Intracytoplasmic trapping of influenza virus by a lipophilic derivative of aglycoristocetin

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9416-9431

  Vanderlinden, Evelien ^a   Vanstreels, Els ^a   Boons, Eline ^a   ter Veer, Wouter ^c   Huckriede, Anke ^c   Daelemans, Dirk ^a   Van Lommel, Alfons ^d   Röth, Erzsébet ^b   Sztaricskai, Ferenc ^b   Herczegh, Pàl ^b   Naesens, Lieve ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; ANTIVIRUS AGENT; GLYCOPEPTIDE; INFLUENZA VIRUS HEMAGGLUTININ; OSELTAMIVIR; SA 19; SA 48; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DOG; DRUG EFFECT; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; EMBRYO; HUMAN; HUMAN CELL; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS B; KIDNEY CELL; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; VIRUS CONCENTRATION; VIRUS ENTRY; VIRUS INHIBITION; VIRUS RESISTANCE;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CYTOPLASM; DOGS; GLYCOPEPTIDES; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA, HUMAN; MOLECULAR STRUCTURE; VIRUS INTERNALIZATION; VIRUS REPLICATION;

CERCOPITHECINE HERPESVIRUS 1; ORTHOMYXOVIRIDAE; VESICULAR STOMATITIS VIRUS;

EID: 84866175162     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.07032-11     Document Type: Article

References (67)

1. Balzarini J, et al. 2006. Inhibition of feline (FIPV) and human (SARS) coronavirus by semisynthetic derivatives of glycopeptide antibiotics. Antiviral Res. 72:20-33. doi:10.1016/j.antiviral.2006.03.005.
2. Balzarini J, et al. 2003. Antiretroviral activity of semisynthetic derivatives of glycopeptide antibiotics. J. Med. Chem. 46:2755-2764.
3. Bardsley B, Williams DH, Baglin TP. 1998. Cleavage of rhamnose from ristocetin A removes its ability to induce platelet aggregation. Blood Coagul. Fibrinolysis. 9:241-244.
4. a.Bauer K, Richter M, Wutzler P, Schmidtke M. 2009. Different neuraminidase inhibitor susceptibilities of human H1N1, H1N2, and H3N2 influenzaAviruses isolated in Germany from 2001 to 2005/2006. Antiviral Res.. 82:34-41.
5. Belser JA, et al. 2007. DAS181, a novel sialidase fusion protein, protects mice from lethal avian influenza H5N1 virus infection. J. Infect. Dis. 196:1493-1499.
6. Bertaux C, et al. 2007. Entry of hepatitis C virus and human immunodeficiency virus is selectively inhibited by carbohydrate-binding agents but not by polyanions. Virology. 366:40-50. doi:10.1016/j.virol.2007.04.008.
7. Cross KJ, Burleigh LM, Steinhauer DA. 2001. Mechanisms of cell entry by influenza virus. Expert Rev. Mol. Med. 3:1-18.
8. Crowley BM, Mori Y, McComas CC, Tang D, Boger DL. 2004. Total synthesis of the ristocetin aglycon. J. Am. Chem. Soc. 126:4310-4317.
9. Daniels RS, et al. 1985. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell. 40:431-439.
10. De Clercq E. 2006. Antiviral agents active against influenza A viruses. Nat. Rev. Drug Discov. 5:1015-1025. doi:10.1038/nrd2175.
11. de Jonge J, et al. 2007. Cellular gene transfer mediated by influenza virosomes with encapsulated plasmid DNA. Biochem. J. 405:41-49.
12. Deyde VM, et al. 2007. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J. Infect. Dis. 196:249-257.
13. Domenech O, Dufrene YF, Van Bambeke F, Tukens PM, Mingeot-Leclercq MP. 2010. Interactions of oritavancin, a new semi-synthetic lipoglycopeptide, with lipids extracted from Staphylococcus aureus. Biochim. Biophys. Acta. 1798:1876-1885.
14. Ehrhardt C, Ludwig S. 2009. A new player in a deadly game: influenza viruses and the PI3K/Akt signalling pathway. Cell Microbiol. 11:863-871. doi:10.1111/j.1462-5822.2009.01309.x.
15. Finnen RL, et al. 2006. Postentry events are responsible for restriction of productive varicella-zoster virus infection in Chinese hamster ovary cells. J. Virol. 80:10325-10334. doi:10.1128/JVI.00939-06.
16. Fukuyama S, Kawaoka Y. 2011. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr. Opin. Immunol. 23:481-486.
17. Gamblin SJ, et al. 2004. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science. 303:1838-1842. doi:10.1126/ science.1093155.
18. Gruenberg J. 2001. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2:721-730.
19. Gubareva LV. 2004. Molecular mechanisms of influenza virus resistance to neuraminidase inhibitors. Virus Res. 103:199-203. doi:10.1016/j.virusres.2004.02.034.
20. Hambleton S, Steinberg SP, Gershon MD, Gershon AA. 2007. Cholesterol dependence of varicella-zoster virion entry into target cells. J. Virol. 81:7548-7558. doi:10.1128/JVI.00486-07.
21. Harada S, Yokomizo K, Monde K, Maeda Y, Yusa K. 2007. A broad antiviral neutral glycolipid, fattiviracin FV-8, is a membrane fluidity modulator. Cell Microbiol. 9:196-203. doi:10.1111/j.1462-5822.2006.00781.x.
22. Ikeda S, et al. 1994. In vitro and in vivo inhibition of ortho-and paramyxovirus infections by a new class of sulfonic acid polymers interacting with virus-cell binding and/or fusion. Antimicrob. Agents Chemother. 38:256-259.
23. Johansson SM, et al. 2007. Multivalent sialic acid conjugates inhibit adenovirus type 37 from binding to and infecting human corneal epithelial cells. Antiviral Res. 73:92-100. doi:10.1016/j.antiviral.2006.08.004.
24. Kang M, Wilson L, Kermode JC. 2008. Evidence from limited proteolysis of a ristocetin-induced conformational change in human von Willebrand factor that promotes its binding to platelet glycoprotein Ib-IX-V. Blood Cells Mol. Dis. 40:433-443.
25. Kao RY, et al. 2010. Identification of influenza A nucleoprotein as an antiviral target. Nat. Biotechnol. 28:600-605. doi:10.1038/nbt.1638.
26. Kimura K, et al. 2000. Antiviral activity of NMSO3 against respiratory syncytial virus infection in vitro and in vivo. Antiviral Res. 47:41-51. doi: 10.1016/S0166-3542(00)00091-7.
27. Kiso M, et al. 2004. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet. 364:759-765. doi:10.1016/S0140-6736(04)16934-1.
28. Kobayashi T, et al. 1999. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol. 1:113-118.
29. Leneva IA, Russell RJ, Boriskin YS, Hay AJ. 2009. Characteristics of arbidol-resistant mutants of influenza virus: implications for the mechanism of anti-influenza action of arbidol. Antiviral Res. 81:132-140. doi: 10.1016/j.antiviral.2008.10.009.
30. Matrosovich M, Matrosovich T, Carr J, Roberts NA, Klenk HD. 2003. Overexpression of the alpha-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J. Virol. 77:8418-8425. doi: 10.1128/JVI.77.15.8418-8425.2003.
31. Matsuda T, Cepko CL. 2004. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl. Acad. Sci. U. S. A. 101:16-22.
32. Mayor S, Pagano RE. 2007. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8:603-612.
33. Medts T, et al. 2010. Acute ligand-independent Src activation mimics low EGF-induced EGFR surface signalling and redistribution into recycling endosomes. Exp. Cell Res. 316:3239-3253.
34. Mohri H, et al. 1997. Synthetic peptide from the V3 loop consensus motif with a potent anti-HIV activity inhibits ristocetin-mediated vWF-GPIb interaction. Peptides. 18:1289-1293. doi:10.1016/S0196-9781(97)00205-2.
35. Moscona A. 2008. Medical management of influenza infection. Annu. Rev. Med. 59:397-413.
36. Moscona A. 2009. Global transmission of oseltamivir-resistant influenza. N. Engl. J. Med. 360:953-956.
37. Naesens L, et al. 2009. Anti-influenza virus activity and structure-activity relationship of aglycoristocetin derivatives with cyclobutenedione carrying hydrophobic chains. Antiviral Res. 82:89-94. doi:10.1016/ j.antiviral.2009.01.003.
38. Obeid S, et al. 2011. Inhibition of hepatitis C virus replication by semisynthetic derivatives of glycopeptide antibiotics. J. Antimicrob. Chemother. 66:1287-1294.
39. Pintér G, et al. 2009. Diazo transfer-click reaction route to new, lipophilic teicoplanin and ristocetin aglycon derivatives with high antibacterial and anti-influenza virus activity: an aggregation and receptor binding study. J. Med. Chem. 52:6053-6061.
40. Pintér G, et al. 2010. Click reaction synthesis of carbohydrate derivatives from ristocetin aglycon with antibacterial and antiviral activity. Bioorg. Med. Chem. Lett. 20:2713-2717.
41. Piper RC, Katzmann DJ. 2007. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23:519-547.
42. Pitkin DH, Mico BA, Sitrin RD, Nisbet LJ. 1986. Charge and lipophilicity govern the pharmacokinetics of glycopeptide antibiotics. Antimicrob. Agents Chemother. 29:440-444.
43. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Epidemiol. 27:493-497.
44. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. 2005. Rab conversion as a mechanism of progression from early to late endosomes. Cell. 122:735-749. doi:10.1016/j.cell.2005.06.043.
45. Roche S, Albertini AA, Lepault J, Bressanelli S, Gaudin Y. 2008. Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited. Cell. Mol. Life Sci. 65:1716-1728. doi:10.1007/s00018-008-7534-3.
46. Root CN, Wills EG, McNair LL, Whittaker GR. 2000. Entry of influenza viruses into cells is inhibited by a highly specific protein kinaseCinhibitor. J. Gen. Virol. 81:2697-2705.
47. Russell RJ, et al. 2008. Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 105:17736-17741.
48. Rust MJ, Lakadamyali M, Zhang F, Zhuang X. 2004. Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat. Struct. Mol. Biol. 11:567-573.
49. Schmolke M, Viemann D, Roth J, Ludwig S. 2009. Essential impact of NF-kappaB signaling on the H5N1 influenza A virus-induced transcriptome. J. Immunol. 183:5180-5189. doi:10.4049/jimmunol.0804198.
50. Sherer NM, et al. 2003. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic. 4:785-801. doi: 10.1034/j.1600-0854.2003.00135.x.
51. Shichiri M, et al. 2012. A novel role for alpha-tocopherol transfer protein (alpha-TTP) in protecting against chloroquine toxicity. J. Biol. Chem. 287:2926-2934.
52. Sieczkarski SB, Whittaker GR. 2002. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76:10455-10464. doi:10.1128/JVI.76.20.10455-10464.2002.
53. Sieczkarski SB, Whittaker GR. 2003. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic. 4:333-343. doi:10.1034/j.1600-0854.2003.00090.x.
54. Suzuki Y, Kato H, Naeve CW, Webster RG. 1989. Single-amino-acid substitution in an antigenic site of influenza virus hemagglutinin can alter the specificity of binding to cell membrane-associated gangliosides. J. Virol. 63:4298-4302.
55. Sztaricskai F, et al. 2006. A new series of glycopeptide antibiotics incorporating a squaric acid moiety. Synthesis, structural and antibacterial studies. J. Antibiot. (Tokyo). 59:564-582.
56. Sztaricskai F, et al. 2007. N-glycosylthioureido aglyco-ristocetins without platelet aggregation activity. J. Antibiot. (Tokyo). 60:529-533.
57. Ulm JW, Perron M, Sodroski J, Mulligan C. 2007. Complex determinants within the Moloney murine leukemia virus capsid modulate susceptibility tibility of the virus to Fv1 and Ref1-mediated restriction. Virology. 363:245-255. doi:10.1016/j.virol.2006.09.048.
58. Van Bambeke F. 2004. Glycopeptides in clinical development: pharmacological profile and clinical perspectives. Curr. Opin. Pharmacol. 4:471-478.
59. Van Bambeke F, Saffran J, Mingeot-Leclercq MP, Tulkens PM. 2005. Mixed-lipid storage disorder induced in macrophages and fibroblasts by oritavancin (LY333328), a new glycopeptide antibiotic with exceptional cellular accumulation. Antimicrob. Agents Chemother. 49:1695-1700. doi:10.1128/AAC.49.5.1695-1700.2005.
60. Vanderlinden E, et al. 2010. Novel inhibitors of influenza virus fusion: structure-activity relationship and interaction with the viral hemagglutinin. J. Virol. 84:4277-4288. doi:10.1128/JVI.02325-09.
61. Veit M, Thaa B. 25 July 2011, posting date. Association of influenza virus proteins with membrane rafts. Adv. Virol. 2011: 370606.
62. Villalaín J. 2010. Membranotropic effects of arbidol, a broad anti-viral molecule, on phospholipid model membranes. J. Phys. Chem. B. 114:8544-8554.
63. Wang W, et al. 2010. A mutation in the receptor binding site enhances infectivity of 2009 H1N1 influenza hemagglutinin pseudotypes without changing antigenicity. Virology. 407:374-380. doi:10.1016/ j.virol.2010.08.027.
64. Wilson JM, et al. 2000. EEA1, a tethering protein of the early sorting endosome, shows a polarized distribution in hippocampal neurons, epithelial cells, and fibroblasts. Mol. Biol. Cell. 11:2657-2671.
65. Wolf MC, et al. 2010. A broad-spectrum antiviral targeting entry of enveloped viruses. Proc. Natl. Acad. Sci. U. S. A. 107:3157-3162.
66. Xu R, Wilson IA. 2011. Structural characterization of an early fusion intermediate of influenza virus hemagglutinin. J. Virol. 85:5172-5182. doi:10.1128/JVI.02430-10.
67. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y. 1991. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 266:17707-17712.