Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses

Antiviral Research

Volumn 69, Issue 1, 2006, Pages 31-38

  Lee, Eva ^a   Pavy, Megan ^a   Young, Nicolie ^a   Freeman, Craig ^a   Lobigs, Mario ^a  

^a Biology and Environment   (Australia)

Author keywords

Flavivirus; Heparan sulfate mimetic; Japanese encephalitis virus; West Nile virus

Indexed keywords

ANTIVIRUS AGENT; HEPARAN SULFATE; PENTOSAN POLYSULFATE; PI 88; SURAMIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENGUE VIRUS; DRUG EFFICACY; FLAVIVIRUS; FLOW CYTOMETRY; IN VITRO STUDY; JAPANESE ENCEPHALITIS VIRUS; MOUSE; MURRAY VALLEY ENCEPHALITIS VIRUS; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTIVITY; VIRUS STRAIN; WEST NILE FLAVIVIRUS;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; DENGUE; DENGUE VIRUS; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; ENCEPHALITIS VIRUSES, JAPANESE; ENCEPHALITIS, ARBOVIRUS; FEMALE; FLAVIVIRUS INFECTIONS; HEPARITIN SULFATE; INJECTIONS, INTRAPERITONEAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGOSACCHARIDES; PENTOSAN SULFURIC POLYESTER; SURAMIN; TREATMENT OUTCOME;

ANIMALIA; DENGUE VIRUS; FLAVIVIRUS; JAPANESE ENCEPHALITIS VIRUS; MURRAY VALLEY ENCEPHALITIS VIRUS; WEST NILE VIRUS;

EID: 29044443281     PISSN: 01663542     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.antiviral.2005.08.006     Document Type: Article

References (45)

1. M. Baba, R. Snoeck, R. Pauwels, and E. de Clercq Sulfated polysaccharides are potent and selective inhibitors of various enveloped viruses, including herpes simplex virus, cytomegalovirus, vesicular stomatitis virus, and human immunodeficiency virus Antimicrob. Agents Chemother. 32 1988 1742 1745
2. B. Bartolini, A. Di Caro, R.A. Cavallaro, L. Liverani, G. Mascellani, G. La Rosa, C. Marianelli, M. Muscillo, A. Benedetto, and L. Cellai Susceptibility to highly sulphated glycosaminoglycans of human immunodeficiency virus type 1 replication in peripheral blood lymphocytes and monocyte-derived macrophages cell cultures Antivir. Res. 58 2003 139 147
3. M. Bernfield, M. Götte, P.W. Park, O. Reizes, M.L. Firzgerald, J. Lincecum, and M. Zako Functions of cell surface heparan sulfate proteoglycans Annu. Rev. Biochem. 68 1999 729 777
4. D.S. Burke, and T.P. Monath Flaviviruses D.M. Knipe P.M. Howley Fields Virology fourth ed. 2001 Lippincott Williams & Wilkins Philadelphia, PA 1043 1126
5. Y. Chen, T. Maguire, R.E. Hileman, J.R. Fromm, J.D. Esko, R.J. Linhardt, and R.M. Marks Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate Nat. Med. 3 1997 866 871
6. E. De Clercq Antivirals and antiviral strategies Nat. Rev. Microbiol. 2 2004 704 720
7. V. Ferro, C. Li, K. Fewings, M.C. Palermo, R.J. Linhardt, and T. Toida Determination of the composition of the oligosaccharide phosphate fraction of Pichia (Hansenula) holstii NRRL Y-2448 phosphomannan by capillary electrophoresis and HPLC Carbohydr. Res. 337 2002 139 146
8. E.L. French Murray Valley encephalitis isolation and characterization of the aetiological agent Med. J. Aust. 1 1952 100 103
9. A. Goto, D. Hayasaka, K. Yoshii, T. Mizutani, H. Kariwa, and I. Takashima A BHK-21 cell culture-adapted tick-borne encephalitis virus mutant is attenuated for neuroinvasiveness Vaccine 21 2003 4043 4051
10. D.J. Gubler Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century Trends Microbiol. 10 2002 100 103
11. R.A. Hall, B.H. Kay, G.W. Burgess, P. Clancy, and I.D. Fanning Epitope analysis of the envelope and non-structural glycoproteins of Murray Valley encephalitis virus J. Gen. Virol. 71 1990 2923 2930
12. A.J. Johnson, and J.T. Roehrig New mouse model for dengue virus vaccine testing J. Virol. 73 1999 783 786
13. G.B. Johnson, G.J. Brunn, Y. Kodaira, and J.L. Platt Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by toll-like receptor 4 J. Immunol. 168 2002 5233 5239
14. G.B. Johnson, G.J. Brunn, and J.L. Platt Cutting edge: an endogenous pathway to systemic inflammatory response syndrome (SIRS)-like reactions through toll-like receptor 4 J. Immunol. 172 2004 20 24
15. J.A. Joyce, C. Freeman, N. Meyer-Morse, C.R. Parish, and D. Hanahan A functional heparan sulfate mimetic implicates both heparanase and heparan sulfate in tumor angiogenesis and invasion in a mouse model of multistage cancer Oncogene 24 2005 4037 4051
16. R.S. Lanciotti, J.T. Roehrig, V. Deubel, J. Smith, M. Parker, K. Steele, B. Crise, K.E. Volpe, M.B. Crabtree, J.H. Scherret, R.A. Hall, J.S. MacKenzie, C.B. Cropp, B. Panigrahy, E. Ostlund, B. Schmitt, M. Malkinson, C. Banet, J. Weissman, N. Komar, H.M. Savage, W. Stone, T. McNamara, and D.J. Gubler Origin of the West Nile virus responsible for an outbreak of encephalitis in the north-eastern United States Science 286 1999 2333 2337
17. E. Lee, R.A. Hall, and M. Lobigs Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses J. Virol. 78 2004 8271 8280
18. E. Lee, and M. Lobigs Substitutions at the putative receptor-binding site of an encephalitic flavivirus alter virulence and host cell tropism and reveal a role for glycosaminoglycans in entry J. Virol. 74 2000 8867 8875
19. E. Lee, and M. Lobigs Mechanism of virulence attenuation of glycosaminoglycan-binding variants of Japanese encephalitis virus and Murray Valley encephalitis virus J. Virol. 76 2002 4901 4911
20. R.M. Licon Luna, E. Lee, A. Müllbacher, R.V. Blanden, R. Langman, and M. Lobigs Lack of both Fas ligand and perforin protects from flavivirus-mediated encephalitis in mice J. Virol. 76 2002 3202 3211
21. Y.L. Lin, H.Y. Lei, Y.S. Lin, T.M. Yeh, S.H. Chen, and H.S. Liu Heparin inhibits dengue-2 virus infection of five human liver cell lines Antivir. Res. 56 2002 93 96
22. M. Lobigs, I.D. Marshall, R.C. Weir, and L. Dalgarno Genetic differentiation of Murray Valley encephalitis virus in Australia and Papua New Guinea Aust. J. Exp. Biol. Med. Sci. 64 1986 571 585
23. M. Lobigs, R. Usha, A. Nestorowicz, I.D. Marshall, R.C. Weir, and L. Dalgarno Host cell selection of Murray Valley encephalitis virus variants altered at an RGD sequence in the envelope protein and in mouse virulence Virology 176 1990 587 595
24. M. Lyon, J.A. Deakin, and J.T. Gallagher Liver heparan sulfate structure. A novel molecular design J. Biol. Chem. 269 1994 11208 11215
25. J.S. Mackenzie, D.J. Gubler, and L.R. Petersen Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses Nat. Med. 10 2004 S98 S109
26. J.S. Mackenzie, M.D. Lindsay, R.J. Coelen, A.K. Broom, R.A. Hall, and D.W. Smith Arboviruses causing human disease in the Australasian zoogeographic region Arch. Virol. 136 1994 447 467
27. J.P. Maffrand, J.M. Herbert, A. Bernat, G. Defreyn, D. Delebassee, P. Savi, J.J. Pinot, and J. Sampol Experimental and clinical pharmacology of pentosan polysulfate Semin. Thromb. Hemost. 2 Suppl. 17 1991 186 198
28. C.W. Mandl, H. Kroschewski, S.L. Allison, R. Kofler, H. Holzmann, T. Meixner, and F.X. Heinz Adaptation of tick-borne encephalitis virus to BHK-21 cells results in the formation of multiple heparan sulfate binding sites in the envelope protein and attenuation in vivo J. Virol. 75 2001 5627 5637
29. R.M. Marks, H. Lu, R. Sundaresan, T. Toida, A. Suzuki, T. Imanari, M.J. Hernaiz, and R.J. Linhardt Probing the interaction of dengue virus envelope protein with heparin: assessment of glycosaminoglycan-derived inhibitors J. Med. Chem. 44 2001 2178 2187
30. Y. Modis, S. Ogata, D. Clements, and S.C. Harrison A ligand-binding pocket in the dengue virus envelope glycoprotein Proc. Natl. Acad. Sci. U.S.A. 100 2003 6986 6991
31. T.P. Monath Japanese encephalitis vaccines: current vaccines and future prospects Curr. Top. Microbiol. Immunol. 267 2002 105 138
32. J. Neyts, A. Meerbach, P. McKenna, and E. De Clercq Use of the yellow fever virus vaccine strain 17D for the study of strategies for the treatment of yellow fever virus infections Antivir. Res. 30 1996 125 132
33. K. Nyberg, M. Ekblad, T. Bergstrom, C. Freeman, C.R. Parish, V. Ferro, and E. Trybala The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus Antivir. Res. 63 2004 15 24
34. L. Ono, W. Wollinger, I.M. Rocco, T.L. Coimbra, P.A. Gorin, and M.R. Sierakowski In vitro and in vivo antiviral properties of sulfated galactomannans against yellow fever virus (BeH111 strain) and dengue 1 virus (Hawaii strain) Antivir. Res. 60 2003 201 208
35. C.R. Parish, C. Freeman, K.J. Brown, D.J. Francis, and W.B. Cowden Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity Cancer Res. 59 1999 3433 3441
36. F.A. Rey, F.X. Heinz, C. Mandl, C. Kunz, and S.C. Harrison The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution Nature 375 1995 291 298
37. P.Y. Shi Strategies for the identification of inhibitors of West Nile virus and other flaviviruses Curr. Opin. Investig. Drugs 3 2002 1567 1573
38. T. Solomon, and D.W. Vaughn Pathogenesis and clinical features of Japanese encephalitis and West Nile virus infections Curr. Top. Microbiol. Immunol. 267 2002 171 194
39. L.B. Talarico, C.A. Pujol, R.G. Zibetti, P.C. Faria, M.D. Noseda, M.E. Duarte, and E.B. Damonte The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell Antivir. Res. 66 2005 103 110
40. P. Thullier, C. Demangel, H. Bedouelle, F. Megret, A. Jouan, V. Deubel, J.C. Mazie, and P. Lafaye Mapping of a dengue virus neutralizing epitope critical for the infectivity of all serotypes: insight into the neutralization mechanism J. Gen. Virol. 82 2001 1885 1892
41. M.F. van den Broek, U. Muller, S. Huang, M. Aguet, and R.M. Zinkernagel Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors J. Virol. 69 1995 4792 4796
42. T.E. Voogd, E.L. Vansterkenburg, J. Wilting, and L.H. Janssen Recent research on the biological activity of suramin Pharmacol. Rev. 45 1993 177 203
43. + T cells mediate recovery and immunopathology in West Nile virus encephalitis J. Virol. 77 2003 13323 13334
44. L.E. Wrenshall, R.B. Stevens, F.B. Cerra, and J.L. Platt Modulation of macrophage and B cell function by glycosaminoglycans J. Leukoc. Biol. 66 1999 391 400
45. G. Yu, N.S. Gunay, R.J. Linhardt, T. Toida, J. Fareed, D.A. Hoppensteadt, H. Shadid, V. Ferro, C. Li, K. Fewings, M.C. Palermo, and D. Podger Preparation and anticoagulant activity of the phosphosulfomannan PI-88 Eur. J. Med. Chem. 37 2002 783 791