Profile of resistance of human immunodeficiency virus to mannose-specific plant lectins

Journal of Virology

Volumn 78, Issue 19, 2004, Pages 10617-10627

  Balzarini, Jan ^a   Van Laethem, Kristel ^a,b   Hatse, Sigrid ^a   Vermeire, Kurt ^a   De Clercq, Erik ^a   Peumans, Willy ^c   Van Damme, Els ^c   Vandamme, Anne Mieke ^a,b   Böhlmstedt, Anders ^d   Schols, Dominique ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c Dept of Molecular Biotechnology ^*  (Belgium)

^d SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

1,1' [1,4 PHENYLENEBIS(METHYLENE)]BIS(1,4,8,11 TETRAAZACYCLOTETRADECANE); CICHORIC ACID; CYANOVIRIN N; DEXTRAN SULFATE; ENFUVIRTIDE; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; MANNOSE BINDING LECTIN; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS RESISTANCE; DRUG ACTIVITY; DRUG MECHANISM; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SYNCYTIUM; T LYMPHOCYTE SUBPOPULATION; VIRUS CULTURE; VIRUS ISOLATION; VIRUS MUTATION; VIRUS RESISTANCE; VIRUS STRAIN;

AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; BACTERIAL PROTEINS; CAFFEIC ACIDS; CARRIER PROTEINS; CELL LINE; COCULTURE TECHNIQUES; DEXTRAN SULFATE; DRUG RESISTANCE, VIRAL; GIANT CELLS; GLYCOSYLATION; HETEROCYCLIC COMPOUNDS; HIV; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; LILIACEAE; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MUTATION, MISSENSE; PEPTIDE FRAGMENTS; PLANT LECTINS; RECEPTORS, HIV; SUCCINATES; VIRUS REPLICATION;

EID: 4544256598     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.19.10617-10627.2004     Document Type: Article

References (47)

1. Arendrup, M., A. Sönnerborg, B. Svennerholm, L. Åkerblom, C. Nielsen, H. Clausen, S. Olofsson, J. O. Nielsen, and J.-E. S. Hansen. 1993. Neutralizing antibody response during human immunodeficiency virus type 1 infection: type and group specificity and viral escape. J. Gen. Virol. 74:855-863.
2. Arthos, J., C. Cicala, T. D. Steenbeke, T. W. Chun, C. Dela Cruz, D. B. Hanback, P. Khazanie, D. Nam, P. Schuck, S. M. Selig, D. Van Ryk, M. A. Chaikin, and A. S.-Fauci. 2002. Biochemical and biological characterization of a dodecameric CD4-Ig fusion protein: implications for therapeutic and vaccine strategies. J. Biol. Chem. 277:11456-11464.
3. Baba, M., O. Nishimura, N. Kanzaki, M. Okamoto, H. Sawada, Y. Iizawa, M. Shiraishi, Y. Aramaki, K. Okonogi, Y. Ogawa, K. Meguro, and M. Fujino. 1999. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc. Natl. Acad. Sci. USA 96:5698-5703.
4. Balzarini, J., D. Schols, J. Neyts, J. Van Damme, W. Peumans, and E. De Clercq. 1991. α-(1-3)- and α-(1-6)-D-mannose-specific plant lectins are markedly inhibitory to human immunodeficiency virus and cytomegalovirus infections in vitro. Antimicrob. Agents Chemother. 35:410-416.
5. Balzarini, J., J. Neyts, D. Schols, M. Hosoya, E. Van Damme, W. Peumans, and E. De Clercq. 1992. The mannose-specific plant lectins from Cymbidium hybrid and Epipactis helleborine and the (TV-acetylglucosamine)n-specific plant lectin from Urtica dioica are potent and selective inhibitors of human immunodeficiency virus and cytomegalovirus replication in vitro. Antivir. Res. 18:191-207.
6. Balzarini, J., A. Karlsson, M.-J. Pérez-Pérez, M.-J. Camarasa, and E. De Clercq. 1993. Knocking-out concentrations of HIV-1-specific inhibitors completely suppress HIV-1 infection and prevent the emergence of drug-resistant virus. Virology 196:576-585.
7. Balzarini, J., H. Pelemans, M.-J. Pérez-Pérez, A. San-Félix, M.-J. Camarasa, E. De Clercq, and A. Karlsson. 1996. Marked inhibitory activity of non-nucleoside reverse transcriptase inhibitors against human immunodeficiency virus type 1 when combined with (-)2′,3′- dideoxy-3′-thiacytidine. Mol. Pharmacol. 49:882-890.
8. a. Balzarini, J., S. Hatse, K. Vermeire, K. Princen, S. Aquaro, C.-F. Perno, E. De Clercq, H. Egberink, G. Vanden Mooter, W. Peumans, E. Van Damme, and D. Schols. Mannose-specific plant lectins from the Amaryllidaceae family qualify as efficient microbicides for prevention of human immunodeficiency virus infection. Antimicrob. Agents Chemother., in press.
9. Binlay, J. M., R. W. Sanders, B. Clas, N. Schuelke, A. Master, Y. Guo, F. Kajumo, D. J. Anselma, P. J. Maddon, W. C. Olson, and J. P. Moore. 2000. A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. Antimicrob. Agents Chemother. 74:627-643.
10. Bleul, C. C., M. Farzan, H. Choe, C. Parolin, I. Clark-Lewis, J. Sodroski, and T. A. Springer. 1996. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-833.
11. Bolmstedt, A. J., B. R. O'Keefe, S. R. Shenoy, J. B. McMahon, and M. R. Boyd. 2001. Cyanovirin-N defines a new class of antiviral agent targeting N-linked, high-mannose glycans in an oligosaccharide-specific manner. Mol. Pharmacol. 59:949-954.
12. Boyd, M. R., K. R. Gustafson, J. B. McMahon, R. H. Shoemaker, B. R. O'Keefe, T. Mori, R. J. Gulakowski, L. Wu, M. I. Rivera, C. M. Laurencot, M. J. Currens, J. H. Cardellina II, R. W. Buckheit, Jr., P. L. Nara, L. K. Pannell, R. C. Sowder II, and L. E. Henderson. 1997. Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob. Agents Chemother. 41:1521-1530.
13. Cocchi, F., A. L. DeVico, A. Garzino-Demo, S. K. Arya, R. C. Gallo, and P. Lusso. 1995. Identification of RANTES, MIP-1α, and MIP-1β as the major HIV-suppressive factors produced by CD8+ T cells. Science 270:1811-1815.
14. De Vreese, K., V. Kofler-Mongold, C. Leutgeb, V. Weber, K. Vermeire, S. Schacht, J. Anné, E. De Clercq, R. Datema, and G. Werner. 1996. The molecular target of bicyclams, potent inhibitors of human immunodeficiency virus replication. J. Virol. 70:689-696.
15. Dragic, T., V. Litwin, G. P. Allaway, S. R. Martin, Y. Huang, K. A. Nagashima, C. Cayanan, P. J. Maddon, R. A. Koup, J. P. Moore, and W. A. Paxton. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667-673.
16. Esté, J., D. Schols, K. De Vreese, K. Van Laethem, A.-M. Vandamme, J. Desmyter, and E. De Clercq. 1997. Development of resistance of human immunodeficiency virus type 1 to dextran sulfate associated with the emergence of specific mutations in the envelope gp120 glycoprotein. Mol. Pharmacol. 52:98-104.
17. Gallaher, W. R., J. M. Ball, R. F. Carry, A. M. Martin-Amedee, and R. C. Montelaro. 1995. A general model for the surface glycoproteins of HIV and other retroviruses. AIDS Res. Hum. Retrovir. 11:191-202.
18. Geyer, H., C. Holschbach, G. Hunsmann, and J. Schneider. 1988. Carbohydrates of human immunodeficiency virus. Structures of oligosaccharides linked to the envelope glycoprotein 120. J. Biol. Chem. 263:11760-11767.
19. Hansen, J.-E. S., C. M. Nielsen, C. Nielsen, P. Heegaard, L. R. Mathiesen, and J. O. Nielsen. 1989. Correlation between carbohydrate structures on the envelope glycoprotein gp120 of HIV-1 and HIV-2 and syncytium inhibition with lectins. AIDS 3:635-641.
20. Hart, M. L., M. Saifuddin, K. Uemura, E. G. Bremer, B. Hooker, T. Kawasaki, and G. T. Spear. 2002. High mannose glycans and sialic acid on gp120 regulate binding of mannose-binding lectin (MBL) to HIV type 1. AIDS Res. Hum. Retrovir. 18:1311-1317.
21. Kilby, J. M., 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. 1998. Potent suppression of HIV-1 replication in humans by T-20, a peptide inhibitor of gp41-mediated virus entry. Nat. Med. 4:1302-1307.
22. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
23. Leonard, C. K., M. W. Spellman, L. Riddle, R. J. Harris, J. N. Thomas, and T. J. Gregory. 1990. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265:10373-10382.
24. Losman, B., A. Bolmstedt, K. Schönning, A. Björndal, C. Westin, E. M. Fenyö, and S. Olofsson. 2001. Protection of neutralization epitopes in the V3 loop of oligomeric human immunodeficiency virus type 1 glycoprotein 120 by N-linked oligosaccharides in the V1 region. AIDS Res. Hum. Retrovir. 17:1067-1076.
25. Menten, P., S. Struyf, E. Schutyser, A. Wuyts, E. De Clercq, D. Schols, P. Proost, and J. Van Damme. 1999. The LD78β isoform of MIP-1α is the most potent CCR5 agonist and HIV-1-inhibiting chemokine. J. Clin. Investig. 104:R1-R5.
26. Mizuochi, T., M. W. Spellman, M. Larkin, J. Solomon, L. J. Basa, and T. Feizi. 1988. Carbohydrate structures of the human immunodeficiency virus (HIV) recombinant envelope glycoprotein gp120 produced in Chinese hamster ovary cells. Biochem. J. 254:599-603.
27. Mizuochi, T., M. W. Spellman, M. Larkin, J. Solomon, L. J. Basa, and T. Feizi. 1988. Structural characterization by chromatographic profiling of the oligosaccharides of human immunodeficiency virus (HIV) recombinant envelope glycoprotein gp120 produced in Chinese hamster ovary cells. Biomed. Chromatogr. 2:260-270.
28. Oberlin, E., A. Amara, F. Bachelerie, C. Bessia, J. L. Virelizier, F. Arenzana-Seisdedos, O. Schwartz, J. M. Heard, I. Clark-Lewis, D. F. Legler, M. Loetscher, M. Baggiolini, and B. Moser. 1996. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382:833-835.
29. O'Keefe, B. R., S. R. Shenoy, D. Xie, W. Zhang, J. M. Muschik, M. J. Currens, I. Chaiken, and M. R. Boyd. 2000. Analysis of the interaction between the HIV-inactivating protein cyanovirin-N and soluble forms of the envelope glycoproteins gp120 and gp41. Mol. Pharmacol. 58:982-992.
30. Oloffson, S., and J. E. Hansen. 1998. Host cell glycosylation of viral glycoproteins - a battlefield for host defence and viral resistance. Scand. J. Infect. Dis. 30:435-440.
31. Pluymers, W., N. Neamati, C. Pannecouque, V. Fikkert, C. Marchand, T. R. Burke, Jr., Y. Pommier, D. Schols, E. De Clercq, Z. Debyser, and M. Witvrouw. 2000. Viral entry as the primary target for the anti-HIV activity of chicoric acid and its tetra-acetyl esters. Mol. Pharmacol. 58:641-648.
32. Pollakis, G., S. Rang, A. Kliphuis, M. I. M. Chalaby, J. Goudsmit, and W. A. Paxton. 2001. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 276:13433-13441.
33. Rizzuto, C. D., R. Wyatt, N. Hernández-Ramos, Y. Sun, P. D. Kwong, W. A. Hendrickson, and J. Sodroski. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949-1953.
34. Scanlan, C. N., R. Pantophlet, M. R. Wormald, E. O. Saphire, R. Stanfield, I. A Wilson, H. Katinger, R. A. Dwek, P. M. Rudd, and D. R. Burton. 2002. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of α1→2 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321.
35. Schols, D., R. Pauwels, J. Desmyter, and E. De Clercq. 1990. Dextran sulfate and other polyanionic anti-HIV compounds specifically interact with the viral gp120 glycoprotein expressed by T-cells persistently infected with HIV-1. Virology 175:556-561.
36. Schols, D., S. Struyf, J. Van Damme, J. A. Esté, G. Henson, and E. De Clercq. 1997. Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J. Exp. Med. 186:1383-1388.
37. Schenning, K., B. Jansson, S. Olofsson, and J. E. S. Hansen. 1996. Rapid selection for an N-linked oligosaccharide by monoclonal antibodies directed against the V3 loop of human immunodeficiency virus type 1. J. Gen. Virol. 77:753-758.
38. Spear, G. T., M. R. Zarifiard, J. Xin, and M. Saifuddin. 2003. Inhibition of DC-SIGN-mediated trans infection of T cells by mannose-binding lectin. Immunology 110:80-85.
39. Strizki, J. M., S. Xu, N. E. Wagner, L. Wojcik, J. Liu, Y. Hou, M. Endres, A. Palani, S. Shapiro, J. W. Clader, W. J. Greenlee, J. R. Tagat, S. McCombie, K. Cox, A. B. Fawzi, C. C. Chou, C. Pugliese-Sivo, L. Davies, M. E. Moreno, D. D. Ho, A. Trkola, C. A. Stoddart, J. P. Moore, G. R. Reyes, and B. M. Baroudy. 2001. 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. USA 98:12718-12723.
40. Trkola, A., M. Purtscher, T. Muster, C. Ballaun, A. Buchacher, N. Sullivan, K. Srinivasan, J. Sodroski, J. P. Moore, and H. Katinger. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70: 1100-1108.
41. Tsai, C.-C., P. Emau, Y. Jiang, B. Tian, W. R. Morton, K. R. Gustafson, and M. R. Boyd. 2003. Cyanovirin-N gel as a topical microbicide prevents rectal transmission of SHIV89.6P in macaques. AIDS Res. Hum. Retrovir. 19:535-541.
42. Van Damme, E. J. M., A. K. Allen, and W. J. Peumans. 1987. Isolation and characterization of a lectin with exclusive specificity towards mannose from snowdrop (Galanthus nivalis) bulbs. FEBS Lett. 215:140-144.
43. Van Damme, E. J. M., A. K. Allen, and W. J. Peumans. 1988. Related mannose-specific lectins from different species of the family Amaryllidaceae. Plant Physiol. 73:52-57.
44. Van Damme, E. J. M., W. J. Peumans, A. Pusztai, and S. Bardocz (ed.). 1998. Handbook of plant lectins: properties and biomedical applications. John Wiley & Sons, Chichester, N.Y.
45. Van den Steen, P. E., P. M. Rudd, M. R. Wormald, R. A. Dwek, and G. Opdenakker. 2000. O-Linked glycosylation in focus. Trends Glycosci. Glycotechnol. 12:35-49.
46. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
47. Wyatt, R., P. D. Kwong, E. Desjardins, R. W. Sweet, J. Robinson, W. A. Hendrickson, and J. G. Sodroski. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711.