Mechanism of resistance to S138A substituted enfuvirtide and its application to peptide design

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 4, 2013, Pages 908-915

  Izumi, Kazuki ^a   Kawaji, Kumi ^b   Miyamoto, Fusasko ^b   Shimane, Kazuki ^a   Shimura, Kazuya ^a   Sakagami, Yasuko ^a   Hattori, Toshio ^b   Watanabe, Kentaro ^a   Oishi, Shinya ^a   Fujii, Nobutaka ^a   Matsuoka, Masao ^a   Kaku, Mitsuo ^b   Sarafianos, Stefan G ^c   Kodama, Eiichi N ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c University of Missouri   (United States)

Author keywords

Fusion inhibitor; gp41; HIV 1; Mutation; Resistance; T 20

Indexed keywords

ENFUVIRTIDE; GLYCOPROTEIN GP 41;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; BINDING AFFINITY; CD34 SELECTION; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS RESISTANCE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MECHANICS; NONHUMAN; VIRUS MUTATION; VIRUS REPLICATION; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; DRUG DESIGN; DRUG RESISTANCE, VIRAL; HEK293 CELLS; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE FRAGMENTS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84874686077     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.01.015     Document Type: Article

References (50)

1. S. Aquaro, R. D'Arrigo, V. Svicher, G.D. Perri, S.L. Caputo, and U. Visco-Comandini Specific mutations in HIV-1 gp41 are associated with immunological success in HIV-1-infected patients receiving enfuvirtide treatment Journal of Antimicrobial Chemotherapy 58 2006 714 722
2. M. Armand-Ugon, A. Gutierrez, B. Clotet, and J.A. Este HIV-1 resistance to the gp41-dependent fusion inhibitor C-34 Antiviral Research 59 2003 137 142
3. X. Bai, K.L. Wilson, J.E. Seedorff, D. Ahrens, J. Green, and D.K. Davison Impact of the enfuvirtide resistance mutation N43D and the associated baseline polymorphism E137K on peptide sensitivity and six-helix bundle structure Biochemistry 47 2008 6662 6670
4. C.E. Baldwin, R.W. Sanders, Y. Deng, S. Jurriaans, J.M. Lange, and M. Lu Emergence of a drug-dependent human immunodeficiency virus type 1 variant during therapy with the T20 fusion inhibitor Journal of Virology 78 2004 12428 12437
5. E. Bianchi, M. Finotto, P. Ingallinella, R. Hrin, A.V. Carella, and X.S. Hou Covalent stabilization of coiled coils of the HIV gp41N region yields extremely potent and broad inhibitors of viral infection Proceedings of the National Academy of Sciences of the United States of America 102 2005 12903 12908
6. C. Cabrera, S. Marfil, E. Garcia, J. Martinez-Picado, A. Bonjoch, and M. Bofill Genetic evolution of gp41 reveals a highly exclusive relationship between codons 36, 38 and 43 in gp41 under long-term enfuvirtide-containing salvage regimen AIDS 20 2006 2075 2080
7. R.M. Cardoso, F.M. Brunel, S. Ferguson, M. Zwick, D.R. Burton, and P.E. Dawson Structural basis of enhanced binding of extended and helically constrained peptide epitopes of the broadly neutralizing HIV-1 antibody 4E10 Journal of Molecular Biology 365 2007 1533 1544
8. R. Carmona, L. Perez-Alvarez, M. Munoz, G. Casado, E. Delgado, and M. Sierra Natural resistance-associated mutations to enfuvirtide (T20) and polymorphisms in the gp41 region of different HIV-1 genetic forms from T20 naive patients Journal of Clinical Virology 32 2005 248 253
9. 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 Proceedings of the National Academy of Sciences of the United States of America 95 1998 15613 15617
10. 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
11. R. Chinnadurai, D. Rajan, J. Munch, and F. Kirchhoff Human immunodeficiency virus type 1 variants resistant to first- and second-version fusion inhibitors and cytopathic in ex vivo human lymphoid tissue Journal of Virology 81 2007 6563 6572
12. T. Cilliers, T. Patience, C. Pillay, M. Papathanasopoulos, and L. Morris Sensitivity of HIV type 1 subtype C isolates to the entry inhibitor T-20 AIDS Research and Human Retroviruses 20 2004 477 482
13. 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 Journal of Medicinal Chemistry 42 1999 3203 3209
14. J.J. Dwyer, K.L. Wilson, D.K. Davison, S.A. Freel, J.E. Seedorff, and S.A. Wring Design of helical, oligomeric HIV-1 fusion inhibitor peptides with potent activity against enfuvirtide-resistant virus Proceedings of the National Academy of Sciences of the United States of America 104 2007 12772 12777
15. J.J. Dwyer, K.L. Wilson, K. Martin, J.E. Seedorff, A. Hasan, and R.J. Medinas Design of an engineered N-terminal HIV-1 gp41 trimer with enhanced stability and potency Protein Science 17 2008 633 643
16. D. Eggink, C.E. Baldwin, Y. Deng, J.P. Langedijk, M. Lu, and R.W. Sanders Selection of T1249-resistant human immunodeficiency virus type 1 variants Journal of Virology 82 2008 6678 6688
17. 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 Journal of Virology 85 2011 10785 10797
18. S.H. Eshleman, S.E. Hudelson, R. Bruce, T. Lee, M.R. Owens, and J. Hackett Analysis of HIV type 1 gp41 sequences in diverse HIV type 1 strains AIDS Research and Human Retroviruses 23 2007 1593 1598
19. V. Fikkert, P. Cherepanov, K. Van Laethem, A. Hantson, B. Van Remoortel, and C. Pannecouque env chimeric virus technology for evaluating human immunodeficiency virus susceptibility to entry inhibitors Antimicrobial Agents and Chemotherapy 46 2002 3954 3962
20. A. Hachiya, E.N. Kodama, S.G. Sarafianos, M.M. Schuckmann, Y. Sakagami, M. Matsuoka, M. Takiguchi, H. Gatanaga, and S. Oka Amino acid mutation N348I in the connection subdomain of human immunodeficiency virus type 1 reverse transcriptase confers multiclass resistance to nucleoside and nonnucleoside reverse transcriptase inhibitors Jouranl of Virology 82 2008 3261 3270
21. A. Hachiya, B. Marchand, K.A. Kirby, E. Michailidis, X. Tu, K. Palczewski, Y.T. Ong, Z. Li, D.T. Griffin, M.M. Schuckmann, J. Tanuma, S. Oka, K. Singh, E.N. Kodama, and S.G. Sarafianos HIV-1 reverse transcriptase (RT) polymorphism 172K suppresses the effect of clinically relevant drug resistance mutations to both nucleoside and non-nucleoside RT inhibitors Journal of Biological Chemistry 287 2012 29988 29999
22. Y. He, Y. Xiao, H. Song, Q. Liang, D. Ju, and X. Chen Design and evaluation of sifuvirtide, a novel HIV-1 fusion inhibitor Journal of Biological Chemistry 283 2008 11126 11134
23. K. Izumi, E. Kodama, K. Shimura, Y. Sakagami, K. Watanabe, and S. Ito Design of peptide-based inhibitors for human immunodeficiency virus type 1 strains resistant to T-20 Journal of Biological Chemistry 284 2009 4914 4920
24. K. Izumi, S. Nakamura, H. Nakano, K. Shimura, Y. Sakagami, and S. Oishi Characterization of HIV-1 resistance to a fusion inhibitor, N36, derived from the gp41 amino-terminal heptad repeat Antiviral Research 87 2010 179 186
25. M.F. Kavlick, K. Wyvill, R. Yarchoan, and H. Mitsuya Emergence of multi-dideoxynucleoside-resistant human immunodeficiency virus type 1 variants, viral sequence variation, and disease progression in patients receiving antiretroviral chemotherapy Journal of Infectious Diseases 177 1998 1506 1513
26. J.M. Kilby, S. Hopkins, T.M. Venetta, B. DiMassimo, G.A. Cloud, and J.Y. Lee Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry Nature Medicine 4 1998 1302 1307
27. P. Kosalaraksa, M.F. Kavlick, V. Maroun, R. Le, and H. Mitsuya Comparative fitness of multi-dideoxynucleoside-resistant human immunodeficiency virus type 1 (HIV-1) in an In vitro competitive HIV-1 replication assay Jouranl of Virology 73 1999 5356 5363
28. C. Kuiken, B. Foley, T. Leitner, C. Apetrei, B. Hahn, and I. Mizrachi HIV sequence compendium 2010 2010 Los Alamos National Laboratory, Theoretical Biology and Biophysics Los Alamos, NM
29. B. Labrosse, J.L. Labernardiere, E. Dam, V. Trouplin, K. Skrabal, and F. Clavel Baseline susceptibility of primary human immunodeficiency virus type 1 to entry inhibitors Journal of Virology 77 2003 1610 1613
30. J.P. Lalezari, K. Henry, M. O'Hearn, J.S. Montaner, P.J. Piliero, and B. Trottier Enfuvirtide, an HIV-1 fusion inhibitor, for drug-resistant HIV infection in North and South America New England Journal of Medicine 348 2003 2175 2185
31. A. Lazzarin, B. Clotet, D. Cooper, J. Reynes, K. Arasteh, and M. Nelson Efficacy of enfuvirtide in patients infected with drug-resistant HIV-1 in Europe and Australia New England Journal of Medicine 348 2003 2186 2195
32. S. Lohrengel, F. Hermann, I. Hagmann, H. Oberwinkler, L. Scrivano, and C. Hoffmann Determinants of human immunodeficiency virus type 1 resistance to membrane-anchored gp41-derived peptides Journal of Virology 79 2005 10237 10246
33. M.R. Loutfy, J.M. Raboud, J.S. Montaner, T. Antoniou, B. Wynhoven, and F. Smaill Assay of HIV gp41 amino acid sequence to identify baseline variation and mutation development in patients with virologic failure on enfuvirtide Antiviral Research 75 2007 58 63
34. V.N. Malashkevich, D.C. Chan, C.T. Chutkowski, and P.S. Kim Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: conserved helical interactions underlie the broad inhibitory activity of gp41 peptides Proceedings of the National Academy of Sciences of the United States of America 95 1998 9134 9139
35. T. Melby, P. Sista, R. DeMasi, T. Kirkland, N. Roberts, and M. Salgo Characterization of envelope glycoprotein gp41 genotype and phenotypic susceptibility to enfuvirtide at baseline and on treatment in the phase III clinical trials TORO-1 and TORO-2 AIDS Research and Human Retroviruses 22 2006 375 385
36. M. Mink, S.M. Mosier, S. Janumpalli, D. Davison, L. Jin, and T. Melby 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 Journal of Virology 79 2005 12447 12454
37. D. Nameki, E. Kodama, M. Ikeuchi, N. Mabuchi, A. Otaka, and H. Tamamura Mutations conferring resistance to human immunodeficiency virus type 1 fusion inhibitors are restricted by gp41 and Rev-responsive element functions Journal of Virology 79 2005 764 770
38. H. Nishikawa, S. Nakamura, E. Kodama, S. Ito, K. Kajiwara, and K. Izumi Electrostatically constrained alpha-helical peptide inhibits replication of HIV-1 resistant to enfuvirtide International Journal of Biochemistry and Cell Biology 41 2009 891 899
39. S. Oishi, S. Ito, H. Nishikawa, K. Watanabe, M. Tanaka, and H. Ohno Design of a novel HIV-1 fusion inhibitor that displays a minimal interface for binding affinity Journal of Medicinal Chemistry 51 2008 388 391
40. A.C. Oliveira, A.N. Martins, A.F. Pires, M.B. Arruda, A. Tanuri, and H.S. Pereira Enfuvirtide (T-20) resistance-related mutations in HIV type 1 subtypes B, C, and F isolates from Brazilian patients failing HAART AIDS Research and Human Retroviruses 25 2009 193 198
41. A. Otaka, M. Nakamura, D. Nameki, E. Kodama, S. Uchiyama, and S. Nakamura Remodeling of gp41-C34 peptide leads to highly effective inhibitors of the fusion of HIV-1 with target cells Angewandte Chemie. International Edition in English 41 2002 2937 2940
42. J.D. Reeves, S.A. Gallo, N. Ahmad, J.L. Miamidian, P.E. Harvey, and M. Sharron Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics Proceedings of the National Academy of Sciences of the United States of America 99 2002 16249 16254
43. K. Shimura, D. Nameki, K. Kajiwara, K. Watanabe, Y. Sakagami, and S. Oishi Resistance profiles of novel electrostatically constrained HIV-1 fusion inhibitors Journal of Biological Chemistry 285 2010 39471 39480
44. T. Shirasaka, M.F. Kavlick, T. Ueno, W.Y. Gao, E. Kojima, M.L. Alcaide, S. Chokekijchai, B.M. Roy, E. Arnold, and R. Yarchoan Emergence of human immunodeficiency virus type 1 variants with resistance to multiple dideoxynucleosides in patients receiving therapy with dideoxynucleosides Proceedings of the National Academy of Sciences of the United States of America 92 1995 2398 2402
45. V. Svicher, S. Aquaro, R. D'Arrigo, A. Artese, S. Dimonte, and S. Alcaro Specific enfuvirtide-associated mutational pathways in HIV-1 Gp41 are significantly correlated with an increase in CD4(+) cell count, despite virological failure Journal of Infectious Diseases 197 2008 1408 1418
46. M. Tolstrup, J. Selzer-Plon, A.L. Laursen, L. Bertelsen, J. Gerstoft, and M. Duch Full fusion competence rescue of the enfuvirtide resistant HIV-1 gp41 genotype (43D) by a prevalent polymorphism (137 K) AIDS 21 2007 519 521
47. M. Ueno, E.N. Kodama, K. Shimura, Y. Sakurai, K. Kajiwara, and Y. Sakagami Synonymous mutations in stem-loop III of Rev responsive elements enhance HIV-1 replication impaired by primary mutations for resistance to enfuvirtide Antiviral Research 82 2009 67 72
48. T. Watabe, Y. Terakawa, K. Watanabe, H. Ohno, H. Nakano, and T. Nakatsu X-ray crystallographic study of an HIV-1 fusion inhibitor with the gp41 S138A substitution Journal of Molecular Biology 392 2009 657 665
49. B.D. Welch, A.P. VanDemark, A. Heroux, C.P. Hill, and M.S. Kay Potent D-peptide inhibitors of HIV-1 entry Proceedings of the National Academy of Sciences of the United States of America 104 2007 16828 16833
50. L. Xu, A. Pozniak, A. Wildfire, S.A. Stanfield-Oakley, S.M. Mosier, and D. Ratcliffe Emergence and evolution of enfuvirtide resistance following long-term therapy involves heptad repeat 2 mutations within gp41 Antimicrobial Agents and Chemotherapy 49 2005 1113 1119