Discovery and Optimization of a Natural HIV-1 Entry Inhibitor Targeting the gp41 Fusion Peptide

Cell

Volumn 129, Issue 2, 2007, Pages 263-275

  Münch, Jan ^a   Ständker, Ludger ^b,g   Adermann, Knut ^b,g   Schulz, Axel ^b   Schindler, Michael ^a   Chinnadurai, Raghavan ^a   Pöhlmann, Stefan ^c   Chaipan, Chawaree ^c   Biet, Thorsten ^d   Peters, Thomas ^d   Meyer, Bernd ^e   Wilhelm, Dennis ^e   Lu, Hong ^f   Jing, Weiguo ^f   Jiang, Shibo ^f   Forssmann, Wolf Georg ^b,g   Kirchhoff, Frank ^a  

^a UNIVERSITY OF ULM   (Germany)

^b IPF PHARMACEUTICALS GMBH   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d UNIVERSITY OF LÜBECK   (Germany)

^e UNIVERSITY OF HAMBURG   (Germany)

^f NEW YORK BLOOD CENTER   (United States)

^g HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

CELLBIO; HUMDISEASE; MICROBIO

Indexed keywords

PROTEIN; PROTEIN GP41; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ARTICLE; BLOOD; ENZYME INHIBITION; GENE FUSION; GENE TARGETING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34147137981     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.02.042     Document Type: Article

References (47)

1. Anderson E.D., Thomas L., Hayflick J.S., and Thomas G. Inhibition of HIV-1 gp160- dependent membrane fusion by a furin-directed alpha 1-antitrypsin variant. J. Biol. Chem. 268 (1993) 24887-24891
2. Armand-Ugon M., Gutierrez A., Clotet B., and Este E.A. HIV-1 resistance to the gp41-dependent fusion inhibitor C-34. Antiviral Res. 59 (2003) 137-142
3. Brantly M.L., Paul L.D., Miller B.H., Falk R.T., Wu M., and Crystal R.G. Clinical features and history of the destructive lung disease associated with alpha-1-antitrypsin deficiency of adults with pulmonary symptoms. Am. Rev. Respir. Dis. 138 (1988) 327-336
4. Chan D.C., Chutkowski C.T., and Kim P.S. Evidence that a prominent cavity in the coiled coil of HIV type 1 gp41 is an attractive drug target. Proc. Natl. Acad. Sci. USA 95 (1998) 15613-15637
5. Charneau P., Mirambeau G., Roux P., Paulous S., Buc H., and Clavel F. HIV-1 reverse transcription. A termination step at the center of the genome. J. Mol. Biol. 241 (1994) 651-662
6. Desrochers P.E., and Weiss S.J. Proteolytic inactivation of alpha-1-proteinase inhibitor by a neutrophil metalloproteinase. J. Clin. Invest. 81 (1988) 1646-1650
7. Detheux M., Standker L., Vakili J., Munch J., Forssmann U., Adermann K., Pohlmann S., Vassart G., Kirchhoff F., Parmentier M., et al. Natural proteolytic processing of hemofiltrate CC chemokine 1 generates a potent CC chemokine receptor (CCR)1 and CCR5 agonist with anti-HIV properties. J. Exp. Med. 192 (2000) 1501-1508
8. Eckstein D.A., Sherman M.P., Penn M.L., Chin P.S., De Noronha C.M., Greene W.C., and Goldsmith M.A. HIV-1 Vpr enhances viral burden by facilitating infection of tissue macrophages but not nondividing CD4+ T cells. J. Exp. Med. 194 (2001) 1407-1419
9. Eron J.J., Gulick R.M., Bartlett J.A., Merigan T., Arduino R., Kilby J.M., Yangco B., Diers A., Drobnes C., DeMasi R., et al. Short-term safety and antiviral activity of T-1249, a second generation fusion inhibitor. J. Infect. Dis. 189 (2004) 1075-1083
10. Fields G.B., and Noble R.L. Solid phase peptide synthesis utilizing 9-fluorenyl-methoxycarbonyl amino acids. Int. J. Pept. Protein Res. 35 (1990) 161-214
11. Forssmann W.G., Schulz-Knappe P., Meyer M., Adermann K., Forssmann D., Hock D., and Aoki A. Characterization of natural posttranslationally processed peptides from human blood: A new tool in the systematic investigation of native peptides. In: Yanaihara N. (Ed). Peptide Chemistry (1992), Escom, Leiden, The Netherlands 553-557
12. Gallo S.A., Wang W., Rawat S.S., Jung G., Waring A.J., Cole A.M., Lu H., Yan X., Daly N.L., Craik D.J., et al. Theta-defensins prevent HIV-1 Env-mediated fusion by binding gp41 and blocking 6-helix bundle formation. J. Biol. Chem. 281 (2006) 18787-18792
13. Geijtenbeek T.B., Kwon D.S., Torensma R., van Vliet S.J., van Duijnhoven G.C., Middel J., Cornelissen I.L., Nottet H.S., KewalRamani V.N., Littman D.R., et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100 (2000) 587-597
14. Goetzl E.J., Banda M.J., and Leppert D. Matrix metalloproteinases in immunity. J. Immunol. 156 (1996) 1-4
15. Greenberg M., and Cammack L.N. Resistance to enfuvirtide, the first HIV fusion inhibitor. J. Antimicrob. Chemother. 54 (2004) 333-340
16. Hallenberger S., Bosch V., Angliker H., Shaw E., Klenk H.D., and Garten W. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360 (1992) 358-361
17. Helmerhorst E.J., Reijnders I.M., van't Hof W., Veerman E.C., and Nieuw Amerongen A.V. A critical comparison of the hemolytic and fungicidal activities of cationic antimicrobial peptides. FEBS Lett. 449 (1999) 105-110
18. Hiebenthal-Millow K., and Kirchhoff F. The most frequent naturally occurring length polymorphism in the HIV-1 LTR has little effect on proviral transcription and viral replication. Virology 292 (2002) 169-175
19. Jiang S., Lin K., and Lu M. A conformation-specific monoclonal antibody reacting with fusion-active gp41 from the human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 72 (1998) 10213-10217
20. Jiang S., Lin K., Zhang L., and Debnath A.K. 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
21. Jiang S., Radigan L., and Zhang L. A convenient cell fusion assay for rapid screening for HIV entry inhibitors. Proc. SPIE 3926 (2000) 212-219
22. Jiang S., Zhao Q., and Debnath A.K. Peptide and non-peptide HIV fusion inhibitors. Curr. Pharm. Des. 8 (2002) 563-580
23. Johnston J.B., Jiang Y., van Marle G., Mayne M.B., Ni W., Holden J., McArthur J.C., and Power C. Lentivirus infection in the brain induces matrix metalloproteinase expression: role of envelope diversity. J. Virol. 74 (2000) 7211-7220
24. Kilby J.M., Hopkins S., Venetta T.M., DiMassimo B., Cloud G.A., Lee J.Y., Alldredge L., Hunter E., Lambert D., Bolognesi D., et al. 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
25. Kushner I. The acute phase response: an overview. Methods Enzymol. 163 (1988) 373-383
26. + cell anti-HIV factor (CAF). Trends Immunol. 24 (2003) 628-632
27. Liu S., Lu H., Niu J., Xu Y., Wu S., and Jiang S. 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. Lu M., Blacklow S.C., and Kim P.S. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2 (1995) 1075-1082
29. Mark S., Forssmann W.G., and Ständker L. Strategy for identifying circulating fragments of insulin-like growth factor binding proteins in a hemofiltrate peptide bank. J. Chromatogr. 852 (1999) 197-205
30. Miyazaki Y., Kuwata T., Takehisa J., and Hayami M. Analysis of a primary isolate-like virus from simian and human immunodeficiency virus-infected macaque having broad neutralizing activity. AIDS Res. Hum. Retroviruses 18 (2002) 469-475
31. Mobley P.W., Curtain C.C., Kirkpatrick A., Rostamkhani M., Waring A.J., and Gordon L.M. The amino-terminal peptide of HIV-1 glycoprotein 41 lyses human erythrocytes and CD4+ lymphocytes. Biochim. Biophys. Acta 1139 (1992) 251-256
32. Mobley P.W., Pilpa R., Brown C., Waring A.J., and Gordon L.M. Membrane-perturbing domains of HIV type 1 glycoprotein 41. AIDS Res. Hum. Retroviruses 17 (2001) 311-327
33. Moore J.P., and Stevenson M. New targets for inhibitors of HIV-1 replication. Nat. Rev. Mol. Cell Biol. 1 (2000) 40-49
34. Münch J., Standker L., Pohlmann S., Baribaud F., Papkalla A., Rosorius O., Stauber R., Sass G., Heveker N., Adermann K., et al. Hemofiltrate CC chemokine 1[9-74] causes effective internalization of CCR5 and is a potent inhibitor of R5-tropic HIV-1 strains in primary T-cells and macrophages. Antimicrob. Agents Chemother. 46 (2002) 982-990
35. Prechtel A.T., Turza N.M., Kobelt D.J., Eisemann J.I., Coffin R.S., McGrath Y., Hacker C., Ju X., Zenke M., and Steinkasserer A. Infection of mature dendritic cells with herpes simplex virus type 1 dramatically reduces lymphoid chemokine-mediated migration. J. Gen. Virol. 86 (2005) 1645-1657
36. Ray N., and Doms R.W. HIV-1 coreceptors and their inhibitors. Curr. Top. Microbiol. Immunol. 303 (2006) 97-120
37. Reimann K.A., Li J.T., Veazey R., Halloran M., Park I.W., Karlsson G.B., Sodroski J., and Letvin N.L. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70 (1996) 6922-6928
38. Rimsky L.T., Shugars D.C., and Matthews T.J. Determinants of human immunodeficiency virus type 1 resistance to gp41-derived inhibitory peptides. J. Virol. 72 (1998) 986-993
39. Root M.J., Kay M.S., and Kim P.S. Protein design of an HIV-1 entry inhibitor. Science 291 (2001) 884-888
40. Schulz-Knappe P., Raida M., Meyer M., Quellhorst E.A., and Forssmann W.-G. Systematic isolation of circulating peptides: the concept of peptide trapping. Eur. J. Med. Res. 1 (1996) 223-236
41. Schulz-Knappe P., Schrader M., Standker L., Richter R., Hess R., Jurgens M., and Forssmann W.-G. Peptide bank generated by large-scale preparation of circulating human peptides. J. Chromatogr. A. 776 (1997) 125-132
42. Shapiro L., Pott G.B., and Ralston A.H. Alpha-1-antitrypsin inhibits human immunodeficiency virus type 1. FASEB J. 15 (2001) 115-122
43. Stevenson M. HIV-1 pathogenesis. Nat. Med. 9 (2003) 853-860
44. Stoller J.K., and Aboussouan L.S. Alpha1-antitrypsin deficiency. Lancet 365 (2005) 2225-2236
45. Travis J., and Salvesen G.S. Human plasma proteinase inhibitors. Annu. Rev. Biochem. 52 (1983) 655-709
46. Walker C.M., Moody D.J., Stites D.P., and Levy J.A. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234 (1986) 1563-1566
47. Walter H., Schmidt B., Rascu A., Helm M., Moschik B., Paatz C., Kurowski M., Korn K., Uberla K., and Harrer T. Phenotypic HIV-1 resistance correlates with treatment outcome of nelfinavir salvage therapy. Antivir. Ther. 5 (2000) 249-256