Momany C, Kovari LC, Prongay AJ, Keller W, Gitti RK, Lee BM, Gorbalenya AE, Tong L, McClure J, Ehrlich LS, et al. Crystal structure of dimeric HIV-1 capsid protein. Nat Struct Mol Biol 1996, 3:763-770.
40. Ivanov D, Tsodikov OV, Kasanov J, Ellenberger T, Wagner G, Collins T. Domain-swapped dimerization of the HIV-1 capsid C-terminal domain. Proc Natl Acad Sci USA 2007, 104:4353-4358. 10.1073/pnas.0609477104, 1838606, 17360528.
41. Worthylake DK, Wang H, Yoo S, Sundquist WI, Hill CP. Structures of the HIV-1 capsid protein dimerization domain at 2.6 A resolution. Acta Crystallogr D Biol Crystallogr 1999, 55:85-92. 10.1107/S0907444998007689, 10089398.
42. Mateu MG. Conformational stability of dimeric and monomeric forms of the C-terminal domain of human immunodeficiency virus-1 capsid protein. J Mol Biol 2002, 318:519-531. 10.1016/S0022-2836(02)00091-8, 12051856.
43. Adamson CS, Salzwedel K, Freed EO. Virus maturation as a new HIV-1 therapeutic target. Expert Opin Ther Targets 2009, 13:895-908. 10.1517/14728220903039714, 2737327, 19534569.
44. Fletcher S, Hamilton AD. Targeting protein-protein interactions by rational design: mimicry of protein surfaces. J R Soc Interface 2006, 3:215-233. 10.1098/rsif.2006.0115, 1578744, 16849232.
45. Yin H, Hamilton AD. Strategies for targeting protein-protein interactions with synthetic agents. Angew Chem Int Ed Engl 2005, 44:4130-4163. 10.1002/anie.200461786, 15954154.
46. Peczuh MW, Hamilton AD. Peptide and protein recognition by designed molecules. Chem Rev 2000, 100:2479-2494. 10.1021/cr9900026, 11749292.
47. Watt PM. Screening for peptide drugs from the natural repertoire of biodiverse protein folds. Nat Biotech 2006, 24:177-183.
48. Ernst JT, Kutzki O, Debnath AK, Jiang S, Lu H, Hamilton AD. Design of a protein surface antagonist based on alpha-helix mimicry: inhibition of gp41 assembly and viral fusion. Angew Chem Int Ed Engl 2002, 41:278-281. 10.1002/1521-3773(20020118)41:2<278::AID-ANIE278>3.0.CO;2-A, 12491408.
49. Fletcher S, Hamilton AD. Targeting protein-protein interactions by rational design: mimicry of protein surfaces. J R Soc Interf 2006, 3:215-233.
50. Fletcher S, Hamilton AD. Protein-protein interaction inhibitors: small molecules from screening techniques. Curr Top Med Chem 2007, 7:922-927. 10.2174/156802607780906735, 17508923.
51. Arkin MR, Randal M, DeLano WL, Hyde J, Luong TN, Oslob JD, Raphael DR, Taylor L, Wang J, McDowell RS, et al. Binding of small molecules to an adaptive protein-protein interface. Proc Natl Acad Sci USA 2003, 100:1603-1608. 10.1073/pnas.252756299, 149879, 12582206.
52. Arkin MR, Wells JA. Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 2004, 3:301-317. 10.1038/nrd1343, 15060526.
53. Zhao L, O'Reilly MK, Shultz MD, Chmielewski J. Interfacial peptide inhibitors of HIV-1 integrase activity and dimerization. Bioorg Med Chem Lett 2003, 13:1175-1177. 10.1016/S0960-894X(03)00040-4, 12643937.
54. Maroun RG, Gayet S, Benleulmi MS, Porumb H, Zargarian L, Merad H, Leh H, Mouscadet JF, Troalen F, Fermandjian S. Peptide inhibitors of HIV-1 integrase dissociate the enzyme oligomers. Biochemistry 2001, 40:13840-13848. 10.1021/bi011328n, 11705373.
55. McPhee F, Good AC, Kuntz ID, Craik CS. Engineering human immunodeficiency virus 1 protease heterodimers as macromolecular inhibitors of viral maturation. Proc Natl Acad Sci USA 1996, 93:11477-11481. 10.1073/pnas.93.21.11477, 56635, 8876160.
56. Divita G, Baillon JG, Rittinger K, Chermann JC, Goody RS. Interface Peptides as Structure-based Human Immunodeficiency Virus Reverse Transcriptase Inhibitors. J Biol Chem 1995, 270:28642-28646. 10.1074/jbc.270.48.28642, 7499382.
57. Byeon IJ, Meng X, Jung J, Zhao G, Yang R, Ahn J, Shi J, Concel J, Aiken C, Zhang P, et al. Structural convergence between Cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function. Cell 2009, 139:780-790. 10.1016/j.cell.2009.10.010, 2782912, 19914170.
58. Ternois F, Sticht J, Duquerroy S, Krausslich HG, Rey FA. The HIV-1 capsid protein C-terminal domain in complex with a virus assembly inhibitor. Nat Struct Mol Biol 2005, 12:678-682. 10.1038/nsmb967, 16041386.
59. Zhang H, Bhattacharya S, Tong X, Waheed AA, Hong A, Heck S, Curreli F, Goger M, Cowburn D, Freed EO, et al. A Cell-penetrating Helical Peptide as a Potential HIV-1 Inhibitor. J Mol Biol 2008, 378:565-580. 10.1016/j.jmb.2008.02.066, 2695608, 18374356.
60. Walensky LD, Kung AL, Escher I, Malia TJ, Barbuto S, Wright RD, Wagner G, Verdine GL, Korsmeyer SJ. Activation of Apoptosis in Vivo by a Hydrocarbon-Stapled BH3 Helix. Science 2004, 305:1466-1470. 10.1126/science.1099191, 1360987, 15353804.
61. Schafmeister CE, Po J, Verdine GL. An All-Hydrocarbon Cross-Linking System for Enhancing the Helicity and Metabolic Stability of Peptides. J Am Chem Soc 2000, 122:5891-5892.
62. Moellering RE, Cornejo M, Davis TN, Bianco CD, Aster JC, Blacklow SC, Kung AL, Gilliland DG, Verdine GL, Bradner JE. Direct inhibition of the NOTCH transcription factor complex. Nature 2009, 462:182-188. 10.1038/nature08543, 2951323, 19907488.
63. Arora PS, Ansari AZ. Chemical biology: A Notch above other inhibitors. Nature 2009, 462:171-173. 10.1038/462171a, 19907487.
64. Wong HC, Shin R, Krishna NR. Solution structure of a double mutant of the carboxy-terminal dimerization domain of the HIV-1 capsid protein. Biochemistry 2008, 47:2289-2297. 10.1021/bi7022128, 18220423.
65. Garzon MT, Lidon-Moya MC, Barrera FN, Prieto A, Gomez J, Mateu MG, Neira JL. The dimerization domain of the HIV-1 capsid protein binds a capsid protein-derived peptide: a biophysical characterization. Protein Sci 2004, 13:1512-1523. 10.1110/ps.03555304, 2279969, 15152086.
66. Bartonova V, Igonet S, Sticht J, Glass B, Habermann A, Vaney MC, Sehr P, Lewis J, Rey FA, Krausslich HG. Residues in the HIV-1 Capsid Assembly Inhibitor Binding Site Are Essential for Maintaining the Assembly-competent Quaternary Structure of the Capsid Protein. J Biol Chem 2008, 283:32024-32033. 10.1074/jbc.M804230200, 18772135.
67. Freed EO, Martin MA. Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type 1 envelope glycoprotein gp120. J Virol 1994, 68:2503-2512. 236728, 8139032.
68. Gross I, Hohenberg H, Krausslich HG. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur J Biochem 1997, 249:592-600. 10.1111/j.1432-1033.1997.t01-1-00592.x, 9370371.
69. Cervia JS, Smith MA. Enfuvirtide (T-20): a novel human immunodeficiency virus type 1 fusion inhibitor. Clin Infect Dis 2003, 37:1102-1106. 10.1086/378302, 14523775.
70. Hanna L. T-20: first of a new class of anti-HIV drugs. BETA 1999, 12:7-8.
71. James JS. T-20: entirely new antiretroviral. AIDS Treat News 1997, 5-6.
72. Lazzarin A. Enfuvirtide: the first HIV fusion inhibitor. Expert Opin Pharmacother 2005, 6:453-464. 10.1517/14656566.6.3.453, 15794736.
73. 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, 72:2855-2864. 109730, 9525605.
74. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. Emergence of Resistant Human Immunodeficiency Virus Type 1 in Patients Receiving Fusion Inhibitor (T-20) Monotherapy. Antimicrob Agents Chemother 2002, 46:1896-1905. 10.1128/AAC.46.6.1896-1905.2002, 127242, 12019106.
75. Brun S, Solignat M, Gay B, Bernard E, Chaloin L, Fenard D, Devaux C, Chazal N, Briant L. VSV-G pseudotyping rescues HIV-1 CA mutations that impair core assembly or stability. Retrovirology 2008, 5:57. 10.1186/1742-4690-5-57, 2474847, 18605989.
76. Bernal F, Tyler AF, Korsmeyer SJ, Walensky LD, Verdine GL. Reactivation of the p53 Tumor Suppressor Pathway by a Stapled p53 Peptide. J Am Chem Soc 2007, 129:2456-2457. 10.1021/ja0693587, 17284038.
77. Walensky LD, Pitter K, Morash J, Oh KJ, Barbuto S, Fisher J, Smith E, Verdine GL, Korsmeyer SJ. A Stapled BID BH3 Helix Directly Binds and Activates BAX. Molecular Cell 2006, 24:199-210. 10.1016/j.molcel.2006.08.020, 17052454.
78. del Alamo M, Neira JL, Mateu MG. Thermodynamic dissection of a low affinity protein-protein interface involved in human immunodeficiency virus assembly. J Biol Chem 2003, 278:27923-27929. 10.1074/jbc.M304466200, 12761222.
79. Walensky LD, Pitter K, Morash J, Oh KJ, Barbuto S, Fisher J, Smith E, Verdine GL, Korsmeyer SJ. A Stapled BID BH3 Helix Directly Binds and Activates BAX. Molecular Cell 2006, 24:199-210. 10.1016/j.molcel.2006.08.020, 17052454.
80. Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, Krausslich HG. Structure and assembly of immature HIV. Proc Natl Acad Sci USA 2009, 106:11090-11095. 10.1073/pnas.0903535106, 2700151, 19549863.
81. Tang C, Loeliger E, Kinde I, Kyere S, Mayo K, Barklis E, Sun Y, Huang M, Summers MF. Antiviral inhibition of the HIV-1 capsid protein. J Mol Biol 2003, 327:1013-1020. 10.1016/S0022-2836(03)00289-4, 12662926.
82. Roldan A, Russell RS, Marchand B, Gotte M, Liang C, Wainberg MA. In vitro identification and characterization of an early complex linking HIV-1 genomic RNA recognition and Pr55Gag multimerization. J Biol Chem 2004, 279:39886-39894. 10.1074/jbc.M405632200, 15247214.
83. Favier A, Brutscher B, Blackledge M, Galinier A, Deutscher J, Penin F, Marion D. Solution structure and dynamics of Crh, the Bacillus subtilis catabolite repression HPr. J Mol Biol 2002, 317:131-144. 10.1006/jmbi.2002.5397, 11916384.
84. Clore GM, Gronenborn AM. Three-dimensional structures of alpha and beta chemokines. Faseb J 1995, 9:57-62.
85. Sticht J, Humbert M, Findlow S, Bodem J, Muller B, Dietrich U, Werner J, Krausslich HG. A peptide inhibitor of HIV-1 assembly in vitro. Nat Struct Mol Biol 2005, 12:671-677. 10.1038/nsmb964, 16041387.
86. Wright ER, Schooler JB, Ding HJ, Kieffer C, Fillmore C, Sundquist WI, Jensen GJ. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J 2007, 26:2218-2226. 10.1038/sj.emboj.7601664, 1852790, 17396149.
87. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, Julias JG, Vandegraaff N, Baumann JG, Wang R, Yuen W, et al. Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 2010, 7:221-233. 10.1016/j.chom.2010.02.007, 2841689, 20227665.
88. Thys W, De HS, Demeulemeester J, Taltynov O, Vancraenenbroeck R, Gerard M, De RJ, Gijsbers R, Christ F, Debyser Z. Interplay between HIV Entry and Transportin-SR2 Dependency. Retrovirology 2011, 8:7. 10.1186/1742-4690-8-7, 3041740, 21276267.
89. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 1986, 59:284-291. 253077, 3016298.
90. Patnaik A, Chau V, Li F, Montelaro RC, Wills JW. Budding of Equine Infectious Anemia Virus Is Insensitive to Proteasome Inhibitors. J Virol 2002, 76:2641-2647. 10.1128/JVI.76.6.2641-2647.2002, 135976, 11861830.
91. Shehu-Xhilaga M, Ablan S, Demirov DG, Chen C, Montelaro RC, Freed EO. Late Domain-Dependent Inhibition of Equine Infectious Anemia Virus Budding. J Virol 2004, 78:724-732. 10.1128/JVI.78.2.724-732.2004, 368837, 14694104.
92. Naldini L, Blomer U, Gage FH, Trono D, Verma IM. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci USA 1996, 93:11382-11388. 10.1073/pnas.93.21.11382, 38066, 8876144.
93. Huang M, Orenstein JM, Martin MA, Freed EO. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J Virol 1995, 69:6810-6818. 189593, 7474093.
94. Huseby D, Barklis RL, Alfadhli A, Barklis E. Assembly of human immunodeficiency virus precursor gag proteins. J Biol Chem 2005, 280:17664-17670.
95. Ehrlich LS, Liu T, Scarlata S, Chu B, Carter CA. HIV-1 capsid protein forms spherical (immature-like) and tubular (mature-like) particles in vitro: structure switching by pH-induced conformational changes. Biophys J 2001, 81:586-594. 10.1016/S0006-3495(01)75725-6, 1301537, 11423440.
96. McPhail D, Cooper A. Thermodynamics and kinetics of dissociation of ligand-induced dimers of vancomycin antibiotics. J Chem Soc, Faraday Trans 1997, 93:2283-2289.
97. Lovatt M, Cooper A, Camilleri P. Energetics of cyclodextrin-induced dissociation of insulin. Eur Biophys J 1996, 24:354-357.
98. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 2002, 46:1896-1905. 10.1128/AAC.46.6.1896-1905.2002, 127242, 12019106.
99. Freed EO, Martin MA. Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix. J Virol 1995, 69:1984-1989. 188822, 7853546.
100. Yee JK, Friedmann T, Burns JC. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol 1994, 43:99-112.
101. Jiang SB, Lin K, Neurath AR. Enhancement of human immunodeficiency virus type 1 infection by antisera to peptides from the envelope glycoproteins gp120/gp41. J Exp Med 1991, 174:1557-1563. 10.1084/jem.174.6.1557, 2119057, 1836013.
102. Jiang S, Lu H, Liu S, Zhao Q, He Y, Debnath AK. N-substituted pyrrole derivatives as novel human immunodeficiency virus type 1 entry inhibitors that interfere with the gp41 six-helix bundle formation and block virus fusion. Antimicrob Agents Chemother 2004, 48:4349-4359. 10.1128/AAC.48.11.4349-4359.2004, 525433, 15504864.