ADS-J1 inhibits HIV-1 infection and membrane fusion by targeting the highly conserved pocket in the gp41 NHR-trimer

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 5, 2014, Pages 1296-1305

  Yu, Fei ^a,b,c   Lu, Lu ^b   Liu, Qi ^b   Yu, Xiaowen ^c   Wang, Lili ^c   He, Elaine ^c   Zou, Peng ^c   Du, Lanying ^c   Sanders, Rogier W ^d,e   Liu, Shuwen ^a   Jiang, Shibo ^a,b,c  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c NEW YORK BLOOD CENTER   (United States)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

gp41; HIV fusion inhibitor; HIV 1; Mutation; Pocket; Six helix bundle

Indexed keywords

ADS J 1; ANTIVIRUS AGENT; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; T2635 PEPTIDE; UNCLASSIFIED DRUG; ZIDOVUDINE;

AMINO TERMINAL SEQUENCE; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; DRUG PROTEIN BINDING; DRUG TARGETING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IC 50; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; VIRUS MUTANT; VIRUS MUTATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

GP41; HIV FUSION INHIBITOR; HIV-1; MUTATION; POCKET; SIX-HELIX BUNDLE;

AMINO ACID SEQUENCE; HIV ENVELOPE PROTEIN GP41; HIV FUSION INHIBITORS; HIV INFECTIONS; HIV-1; HUMANS; MEMBRANE FUSION; MOLECULAR SEQUENCE DATA; MUTATION; NAPHTHALENESULFONATES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; TRIAZINES;

EID: 84894601292     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.12.022     Document Type: Article

References (43)

1. C.G. Anastassopoulou, T.J. Ketas, R.S. Depetris, A.M. Thomas, P.J. Klasse, and J.P. Moore Resistance of a human immunodeficiency virus type 1 isolate to a small molecule CCR5 inhibitor can involve sequence changes in both gp120 and gp41 Virology 413 2011 47 59
2. C.G. Anastassopoulou, T.J. Ketas, P.J. Klasse, and J.P. Moore Resistance to CCR5 inhibitors caused by sequence changes in the fusion peptide of HIV-1 gp41 Proc. Natl. Acad. Sci. U. S. A. 106 2009 5318 5323
3. M. Armand-Ugon, I. Clotet-Codina, C. Tintori, F. Manetti, B. Clotet, M. Botta, and J.A. Este The anti-HIV activity of ADS-J1 targets the HIV-1 gp120 Virology 343 2005 141 149
4. C.E. Baldwin, R.W. Sanders, Y. Deng, S. Jurriaans, J.M. Lange, M. Lu, and B. Berkhout Emergence of a drug-dependent human immunodeficiency virus type 1 variant during therapy with the T20 fusion inhibitor J. Virol. 78 2004 12428 12437
5. D.C. Chan, C.T. Chutkowski, and P.S. Kim Evidence that a prominent cavity in the coiled coil of HIV type 1 gp41 is an attractive drug target Proc. Natl. Acad. Sci. U. S. A. 95 1998 15613 15617
6. D.C. Chan, D. Fass, J.M. Berger, and P.S. Kim Core structure of gp41 from the HIV envelope glycoprotein Cell 89 1997 263 273
7. D.C. Chan, and P.S. Kim HIV entry and its inhibition Cell 93 1998 681 684
8. X. Chen, L. Lu, Z. Qi, H. Lu, J. Wang, X. Yu, Y. Chen, and S. Jiang Novel recombinant engineered gp41 N-terminal heptad repeat trimers and their potential as anti-HIV-1 therapeutics or microbicides J. Biol. Chem. 285 2010 25506 25515
9. A.K. Debnath, L. Radigan, and S. Jiang Structure-based identification of small molecule antiviral compounds targeted to the gp41 core structure of the human immunodeficiency virus type 1 J. Med. Chem. 42 1999 3203 3209
10. J.J. Dwyer, K.L. Wilson, D.K. Davison, S.A. Freel, J.E. Seedorff, S.A. Wring, N.A. Tvermoes, T.J. Matthews, M.L. Greenberg, and M.K. Delmedico Design of helical, oligomeric HIV-1 fusion inhibitor peptides with potent activity against enfuvirtide-resistant virus Proc. Natl. Acad. Sci. U. S. A. 104 2007 12772 12777
11. D.M. Eckert, V.N. Malashkevich, L.H. Hong, P.A. Carr, and P.S. Kim Inhibiting HIV-1 entry: discovery of d-peptide inhibitors that target the gp41 coiled-coil pocket Cell 99 1999 103 115
12. D. Eggink, I. Bontjer, J.P. Langedijk, B. Berkhout, and R.W. Sanders Resistance of human immunodeficiency virus type 1 to a third-generation fusion inhibitor requires multiple mutations in gp41 and is accompanied by a dramatic loss of gp41 function J. Virol. 85 2011 10785 10797
13. D. Eggink, J.P. Langedijk, A.M. Bonvin, Y. Deng, M. Lu, B. Berkhout, and R.W. Sanders Detailed mechanistic insights into HIV-1 sensitivity to three generations of fusion inhibitors J. Biol. Chem. 284 2009 26941 26950
14. E. Gonzalez-Ortega, M.P. Mena, M. Permanyer, E. Ballana, B. Clotet, and J.A. Este ADS-J1 inhibits HIV-1 entry by interacting with gp120 and does not block fusion-active gp41 core formation Antimicrob. Agents Chemother. 54 2010 4487 4492
15. Y. He, J. Cheng, H. Lu, J. Li, J. Hu, Z. Qi, Z. Liu, S. Jiang, and Q. Dai Potent HIV fusion inhibitors against Enfuvirtide-resistant HIV-1 strains Proc. Natl. Acad. Sci. U. S. A. 105 2008 16332 16337
16. E. Helseth, U. Olshevsky, C. Furman, and J. Sodroski Human immunodeficiency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein J. Virol. 65 1991 2119 2123
17. H. Ji, W. Shu, T. Burling, S. Jiang, and M. Lu Inhibition of HIV-1 infectivity by the gp41 core: role of a conserved hydrophobic cavity in membrane fusion J. Virol. 73 1999 8578 8586
18. S. Jiang, K. Lin, N. Strick, and A.R. Neurath HIV-1 inhibition by a peptide Nature 365 1993 113
19. S. Jiang, K. Lin, L. Zhang, and A.K. Debnath A screening assay for antiviral compounds targeted to the HIV-1 gp41 core structure using a conformation-specific monoclonal antibody J. Virol. Methods 80 1999 85 96
20. S. Jiang, P. Siddiqui, and S. Liu Blocking viral entry: a complementary strategy for HIV therapy Drug Discovery Today 1 2004 497 503
21. S. Jiang, Q. Zhao, and A.K. Debnath Peptide and non-peptide HIV fusion inhibitors Curr. Pharm. Des. 8 2002 563 580
22. J.P. Julien, A. Cupo, D. Sok, R.L. Stanfield, D. Lyumkis, M.C. Deller, P.J. Klasse, D.R. Burton, R.W. Sanders, J.P. Moore, A.B. Ward, and I.A. Wilson Crystal structure of a soluble cleaved HIV-1 envelope trimer Science 342 2013 1477 1483
23. J.M. Kilby, S. Hopkins, T.M. Venetta, B. DiMassimo, G.A. Cloud, J.Y. Lee, L. Alldredge, E. Hunter, D. Lambert, D. Bolognesi, T. Matthews, M.R. Johnson, M.A. Nowak, G.M. Shaw, and M.S. Saag Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry Nat. Med. 4 1998 1302 1307
24. S. Liu, L. Boyer-Chatenet, H. Lu, and S. Jiang Rapid and automated fluorescence-linked immunosorbent assay for high throughput screening of HIV-1 fusion inhibitors targeting gp41 J. Biomol. Screen. 8 2003 685 693
25. S. Liu, and S. Jiang High throughput screening and characterization of HIV-1 entry inhibitors targeting gp41: theories and techniques Curr. Pharm. Des. 10 2004 1827 1843
26. S. Liu, W. Jing, B. Cheung, H. Lu, J. Sun, X. Yan, J. Niu, J. Farmar, S. Wu, and S. Jiang HIV gp41 C-terminal heptad repeat contains multifunctional domains: relation to mechanisms of action of anti-HIV peptides J. Biol. Chem. 282 2007 9612 9620
27. S. Liu, H. Lu, Y. Xu, S. Wu, and S. Jiang Different from the HIV fusion inhibitor C34, the anti-HIV drug Fuzeon (T-20) inhibits HIV-1 entry by targeting multiple sites in gp41 and gp120 J. Biol. Chem. 280 2005 11259 11273
28. S. Liu, S. Wu, and S. Jiang HIV entry inhibitors targeting gp41: from polypeptides to small-molecule compounds Curr. Pharm. Des. 13 2007 143 162
29. S. Liu, Q. Zhao, and S. Jiang Determination of the HIV-1 gp41 postfusion conformation modeled by synthetic peptides: applicable for identification of the HIV-1 fusion inhibitors Peptide 24 2003 1303 1313
30. L. Lu, P. Tong, X. Yu, C. Pan, P. Zou, Y.H. Chen, and S. Jiang HIV-1 variants with a single-point mutation in the gp41 pocket region exhibiting different susceptibility to HIV fusion inhibitors with pocket- or membrane-binding domain Biochim. Biophys. Acta 1818 2012 2950 2957
31. M. Lu, S.C. Blacklow, and P.S. Kim A trimeric structural domain of the HIV-1 transmembrane glycoprotein Nat. Struct. Biol. 2 1995 1075 1082
32. M. Lu, and P.S. Kim A trimeric structural subdomain of the HIV-1 transmembrane glycoprotein J. Biomol. Struct. Dyn. 15 1997 465 471
33. M. Mink, S.M. Mosier, S. Janumpalli, D. Davison, L. Jin, T. Melby, P. Sista, J. Erickson, D. Lambert, S.A. Stanfield-Oakley, M. Salgo, N. Cammack, T. Matthews, and M.L. Greenberg Impact of human immunodeficiency virus type 1 gp41 amino acid substitutions selected during enfuvirtide treatment on gp41 binding and antiviral potency of enfuvirtide in vitro J. Virol. 79 2005 12447 12454
34. H. Mo, A.K. Konstantinidis, K.D. Stewart, T. Dekhtyar, T. Ng, K. Swift, E.D. Matayoshi, W. Kati, W. Kohlbrenner, and A. Molla Conserved residues in the coiled-coil pocket of human immunodeficiency virus type 1 gp41 are essential for viral replication and interhelical interaction Virology 329 2004 319 327
35. K. Papanikolopoulou, V. Forge, P. Goeltz, and A. Mitraki Formation of highly stable chimeric trimers by fusion of an adenovirus fiber shaft fragment with the foldon domain of bacteriophage T4 fibritin J. Biol. Chem. 279 2004 8991 8998
36. N. Ray, L.A. Blackburn, and R.W. Doms HR-2 mutations in human immunodeficiency virus type 1 gp41 restore fusion kinetics delayed by HR-1 mutations that cause clinical resistance to enfuvirtide J. Virol. 83 2009 2989 2995
37. J.D. Reeves, S.A. Gallo, N. Ahmad, J.L. Miamidian, P.E. Harvey, M. Sharron, S. Pohlmann, J.N. Sfakianos, C.A. Derdeyn, R. Blumenthal, E. Hunter, and R.W. Doms Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics Proc. Natl. Acad. Sci. U. S. A. 99 2002 16249 16252
38. H. Wang, Z. Qi, A. Guo, Q. Mao, H. Lu, X. An, C. Xia, X. Li, A.K. Debnath, S. Wu, S. Liu, and S. Jiang ADS-J1 inhibits HIV-1 entry by interacting with the gp41 pocket region and blocking the fusion-active gp41 core formation Antimicrob. Agents Chemother. 53 2009 4987 4998
39. X. Wei, J.M. Decker, H. Liu, Z. Zhang, R.B. Arani, J.M. Kilby, M.S. Saag, X. Wu, G.M. Shaw, and J.C. Kappes Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy Antimicrob. Agents Chemother. 46 2002 1896 1905
40. W. Weissenhorn, A. Dessen, S.C. Harrison, J.J. Skehel, and D.C. Wiley Atomic structure of the ectodomain from HIV-1 gp41 Nature 387 1997 426 428
41. C.T. Wild, D.C. Shugars, T.K. Greenwell, C.B. McDanal, and T.J. Matthews Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection Proc. Natl. Acad. Sci. U. S. A. 91 1994 9770 9774
42. L. Xu, A. Pozniak, A. Wildfire, S.A. Stanfield-Oakley, S.M. Mosier, D. Ratcliffe, J. Workman, A. Joall, R. Myers, E. Smit, P.A. Cane, M.L. Greenberg, and D. Pillay Emergence and evolution of enfuvirtide resistance following long-term therapy involves heptad repeat 2 mutations within gp41 Antimicrob. Agents Chemother. 49 2005 1113 1119
43. X. Yu, L. Lu, L. Cai, P. Tong, S. Tan, P. Zou, F. Meng, Y.H. Chen, and S. Jiang Mutations of Gln64 in the HIV-1 gp41 N-terminal heptad repeat render viruses resistant to peptide HIV fusion inhibitors targeting gp41 pocket J. Virol. 86 2012 589 593