Potent anti-respiratory syncytial virus activity of a cholestanol-sulfated tetrasaccharide conjugate

Antiviral Research

Volumn 93, Issue 1, 2012, Pages 101-109

  Lundin, Anna ^a   Bergström, Tomas ^a   Andrighetti Fröhner, Carla R ^a   Bendrioua, Loubna ^a   Ferro, Vito ^b   Trybala, Edward ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b Progen Pharmaceuticals Limited   (Australia)

Author keywords

PG545; Respiratory syncytial virus; Sulfated oligosaccharides; Virucidal activity

Indexed keywords

CHOLESTANOL; CHOLESTANOL CONJUGATED TETRASACCHARIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANTIVIRAL ACTIVITY; ARTICLE; CELL VIABILITY; CHEMICAL MODIFICATION; CHEMICAL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENCY; HUMAN; HUMAN CELL; IC 50; LIPOPHILICITY; NOSE SECRETION; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RESPIRATORY SYNCYTIAL VIRUS INFECTION; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS CHARACTERIZATION; VIRUS INHIBITION; VIRUS INTERFERENCE; VIRUS RESISTANCE;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE, TUMOR; DOGS; HUMANS; MICROBIAL SENSITIVITY TESTS; RESPIRATORY SYNCYTIAL VIRUSES; SAPONINS;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 84355166427     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2011.11.002     Document Type: Article

References (52)

1. Abrams D.I., Kuno S., Wong R., Jeffords K., Nash M., Molaghan J.B., Gorter R., Ueno R. Oral dextran sulfate (UA001) in the treatment of the acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. Ann. Intern. Med. 1989, 110:183-188.
2. Adamiak B., Ekblad M., Bergstrom T., Ferro V., Trybala E. Herpes simplex virus type 2 glycoprotein G is targeted by the sulfated oligo- and polysaccharide inhibitors of the virus attachment to cells. J. Virol. 2007, 81:13424-13434.
3. Adams T., Freeman C., Schwartz-Albiez R., Ferro V., Parish C.R., Andrews K.T. Inhibition of Plasmodium falciparum growth in vitro and adhesion to chondroitin-4-sulfate by the heparan sulfate mimetic PI-88 and other sulfated oligosaccharides. Antimicrob. Agents Chemother. 2006, 50:2850-28522.
4. Baba M., Snoeck R., Pauwels R., de Clercq E. 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. 1988, 32:1742-1745.
5. Carlucci M.J., Ciancia M., Matulewicz M.C., Cerezo A.S., Damonte E.B. Antiherpetic activity and mode of action of natural carrageenans of diverse structural types. Antivir. Res. 1999, 43:93-102.
6. Cheshenko N., Keller M.J., MasCasullo V., Jarvis G.A., Cheng H., John M., Li J.H., Hogarty K., Anderson R.A., Waller D.P., Zaneveld L.J., Profy A.T., Klotman M.E., Herold B.C. Candidate topical microbicides bind herpes simplex virus glycoprotein B and prevent viral entry and cell-to-cell spread. Antimicrob. Agents Chemother. 2004, 48:2025-2036.
7. Cochran S., Li C., Fairweather J.K., Kett W.C., Coombe D.R., Ferro V. Probing the interactions of phosphosulfomannans with angiogenic growth factors by surface plasmon resonance. J. Med. Chem. 2003, 46:4601-4608.
8. Cohen J. AIDS research. Microbicide fails to prevent against HIV. Science 2008, 319:1026-1027.
9. Cohen J. Novel HIV-fighting method finally gels. Sci. NOW Daily News 2009, 209:1.
10. Coil D.A., Miller A.D. Phosphatidylserine is not the cell surface receptor for vesicular stomatitis virus. J. Virol. 2004, 78:10920-10926.
11. Collins P.L., Graham B.S. Viral and host factors in human respiratory syncytial virus pathogenesis. J. Virol. 2008, 82:2040-2055.
12. Do T.Q., Moshkani S., Castillo P., Anunta S., Pogosyan A., Cheung A., Marbois B., Faull K.F., Ernst W., Chiang S.M., Fujii G., Clarke C.F., Foster K., Porter E. Lipids including cholesteryl linoleate and cholesteryl arachidonate contribute to the inherent antibacterial activity of human nasal fluid. J. Immunol. 2008, 181:4177-4187.
13. Dredge K., Hammond E., Davis K., Li C.P., Liu L., Johnstone K., Handley P., Wimmer N., Gonda T.J., Gautam A., Ferro V., Bytheway I. The PG500 series: novel heparan sulfate mimetics as potent angiogenesis and heparanase inhibitors for cancer therapy. Invest. New Drugs 2010, 28:276-283.
14. Dredge K., Hammond E., Handley P., Gonda T.J., Smith M.T., Vincent C., Brandt R., Ferro V., Bytheway I. PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and anti-metastatic efficacy in preclinical models. Br. J. Cancer 2011, 104:635-642.
15. Ekblad M., Adamiak B., Bergefall K., Nenonen H., Roth A., Bergstrom T., Ferro V., Trybala E. Molecular basis for resistance of herpes simplex virus type 1 mutants to the sulfated oligosaccharide inhibitor PI-88. Virology 2007, 367:244-252.
16. Ekblad M., Adamiak B., Bergstrom T., Johnstone K.D., Karoli T., Liu L., Ferro V., Trybala E. A highly lipophilic sulfated tetrasaccharide glycoside related to muparfostat (PI-88) exhibits virucidal activity against herpes simplex virus. Antivir. Res. 2010, 86:196-203.
17. Feldman S.A., Hendry R.M., Beeler J.A. Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J. Virol. 1999, 73:6610-6617.
18. Ferro, V., Karoli, T., Liu, L., Handley, P.N., Johnstone, K.D., Wimmer, N., Hammond, E.T., 2008. PCT international Application No. WO 2009049370 A1.
19. Ghildyal R., Hartley C., Varrasso A., Meanger J., Voelker D.R., Anders E.M., Mills J. Surfactant protein A binds to the fusion glycoprotein of respiratory syncytial virus and neutralizes virion infectivity. J. Infect. Dis. 1999, 180:2009-2013.
20. Hallak L.K., Collins P.L., Knudson W., Peeples M.E. Iduronic acid-containing glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology 2000, 271:264-275.
21. Hallak L.K., Kwilas S.A., Peeples M.E. Interaction between respiratory syncytial virus and glycosaminoglycans, including heparan sulfate. Meth. Mol. Biol. 2007, 379:15-34.
22. Ingallinella P., Bianchi E., Ladwa N.A., Wang Y.J., Hrin R., Veneziano M., Bonelli F., Ketas T.J., Moore J.P., Miller M.D., Pessi A. Addition of a cholesterol group to an HIV-1 peptide fusion inhibitor dramatically increases its antiviral potency. Proc. Natl. Acad. Sci. USA 2009, 106:5801-5806.
23. Johnson J.E., Gonzales R.A., Olson S.J., Wright P.F., Graham B.S. The histopathology of fatal untreated human respiratory syncytial virus infection. Mod. Pathol. 2007, 20:108-119.
24. Johnstone K.D., Karoli T., Liu L., Dredge K., Copeman E., Li C.P., Davis K., Hammond E., Bytheway I., Kostewicz E., Chiu F.C., Shackleford D.M., Charman S.A., Charman W.N., Harenberg J., Gonda T.J., Ferro V. Synthesis and biological evaluation of polysulfated oligosaccharide glycosides as inhibitors of angiogenesis and tumor growth. J. Med. Chem. 2010, 53:1686-1699.
25. Kimura K., Ishioka K., Hashimoto K., Mori S., Suzutani T., Bowlin T.L., Shigeta S. Isolation and characterization of NMSO3-resistant mutants of respiratory syncytial virus. Antivir. Res. 2004, 61:165-171.
26. Kimura K., Mori S., Tomita K., Ohno K., Takahashi K., Shigeta S., Terada M. Antiviral activity of NMSO3 against respiratory syncytial virus infection in vitro and in vivo. Antivir. Res. 2000, 47:41-51.
27. Kota S., Sabbah A., Chang T.H., Harnack R., Xiang Y., Meng X., Bose S. Role of human beta-defensin-2 during tumor necrosis factor-alpha/NF-kappaB-mediated innate antiviral response against human respiratory syncytial virus. J. Biol. Chem. 2008, 283:22417-22429.
28. Krusat T., Streckert H.J. Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. Arch. Virol. 1997, 142:1247-1254.
29. Kudchadkar R., Gonzalez R., Lewis K.D. PI-88: a novel inhibitor of angiogenesis. Expert Opin. Investig. Drugs 2008, 17:1769-1776.
30. Kwilas S., Liesman R.M., Zhang L., Walsh E., Pickles R.J., Peeples M.E. Respiratory syncytial virus grown in Vero cells contains a truncated attachment protein that alters its infectivity and dependence on glycosaminoglycans. J. Virol. 2009, 83:10710-10718.
31. Laube D.M., Yim S., Ryan L.K., Kisich K.O., Diamond G. Antimicrobial peptides in the airway. Curr. Top. Microbiol. Immunol. 2006, 306:153-182.
32. Lee E., Pavy M., Young N., Freeman C., Lobigs M. Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. Antivir. Res. 2006, 69:31-38.
33. Levine S., Klaiber-Franco R., Paradiso P.R. Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. J. Gen. Virol. 1987, 68:2521-2524.
34. Lewis F.A., Rae M.L., Lehmann N.I., Ferris A.A. A syncytial virus associated with epidemic disease of the lower respiratory tract in infants and young children. Med. J. Aust. 1961, 2:932-933.
35. Lundin A., Bergstrom T., Kann N., Adamiak B., Hannoun C., Trybala E. Two novel fusion inhibitors of human respiratory syncytial virus. Antivir. Res. 2010, 88:317-324.
36. McCarthy T.D., Karellas P., Henderson S.A., Giannis M., ÓKeefe D.F., Heery G., Paull J.R., Matthews B.R., Holan G. Dendrimers as drugs: discovery and preclinical and clinical development of dendrimer-based microbicides for HIV and STI prevention. Mol. Pharm. 2005, 2:312-318.
37. Monzon M.E., Casalino-Matsuda S.M., Forteza R.M. Identification of glycosaminoglycans in human airway secretions. Am. J. Respir. Cell Mol. Biol. 2006, 34:135-141.
38. Neyts J., De Clercq E. Effect of polyanionic compounds on intracutaneous and intravaginal herpesvirus infection in mice: impact on the search for vaginal microbicides with anti-HIV activity. J. Acquir. Immune Def. Synd. Hum. Retrovirol. 1995, 10:8-12.
39. Nyberg K., Ekblad M., Bergstrom T., Freeman C., Parish C.R., Ferro V., Trybala E. The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. Antivir. Res. 2004, 63:15-24.
40. Parish C.R., Freeman C., Brown K.J., Francis D.J., Cowden W.B. Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity. Cancer Res. 1999, 59:3433-3441.
41. Porotto M., Porotto M., Yokoyama C.C., Palermo L.M., Mungall B., Aljofan M., Cortese R., Pessi A., Moscona A. Viral entry inhibitors targeted to the membrane site of action. J. Virol. 2010, 84:6760-6768.
42. Rubin B.K. Physiology of airway mucus clearance. Respir. Care 2002, 47:761-768.
43. Said J., Trybala E., Andersson E., Johnstone K., Liu L., Wimmer N., Ferro V., Bergström T. Lipophile-conjugated sulfated oligosaccharides as novel microbicides against HIV-1. Antivir. Res. 2010, 86:286-295.
44. Techaarpornkul S., Barretto N., Peeples M.E. Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J. Virol. 2001, 75:6825-6834.
45. Vaheri A. Heparin and related polyionic substances as virus inhibitors. Acta Pathol. Microbiol. Scand. Suppl. 1964, 171:1-98.
46. Van de Wijgert J.H., Shattock R.J. Vaginal microbicides: moving ahead after an unexpected setback. AIDS 2007, 21:2369-2376.
47. Von Itzstein M., Wu W.Y., Kok G.B., Pegg M.S., Dyason J.C., Jin B., Van Phan T., Smythe M.L., White H.F., Oliver S.W., Colman P.M., Varghese J.N., Ryan D.M., Woods J.M., Bethell R.C., Hotham V.J., Cameron J.M., Penn C.R. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 1993, 363:418-423.
48. Welliver T.P., Garofalo R.P., Hosakote Y., Hintz K.H., Avendano L., Sanchez K., Velozo L., Jafri H., Chavez-Bueno S., Ogra P.L., McKinney L., Reed J.L., Welliver R.C. Severe human lower respiratory tract illness caused by respiratory syncytial virus and influenza virus is characterized by the absence of pulmonary cytotoxic lymphocyte responses. J. Infect. Dis. 2007, 195:1126-1136.
49. Witvrouw M., De Clercq E. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen. Pharmacol. 1997, 29:497-511.
50. Wyde P.R., Moylett E.H., Chetty S.N., Jewell A., Bowlin T.L., Piedra P.A. Comparison of the inhibition of human metapneumovirus and respiratory syncytial virus by NMSO3 in tissue culture assays. Antivir. Res. 2004, 63:51-59.
51. Zhang L., Bukreyev A., Thompson C.I., Watson B., Peeples M.E., Collins P.L., Pickles R.J. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J. Virol. 2005, 79:1113-1124.
52. Zhang L., Peeples M.E., Boucher R.C., Collins P.L., Pickles R.J. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J. Virol. 2002, 76:5654-5666.