Activity and safety of synthetic lectins based on benzoboroxole- functionalized polymers for inhibition of HIV entry

Molecular Pharmaceutics

Volumn 8, Issue 6, 2011, Pages 2465-2475

  Mahalingam, Alamelu ^a   Geonnotti, Anthony R ^b   Balzarini, Jan ^c   Kiser, Patrick F ^a  

^a UNIVERSITY OF UTAH   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

benzoboroxole; entry inhibitor; HIV; polyvalency; synthetic lectins

Indexed keywords

BENZOBOROXOLE DERIVATIVE; COPOLYMER; FRUCTOSE; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; LECTIN; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG SAFETY; DRUG SOLUBILITY; DRUG SPECIFICITY; MOLECULAR INTERACTION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; VIRUS ENTRY;

ANTIVIRAL AGENTS; BORONIC ACIDS; CALORIMETRY; HIV; HUMANS; LECTINS; MODELS, MOLECULAR; POLYMERS; VIRUS INTERNALIZATION;

EID: 82955240656     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp2002957     Document Type: Article

References (53)

1. Wyatt, R.; Kwong, P. D.; Desjardins, E.; Sweet, R. W.; Robinson, J.; Hendrickson, W. A.; Sodroski, J. G. The antigenic structure of the HIV gp120 envelope glycoprotein Nature 1998, 393 (6686) 705-711 (Pubitemid 28289663)
2. Poignard, P.; Saphire, E. O.; Parren, P. W.; Burton, D. R. gp120: Biologic aspects of structural features Annu. Rev. Immunol. 2001, 19, 253-274 (Pubitemid 32368036)
3. Gallaher, W. R.; Ball, J. M.; Garry, R. F.; Martin-Amedee, A. M.; Montelaro, R. C. A general model for the surface glycoproteins of HIV and other retroviruses AIDS Res. Hum. Retroviruses 1995, 11 (2) 191-202
4. Leonard, C. K.; Spellman, M. W.; Riddle, L.; Harris, R. J.; Thomas, J. N.; Gregory, T. J. 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. 1990, 265 (18) 10373-10382
5. Balzarini, J.; Van Laethem, K.; Hatse, S.; Vermeire, K.; De Clercq, E.; Peumans, W.; Van Damme, E.; Vandamme, A. M.; Bolmstedt, A.; Schols, D. Profile of resistance of human immunodeficiency virus to mannose-specific plant lectins J. Virol. 2004, 78 (19) 10617-10627 (Pubitemid 39258388)
6. Balzarini, J.; Van Laethem, K.; Hatse, S.; Froeyen, M.; Van Damme, E.; Bolmstedt, A.; Peumans, W.; De Clercq, E.; Schols, D. Marked depletion of glycosylation sites in HIV-1 gp120 under selection pressure by the mannose-specific plant lectins of Hippeastrum hybrid and Galanthus nivalis Mol. Pharmacol. 2005, 67 (5) 1556-1565 (Pubitemid 40594154)
7. Balzarini, J.; Van Laethem, K.; Hatse, S.; Froeyen, M.; Peumans, W.; Van Damme, E.; Schols, D. Carbohydrate-binding agents cause deletions of highly conserved glycosylation sites in HIV gp120: A new therapeutic concept to hit the achilles heel of HIV J. Biol. Chem. 2005, 280 (49) 41005-41014 (Pubitemid 41780596)
8. Balzarini, J.; Van Laethem, K.; Peumans, W. J.; Van Damme, E. J. M.; Bolmstedt, A.; Gago, F.; Schols, D. Mutational pathways, resistance profile, and side effects of cyanovirin relative to human immunodeficiency virus type 1 strains with N-glycan deletions in their gp120 envelopes J. Virol. 2006, 80 (17) 8411-8421 (Pubitemid 44384854)
9. Balzarini, J. Large-molecular-weight carbohydrate-binding agents as HIV entry inhibitors targeting glycoprotein gp120 Curr. Opin. HIV AIDS 2006, 1 (5) 355-360
10. Vandekerckhove, L.; Verhofstede, C.; Vogelaers, D. Maraviroc: integration of a new antiretroviral drug class into clinical practice J. Antimicrob. Chemother. 2008, 61 (6) 1187-1190 (Pubitemid 351753580)
11. Makinson, A.; Reynes, J. The fusion inhibitor enfuvirtide in recent antiretroviral strategies Curr. Opin. HIV AIDS 2009, 4 (2) 150-158
12. Pirrone, V.; Wigdahl, B.; Krebs, F. C. The rise and fall of polyanionic inhibitors of the human immunodeficiency virus type 1 Antiviral Res. 2011, 90 (3) 168-182
13. Van Damme, L.; Govinden, R.; Mirembe, F. M.; Guedou, F.; Solomon, S.; Becker, M. L.; Pradeep, B. S.; Krishnan, A. K.; Alary, M.; Pande, B.; Ramjee, G.; Deese, J.; Crucitti, T.; Taylor, D. Lack of effectiveness of cellulose sulfate gel for the prevention of vaginal HIV transmission N. Engl. J. Med. 2008, 359 (5) 463-472
14. McCormack, S.; Ramjee, G.; Kamali, A.; Rees, H.; Crook, A. M.; Gafos, M.; Jentsch, U.; Pool, R.; Chisembele, M.; Kapiga, S.; Mutemwa, R.; Vallely, A.; Palanee, T.; Sookrajh, Y.; Lacey, C. J.; Darbyshire, J.; Grosskurth, H.; Profy, A.; Nunn, A.; Hayes, R.; Weber, J. PRO2000 vaginal gel for prevention of HIV-1 infection (Microbicides Development Programme 301): a phase 3, randomised, double-blind, parallel-group trial Lancet 2010, 376 (9749) 1329-1337
15. Greene, W. C. The brightening future of HIV therapeutics Nat. Immunol. 2004, 5 (9) 867-871 (Pubitemid 39276227)
16. Sato, Y.; Hirayama, M.; Morimoto, K.; Yamamoto, N.; Okuyama, S.; Hori, K. High mannose-binding lectin with preference for the cluster of {alpha}1-2-mannose from the green alga Boodlea coacta is a potent entry inhibitor of HIV-1 and influenza viruses J. Biol. Chem. 2011, 286 (22) 19446-19458
17. Boyd, M.; Gustafson, K.; McMahon, J.; Shoemaker, R.; O'Keefe, B.; Mori, T.; Gulakowski, R.; Wu, L.; Rivera, M.; Laurencot, C.; Currens, M.; Cardellina, J., 2nd; Buckheit, R., Jr; Nara, P.; Pannell, L.; Sowder, R., 2nd; Henderson, L. 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. 1997, 41 (7) 1521-1530 (Pubitemid 27289680)
18. Mori, T.; O'Keefe, B. R.; Sowder, R. C., 2nd; Bringans, S.; Gardella, R.; Berg, S.; Cochran, P.; Turpin, J. A.; Buckheit, R. W., Jr.; McMahon, J. B.; Boyd, M. R. Isolation and characterization of griffithsin, a novel HIV-inactivating protein, from the red alga Griffithsia sp J. Biol. Chem. 2005, 280 (10) 9345-9353 (Pubitemid 40409628)
19. Dey, B.; Lerner, D. L.; Lusso, P.; Boyd, M. R.; Elder, J. H.; Berger, E. A. Multiple antiviral activities of cyanovirin-N: blocking of human immunodeficiency virus type 1 gp120 interaction with CD4 and coreceptor and inhibition of diverse enveloped viruses J. Virol. 2000, 74 (10) 4562-4569 (Pubitemid 30237881)
20. Micewicz, E. D.; Cole, A. L.; Jung, C. L.; Luong, H.; Phillips, M. L.; Pratikhya, P.; Sharma, S.; Waring, A. J.; Cole, A. M.; Ruchala, P. Grifonin-1: a small HIV-1 entry inhibitor derived from the algal lectin, Griffithsin PLoS One 2010, 5 (12) e14360
21. Balzarini, J.; Van Laethem, K.; Daelemans, D.; Hatse, S.; Bugatti, A.; Rusnati, M.; Igarashi, Y.; Oki, T.; Schols, D. Pradimicin A, a carbohydrate-binding nonpeptidic lead compound for treatment of infections with viruses with highly glycosylated envelopes, such as human immunodeficiency virus J. Virol. 2007, 81 (1) 362-373 (Pubitemid 44975175)
22. Mammen, M.; Choi, S.-K.; Whitesides, G. M. Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors Angew. Chem., Int. Ed. 1998, 37 (20) 2754-2794 (Pubitemid 29008561)
23. Kitov, P. I.; Bundle, D. R. On the nature of the multivalency effect: A thermodynamic model J. Am. Chem. Soc. 2003, 125 (52) 16271-16284 (Pubitemid 38020650)
24. Mammen, M.; Dahmann, G.; Whitesides, G. M. Effective inhibitors of hemagglutination by influenza virus synthesized from polymers having active ester groups-insight into mechanism of inhibition J. Med. Chem. 1995, 38 (21) 4179-4190
25. Taylor, M. E.; Drickamer, K. Introduction to glycobiology, 2 nd ed.; Oxford University Press: 2006.
26. Springsteen, G.; Wang, B. H. A detailed examination of boronic acid-diol complexation Tetrahedron 2002, 58 (26) 5291-5300 (Pubitemid 34663811)
27. Yan, J.; Springsteen, G.; Deeter, S.; Wang, B. The relationship among pKa, pH, and binding constants in the interactions between boronic acids and diols-it is not as simple as it appears Tetrahedron 2004, 60 (49) 11205-11209 (Pubitemid 39425240)
28. Cai, S. X.; Keana, J. F. W. o-Acetamidophenylboronate esters stabilized toward hydrolysis by an intramolecular O-B interaction: potential linkers for selective bioconjugation via vicinal diol moieties of carbohydrates Bioconjugate Chem. 1991, 2, 317-322
29. Dowlut, M.; Hall, D. G. An improved class of sugar-binding boronic acids, soluble and capable of complexing glycosides in neutral water J. Am. Chem. Soc. 2006, 128 (13) 4226-4227
30. Kaur, G.; Fang, H.; Gao, X.; Li, H.; Wang, B. Substituent effect on anthracene-based bisboronic acid glucose sensors Tetrahedron 2006, 62 (11) 2583-2589 (Pubitemid 43243594)
31. Mulla, H. R.; Agard, N. J.; Basu, A. 3-methoxycarbonyl-5-nitrophenyl boronic acid: high affinity diol recognition at neutral pH Bioorg. Med. Chem. Lett. 2004, 14 (1) 25-27 (Pubitemid 38016207)
32. Bérubé, M.; Dowlut, M.; Hall, D. G. Benzoboroxoles as efficient glycopyranoside-binding agents in physiological conditions: structure and selectivity of complex formation J. Org. Chem. 2008, 73 (17) 6471-6479
33. Jay, J. I.; Lai, B. E.; Myszka, D. G.; Mahalingam, A.; Langheinrich, K.; Katz, D. F.; Kiser, P. F. Multivalent benzoboroxole functionalized polymers as gp120 glycan targeted microbicide entry inhibitors Mol. Pharmaceutics 2010, 7 (1) 116-129
34. Springsteen, G.; Wang, B. Alizarin Red S. as a general optical reporter for studying the binding of boronic acids with carbohydrates Chem. Commun. 2001, 17) 1608-1609 (Pubitemid 32808017)
35. Bhat, K. L.; Howard, N. J.; Rostami, H.; Lai, J. H.; Bock, C. W. Intramolecular dative bonds involving boron with oxygen and nitrogen in boronic acids and esters: a computational study J. Mol. Struct. 2005, 723 (1-3) 147-157 (Pubitemid 40630949)
36. Winblade, N. D.; Schmökel, H.; Baumann, M.; Hoffman, A. S.; Hubbell, J. A. Sterically blocking adhesion of cells to biological surfaces with a surface-active copolymer containing poly(ethylene glycol) and phenylboronic acid J. Biomed. Mater. Res. 2002, 59 (4) 618-631 (Pubitemid 34044464)
37. Cutalo, J. M.; Deterding, L. J.; Tomer, K. B. Characterization of glycopeptides from HIV-I(SF2) gp120 by liquid chromatography mass spectrometry J. Am. Soc. Mass Spectrom. 2004, 15 (11) 1545-1555 (Pubitemid 39433848)
38. Zhu, X.; Borchers, C.; Bienstock, R. J.; Tomer, K. B. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells Biochemistry 2000, 39 (37) 11194-11204
39. Buffa, V.; Stieh, D.; Mamhood, N.; Hu, Q.; Fletcher, P.; Shattock, R. J. Cyanovirin-N potently inhibits human immunodeficiency virus type 1 infection in cellular and cervical explant models J. Gen. Virol. 2009, 90 (1) 234-243
40. Rogers, K. M.; Heise, M. Modulation of cellular tropism and innate antiviral response by viral glycans J. Innate Immun. 2009, 1 (5) 405-412
41. Moulard, M.; Lortat-Jacob, H.; Mondor, I.; Roca, G.; Wyatt, R.; Sodroski, J.; Zhao, L.; Olson, W.; Kwong, P. D.; Sattentau, Q. J. Selective interactions of polyanions with basic surfaces on human immunodeficiency virus type 1 gp120 J. Virol. 2000, 74 (4) 1948-60 (Pubitemid 30434054)
42. Vigerust, D. J.; Shepherd, V. L. Virus glycosylation: role in virulence and immune interactions Trends Microbiol. 2007, 15 (5) 211-218 (Pubitemid 46660602)
43. Balzarini, J.; Schols, D.; Neyts, J.; Van Damme, E.; Peumans, W.; De Clercq, E. Alpha-(1-3)- and alpha-(1-6)-D-mannose-specific plant lectins are markedly inhibitory to human immunodeficiency virus and cytomegalovirus infections in vitro Antimicrob. Agents Chemother. 1991, 35 (3) 410-406
44. Barrientos, L. G.; O'Keefe, B. R.; Bray, M.; Sanchez, A.; Gronenborn, A. M.; Boyd, M. R. Cyanovirin-N binds to the viral surface glycoprotein, GP1,2 and inhibits infectivity of Ebola virus Antiviral Res. 2003, 58 (1) 47-56 (Pubitemid 36507221)
45. Tsai, C. C.; Emau, P.; Jiang, Y.; Agy, M. B.; Shattock, R. J.; Schmidt, A.; Morton, W. R.; Gustafson, K. R.; Boyd, M. R. Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models AIDS Res. Hum. Retroviruses 2004, 20 (1) 11-18 (Pubitemid 38147172)
46. Helle, F.; Wychowski, C.; Vu-Dac, N.; Gustafson, K. R.; Voisset, C.; Dubuisson, J. Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans J. Biol. Chem. 2006, 281 (35) 25177-25183 (Pubitemid 44401904)
47. O'Keefe, B. R.; Smee, D. F.; Turpin, J. A.; Saucedo, C. J.; Gustafson, K. R.; Mori, T.; Blakeslee, D.; Buckheit, R.; Boyd, M. R. Potent anti-influenza activity of cyanovirin-N and interactions with viral hemagglutinin Antimicrob. Agents Chemother. 2003, 47 (8) 2518-2525 (Pubitemid 36919454)
48. Kataoka, K.; Miyazaki, H.; Okano, T.; Sakurai, Y. Sensitive glucose-induced change of the lower critical solution temperature of poly[N,N-(dimethylacrylamide)-co-3-(acrylamido)-phenylboronic acid] in physiological saline Macromolecules 1994, 27 (4) 1061-1062
49. Morokoshi, S.; Ohhori, K.; Mizukami, K.; Kitano, H. Sensing capabilities of colloidal gold modified with a self-assembled monolayer of a glucose-carrying polymer chain on a glass substrate Langmuir 2004, 20 (20) 8897-8902
50. Winblade, N. D.; Nikolic, I. D.; Hoffman, A. S.; Hubbell, J. A. Blocking adhesion to cell and tissue surfaces by the chemisorption of a poly-l-lysine-graft-(poly(ethylene glycol); phenylboronic acid) copolymer Biomacromolecules 2000, 1 (4) 523-533
51. Patel, S.; Hazrati, E.; Cheshenko, N.; Galen, B.; Yang, H.; Guzman, E.; Wang, R.; Herold, B. C.; Keller, M. J. Seminal plasma reduces the effectiveness of topical polyanionic microbicides J. Infect. Dis. 2007, 196 (9) 1394-1402 (Pubitemid 351412013)
52. Owen, D. H.; Katz, D. F. A review of the physical and chemical properties of human semen and the formulation of a semen simulant J. Androl. 2005, 26 (4) 459-469 (Pubitemid 40847857)
53. Ayehunie, S.; Cannon, C.; Lamore, S.; Kubilus, J.; Anderson, D. J.; Pudney, J.; Klausner, M. Organotypic human vaginal-ectocervical tissue model for irritation studies of spermicides, microbicides, and feminine-care products Toxicol. in Vitro 2006, 20 (5) 689-698 (Pubitemid 43816250)