Antiviral activity of carbohydrate-binding agents against Nidovirales in cell culture

Antiviral Research

Volumn 76, Issue 1, 2007, Pages 21-29

  van der Meer, F J U M ^a   de Haan, C A M ^a   Schuurman, N M P ^a   Haijema, B J ^a   Peumans, W J ^b   Van Damme, E J M ^b   Delputte, P L ^b   Balzarini, J ^c   Egberink, H F ^a  

^a Department of Infectious Diseases and Immunology   (Netherlands)

^b GHENT UNIVERSITY   (Belgium)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

Glycosylation; Immunoperoxidase; In vitro assay; Luciferase; MTT; Nidovirales

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; AGGLUTININ; ANTIVIRUS AGENT; CARBOHYDRATE; CYANOVIRIN N; CYMBIDIUM AGGLUTININ; GALANTHUS NIVALIS AGGLUTININ; LECTIN; LUCIFERASE; OLIGOSACCHARIDE; PEROXIDASE; PRADIMICIN A; UNCLASSIFIED DRUG; URTICA DIOICA AGGLUTININ; URTICA DIOICA EXTRACT; VIRUS PROTEIN;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTERIVIRUS; ARTICLE; AVIAN INFECTIOUS BRONCHITIS VIRUS; CELL CULTURE; CELL VIABILITY; COLORIMETRY; CONTROLLED STUDY; CORONAVIRUS; CYMBIDIUM; EQUINE VIRAL ARTERITIS VIRUS; GALANTHUS NIVALIS; HIPPEASTRUM; LUNG ALVEOLUS MACROPHAGE; MEDICINAL PLANT; MURINE HEPATITIS CORONAVIRUS; NIDOVIRALES; NONHUMAN; PRIORITY JOURNAL; TOROVIRUS; TRANSMISSIBLE GASTROENTERITIS VIRUS; URTICA DIOICA;

ANGIOSPERMS; ANIMALS; ANTHRACYCLINES; ANTIVIRAL AGENTS; BACTERIAL PROTEINS; CARRIER PROTEINS; CATS; CELL LINE; CERCOPITHECUS AETHIOPS; COLORIMETRY; FEMALE; GALANTHUS; IMMUNOHISTOCHEMISTRY; LILIACEAE; LUCIFERASES; MICE; MICROBIAL SENSITIVITY TESTS; NIDOVIRALES; PLANT LECTINS; RNA VIRUS INFECTIONS; SWINE; TETRAZOLIUM SALTS; THIAZOLES; URTICA DIOICA;

ANIMALIA; AVIAN INFECTIOUS BRONCHITIS VIRUS; BERNE VIRUS; CYMBIDIUM; EQUIDAE; EQUINE ARTERITIS VIRUS; FELIDAE; GALANTHUS NIVALIS; HIPPEASTRUM; MURINE HEPATITIS VIRUS; NIDOVIRALES; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SARS CORONAVIRUS; TOROVIRUS; TRANSMISSIBLE GASTROENTERITIS VIRUS; URTICA DIOICA;

EID: 34447501702     PISSN: 01663542     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.antiviral.2007.04.003     Document Type: Article

References (65)

1. Alonso-Caplen F.V., Matsuoka Y., Wilcox G.E., and Compans R.W. Replication and morphogenesis of avian coronavirus in Vero cells and their inhibition by monensin. Virus Res. 1 (1984) 153
2. Ansari I.H., Kwon B., Osorio F.A., and Pattnaik A.K. Influence of N-linked glycosylation of porcine reproductive and respiratory syndrome virus GP5 on virus infectivity, antigenicity, and ability to induce neutralizing antibodies. J. Virol. 80 (2006) 3994-4004
3. Balzarini J. Targeting the glycans of gp120: a novel approach aimed at the Achilles heel of HIV. Lancet Infect Dis. 5 (2005) 726-731
4. Balzarini J., Schols D., Neyts J., Van Damme E., Peumans W., and 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. 35 (1991) 410-416
5. Balzarini J., Neyts J., Schols D., Hosoya M., Van Damme E., Peumans W., and De Clercq E. The mannose-specific plant lectins from Cymbidium hybrid and Epipactis helleborine and the (N-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 (1992) 191-207
6. Balzarini J., Hatse S., Vermeire K., Princen K., Aquaro S., Perno C.F., De Clercq E., Egberink H., Vanden Mooter G., Peumans W., Van Damme E., and Schols D. Mannose-specific plant lectins from the Amaryllidaceae family qualify as efficient microbicides for prevention of human immunodeficiency virus infection. Antimicrob. Agents Chemother. 48 (2004) 3858-3870
7. Balzarini J., Van Laethem K., Hatse S., Vermeire K., De Clercq E., Peumans W., Van Damme E., Vandamme A.M., Bolmstedt A., and Schols D. Profile of resistance of human immunodeficiency virus to mannose-specific plant lectins. J. Virol. 78 (2004) 10617-10627
8. Balzarini J., Vijgen L., Keyaerts E., Van Damme E., Peumans W., De Clercq E., Egberink H., and Van Ranst M. Mannose-specific plant lectins are potent inhibitors of coronavirus infection including the virus causing SARS. Proceedings of the 17th International Conference on Antiviral Research (2004) 122 (Antivir. Res. 62, A76)
9. Balzarini J., Van Laethem K., Hatse S., Froeyen M., Peumans W., Van Damme E., and 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. 280 (2005) 41005-41014
10. Balzarini J., Van Laethem K., Hatse S., Froeyen M., Van Damme E., Bolmstedt A., Peumans W., De Clercq E., and 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. 67 (2005) 1556-1565
11. Balzarini J., Van Laethem K., Peumans W.J., Van Damme E.J., Bolmstedt A., Gago F., and 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. 80 (2006) 8411-8421
12. Balzarini J., Van Laethem K., Daelemans D., Hatse S., Bugatti A., Rusnati M., Igarashi Y., Oki T., and 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. 81 (2007) 362-373
13. Barrientos L.G., O'Keefe B.R., Bray M., Sanchez A., Gronenborn A.M., and Boyd M.R. Cyanovirin-N binds to the viral surface glycoprotein, GP1 2 and inhibits infectivity of Ebola virus. Antivir. Res. 58 (2003) 47-56
14. Bedard J., May S., Barbeau D., Yuen L., Rando R.F., and Bowlin T.L. A high throughput colorimetric cell proliferation assay for the identification of human cytomegalovirus inhibitors. Antivir. Res. 41 (1999) 35-43
15. Blay W.M., Gnanakaran S., Foley B., Doria-Rose N.A., Korber B.T., and Haigwood N.L. Consistent patterns of change during the divergence of human immunodeficiency virus type 1 envelope from that of the inoculated virus in simian/human immunodeficiency virus-infected macaques. J. Virol. 80 (2006) 999-1014
16. Boyd M.R., Gustafson K.R., McMahon J.B., Shoemaker R.H., O'Keefe B.R., Mori T., Gulakowski R.J., Wu L., Rivera M.I., Laurencot C.M., Currens M.J., Cardellina II J.H., Buckheit Jr. R.W., Nara P.L., Pannell L.K., Sowder II R.C., and Henderson L.E. 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 (1997) 1521-1530
17. Chakraborti S., Prabakaran P., Xiao X., and Dimitrov D.S. The SARS coronavirus S glycoprotein receptor binding domain: fine mapping and functional characterization. Virol J. 2 (2005) 73
18. Costers S., Delputte P.L., and Nauwynck H.J. Porcine reproductive and respiratory syndrome virus-infected alveolar macrophages contain no detectable levels of viral proteins in their plasma membrane and are protected against antibody-dependent, complement-mediated cell lysis. J. Gen. Virol. 87 (2006) 2341-2351
19. De Clercq E. Antivirals and antiviral strategies. Nat. Rev. Microbiol. 2 (2004) 704-720
20. De Clercq E. Potential antivirals and antiviral strategies against SARS coronavirus infections. Expert Rev. Anti Infect Ther. 4 (2006) 291-302
21. de Haan C.A., van Genne L., Stoop J.N., Volders H., and Rottier P.J. Coronaviruses as vectors: position dependence of foreign gene expression. J. Virol. 77 (2003) 11312-11323
22. de Haan C.A., Haijema B.J., Boss D., Heuts F.W., and Rottier P.J. Coronaviruses as vectors: stability of foreign gene expression. J. Virol. 79 (2005) 12742-12751
23. De Vries A.A., Horzinek M.C., Rottier P.J.M., and De Groot R.J. The genome organization of the Nidovirales: similarities and differences between Arteri-, Toro-, and coronaviruses. Semin. Virol. 8 (1997) 33-47
24. Delputte P.L., and Nauwynck H.J. Porcine arterivirus infection of alveolar macrophages is mediated by sialic acid on the virus. J. Virol. 78 (2004) 8094-8101
25. Dey B., Lerner D.L., Lusso P., Boyd M.R., Elder J.H., and 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. 74 (2000) 4562-4569
26. Drosten C., Gunther S., Preiser W., van der Werf S., Brodt H.-R., Becker S., Rabenau H., Panning M., Kolesnikova L., Fouchier R.A.M., Berger A., Burguiere A.-M., Cinatl J., Eickmann M., Escriou N., Grywna K., Kramme S., Manuguerra J.-C., Muller S., Rickerts V., Sturmer M., Vieth S., Klenk H.-D., Osterhaus A.D.M.E., Schmitz H., and Doerr H.W. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348 (2003) 1967-1976
27. Fujikawa K., Tsukamoto Y., Oki T., and Lee Y.C. Spectroscopic studies on the interaction of pradimicin BMY-28864 with mannose derivatives. Glycobiology 8 (1998) 407-414
28. Glaser A.L., Chirnside E.D., Horzinek M.C., and de Vries A.A.F. Equine arteritis virus. Theriogenology 47 (1997) 1275
29. Gorbalenya A.E., Enjuanes L., Ziebuhr J., and Snijder E.J. Nidovirales: evolving the largest RNA virus genome. Virus Res. 117 (2006) 17
30. Grail A., and Norval M. Effect of concanavalin A and succinyl concanavalin A on cytomegalovirus replication in fibroblasts. Arch. Virol. 91 (1986) 61-71
31. Hansen J.E., Nielsen C.M., Nielsen C., Heegaard P., Mathiesen L.R., and Nielsen J.O. Correlation between carbohydrate structures on the envelope glycoprotein gp120 of HIV-1 and HIV-2 and syncytium inhibition with lectins. AIDS 3 (1989) 635-641
32. Hart M.L., Saifuddin M., Uemura K., Bremer E.G., Hooker B., Kawasaki T., and Spear G.T. High mannose glycans and sialic acid on gp120 regulate binding of mannose-binding lectin (MBL) to HIV type 1. AIDS Res. Hum. Retroviruses 18 (2002) 1311-1317
33. Helle F., Wychowski C., Vu-Dac N., Gustafson K.R., Voisset C., and Dubuisson J. Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans. J. Biol. Chem. 281 (2006) 25177-25183
34. Herrewegh A.A.P.M., Mahler M., Hedrich H.J., Haagmans B.L., Egberink H.F., Horzinek M.C., Rottier P.J.M., and de Groot R.J. Persistence and evolution of feline coronavirus in a closed cat-breeding colony. Virology 234 (1997) 349
35. Hohdatsu T., Izumiya Y., Yokoyama Y., Kida K., and Koyama H. Differences in virus receptor for type I and type II feline infectious peritonitis virus. Arch. Virol. 143 (1998) 839-850
36. Iagrashi Y., and Oki T. Mannose-binding quinone glycoside MBQ: potential utility and action mechanism. Adv. Appl. Microbiol. 54 (2004) 147-166
37. McKeirnan A.J., Evermann F.J., Hargis A., Miller L.M., and Ott R.L. Isolation of feline coronaviruses from two cats with diverse disease manifestations. Feline Pract. 11 (1981) 16-20
38. Mori T., Gustafson K.R., Pannell L.K., Shoemaker R.H., Wu L., McMahon J.B., and Boyd M.R. Recombinant production of cyanovirin-N, a potent human immunodeficiency virus-inactivating protein derived from a cultured cyanobacterium. Protein Expr. Purif. 12 (1998) 151-158
39. Naqi S., Gay K., Patalla P., Mondal S., and Liu R. Establishment of persistent avian infectious bronchitis virus infection in antibody-free and antibody-positive chickens. Avian Dis. 47 (2003) 594-601
40. NetNGlyc 1.0 Server. URL: http://www.cbs.dtu.dk/services/NetNGlyc/ Gupta, R., Jung, E., Brunak, S., unpublished data.
41. O'Keefe B.R., Smee D.F., Turpin J.A., Saucedo C.J., Gustafson K.R., Mori T., Blakeslee D., Buckheit R., and Boyd M.R. Potent anti-influenza activity of cyanovirin-N and interactions with viral hemagglutinin. Antimicrob. Agents Chemother. 47 (2003) 2518-2525
42. Oki T., Konishi M., Tomatsu K., Tomita K., Saitoh K., Tsunakawa M., Nishio M., Miyaki T., and Kawaguchi H. Pradimicin, a novel class of potent antifungal antibiotics. J. Antibiot. (Tokyo) 41 (1988) 1701-1704
43. Olivo P.D. Transgenic cell lines for detection of animal viruses. Clin. Microbiol. Rev. 9 (1996) 321-334
44. Pauwels R., Balzarini J., Baba M., Snoeck R., Schols D., Herdewijn P., Desmyter J., and De Clercq E. Rapid and automated tetrazolium-based colorimetric assay for the detection of anti-HIV compounds. J. Virol. Meth. 20 (1988) 309-321
45. Pedersen N.C., and Black J.W. Attempted immunization of cats against feline infectious peritonitis, using avirulent live virus or sublethal amounts of virulent virus. Am. J. Vet. Res. 44 (1983) 229-234
46. Pyrc, K., Berkhout, B., van der Hoek, L., in press. The novel human coronaviruses NL63 and HKU1. J. Virol., JVI.01466-01406.
47. Reitter J.N., Means R.E., and Desrosiers R.C. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4 (1998) 679-684
48. Robinson Jr. W.E., Montefiori D.C., and Mitchell W.M. Evidence that mannosyl residues are involved in human immunodeficiency virus type 1 (HIV-1) pathogenesis. AIDS Res. Hum. Retroviruses 3 (1987) 265-282
49. Rossen J.W., Kouame J., Goedheer A.J., Vennema H., and Rottier P.J. Feline and canine coronaviruses are released from the basolateral side of polarized epithelial LLC-PK1 cells expressing the recombinant feline aminopeptidase-N cDNA. Arch. Virol. 146 (2001) 791-799
50. Rottier P.J., Horzinek M.C., and van der Zeijst B.A. Viral protein synthesis in mouse hepatitis virus strain A59-infected cells: effect of tunicamycin. J. Virol. 40 (1981) 350-357
51. Rudd P.M., Elliott T., Cresswell P., Wilson I.A., and Dwek R.A. Glycosylation and the immune system. Science 291 (2001) 2370-2376
52. Smith A.E., and Helenius A. How viruses enter animal cells. Science 304 (2004) 237-242
53. Tanabe A., Nakashima H., Yoshida O., Yamamoto N., Tenmyo O., and Oki T. Inhibitory effect of new antibiotic, pradimincin A on infectivity, cytopathic effect and replication of human immunodeficiency virus in vitro. J. Antibiot. (Tokyo) 41 (1988) 1708-1710
54. Tanabe-Tochikura A., Tochikura T.S., Yoshida O., Oki T., and Yamamoto N. Pradimicin A inhibition of human immunodeficiency virus: attenuation by mannan. Virology 176 (1990) 467-473
55. Tresnan D.B., Levis R., and Holmes K.V. Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J. Virol. 70 (1996) 8669-8674
56. Tsai C.C., Emau P., Jiang Y., Agy M.B., Shattock R.J., Schmidt A., Morton W.R., Gustafson K.R., and Boyd M.R. Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models. AIDS Res. Hum. Retroviruses 20 (2004) 11-18
57. Van Damme E.J.M., Peumans W.J., Pusztai A., and Bardocz S. Handbook of Plant Lectins: Properties and Biomedical Applications (1998), John Wiley & Sons, Chichester, New York
58. Vierheilig H., Iseli B., Alt M., Raikhel N., Wiemken A., and Boller T. Resistance of Urtica dioica to mycorrhizal colonization: a possible involvement of Urtica dioica agglutinin. Plant Soil. 183 (1996) 131-136
59. Vijgen L., Keyaerts E., Van Damme E., Peumans W., De Clercq E., Balzarini J., and Van Ranst M. Antiviral effect of plant compounds of the Alliaceae family against the SARS coronavirus. Proceedings of the 17th International Conference on Antiviral Research (2004) 123 (Antivir. Res. 62, A76)
60. Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S., Komarova N.L., Nowak M.A., Hahn B.H., Kwong P.D., and Shaw G.M. Antibody neutralization and escape by HIV-1. Nature 422 (2003) 307
61. Weiss M., Steck F., and Horzinek M.C. Purification and partial characterization of a new enveloped RNA virus (Berne virus). J. Gen. Virol. 64 Pt 9 (1983) 1849-1858
62. Westby M., Nakayama G.R., Butler S.L., and Blair W.S. Cell-based and biochemical screening approaches for the discovery of novel HIV-1 inhibitors. Antivir. Res. 67 (2005) 121
63. Wieczorek-Krohmer M., Weiland F., Conzelmann K., Kohl D., Visser N., van Woensel P., Thiel H.J., and Weiland E. Porcine reproductive and respiratory syndrome virus (PRRSV): monoclonal antibodies detect common epitopes on two viral proteins of European and U.S. isolates. Vet. Microbiol. 51 (1996) 257
64. Witvrouw M., Fikkert V., Hantson A., Pannecouque C., O'Keefe B.R., McMahon J., Stamatatos L., de Clercq E., and Bolmstedt A. Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirin N and concanavalin A. J. Virol. 79 (2005) 7777-7784
65. Ziolkowska N.E., O'Keefe B.R., Mori T., Zhu C., Giomarelli B., Vojdani F., Palmer K.E., McMahon J.B., and Wlodawer A. Domain-swapped structure of the potent antiviral protein griffithsin and its mode of carbohydrate binding. Structure 14 (2006) 1127-1135