Sulfated Escherichia coli K5 Polysaccharide Derivatives Inhibit Dengue Virus Infection of Human Microvascular Endothelial Cells by Interacting with the Viral Envelope Protein E Domain III

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Vervaeke, Peter ^a   Alen, Marijke ^a   Noppen, Sam ^a   Schols, Dominique ^a   Oreste, Pasqua ^a,b   Liekens, Sandra ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b Glycores 2000 Srl   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CD209 ANTIGEN; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN; HEPARIN LYASE; HEPARINASE II; MANNOSE RECEPTOR; POLYSACCHARIDE; PROTEOHEPARAN SULFATE; SULFATED ESCHERICHIA COLI K5 DERIVATIVE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS ENVELOPE PROTEIN E DOMAIN III;

ANTIVIRAL ACTIVITY; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DENGUE; DRUG PROTEIN BINDING; DRUG STRUCTURE; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; SKIN CELL; STRUCTURAL HOMOLOGY; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS INHIBITION;

AEDES; ANIMALS; CELL ADHESION MOLECULES; CELL LINE, TRANSFORMED; DENGUE; DENGUE VIRUS; ENDOTHELIAL CELLS; ESCHERICHIA COLI; HUMANS; LECTINS, C-TYPE; POLYSACCHARIDE-LYASES; POLYSACCHARIDES, BACTERIAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; VIRAL ENVELOPE PROTEINS;

EID: 84883415457     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074035     Document Type: Article

References (67)

1. World Health Organization (2012) Dengue and severe dengue. Fact sheet N°117. Available: http://www.who.int/mediacentre/factsheets/fs117/en/. Accessed 2013 Aug 5.
2. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, et al. (2010) Dengue: a continuing global threat. Nat Rev Microbiol 8: 7-16.
3. Mathew A, Rothman AL, (2008) Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol Rev 225: 300-313.
4. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, et al. (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745-748.
5. Whitehead SS, Blaney JE, Durbin AP, Murphy BR, (2007) Prospects for a dengue virus vaccine. Nat Rev Microbiol 5: 518-528.
6. Fang S, Wu Y, Wu N, Zhang J, An J (2013) Recent advances in DENV receptors. ScientificWorldJournal 2013: 684690.
7. Navarro-Sanchez E, Altmeyer R, Amara A, Schwartz O, Fieschi F, et al. (2003) Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 4: 723-728.
8. Miller JL, de Wet BJ, Martinez-Pomares L, Radcliffe CM, Dwek RA, et al. (2008) The mannose receptor mediates dengue virus infection of macrophages. PLoS Pathog 4: e17.
9. Jessie K, Fong MY, Devi S, Lam SK, Wong KT, (2004) Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 189: 1411-1418.
10. Balsitis SJ, Coloma J, Castro G, Alava A, Flores D, et al. (2009) Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. Am J Trop Med Hyg 80: 416-424.
11. Killen H, O'Sullivan MA, (1993) Detection of dengue virus by in situ hybridization. J Virol Methods 41: 135-146.
12. Zellweger RM, Prestwood TR, Shresta S, (2010) Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 7: 128-139.
13. Chen HC, Hofman FM, Kung JT, Lin YD, Wu-Hsieh BA, (2007) Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 81: 5518-5526.
14. Yen YT, Chen HC, Lin YD, Shieh CC, Wu-Hsieh BA, (2008) Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virol 82: 12312-12324.
15. Bonner SM, O'Sullivan MA, (1998) Endothelial cell monolayers as a model system to investigate dengue shock syndrome. J Virol Methods 71: 159-167.
16. Zamudio-Meza H, Castillo-Alvarez A, Gonzalez-Bonilla C, Meza I, (2009) Cross-talk between Rac1 and Cdc42 GTPases regulates formation of filopodia required for dengue virus type-2 entry into HMEC-1 cells. J Gen Virol 90: 2902-2911.
17. Dalrymple N, Mackow ER, (2011) Productive dengue virus infection of human endothelial cells is directed by heparan sulfate-containing proteoglycan receptors. J Virol 85: 9478-9485.
18. Arevalo MT, Simpson-Haidaris PJ, Kou Z, Schlesinger JJ, Jin X, (2009) Primary human endothelial cells support direct but not antibody-dependent enhancement of dengue viral infection. J Med Virol 81: 519-528.
19. Peyrefitte CN, Pastorino B, Grau GE, Lou J, Tolou H, et al. (2006) Dengue virus infection of human microvascular endothelial cells from different vascular beds promotes both common and specific functional changes. J Med Virol 78: 229-242.
20. Kanlaya R, Pattanakitsakul SN, Sinchaikul S, Chen ST, Thongboonkerd V, (2009) Alterations in actin cytoskeletal assembly and junctional protein complexes in human endothelial cells induced by dengue virus infection and mimicry of leukocyte transendothelial migration. J Proteome Res 8: 2551-2562.
21. Warke RV, Xhaja K, Martin KJ, Fournier MF, Shaw SK, et al. (2003) Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells. J Vrol 77: 11822-11832.
22. Warke RV, Martin KJ, Giaya K, Shaw SK, Rothman AL, et al. (2008) TRAIL is a novel antiviral protein against dengue virus. J Virol 82: 555-564.
23. Dalrymple NA, Mackow ER, (2012) Endothelial cells elicit immune-enhancing responses to dengue virus infection. J Virol 86: 6408-6415.
24. Avirutnan P, Malasit P, Seliger B, Bhakdi S, Husmann M, (1998) Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 161: 6338-6346.
25. Huang YH, Lei HY, Liu HS, Lin YS, Chen SH, et al. (2003) Tissue plasminogen activator induced by dengue virus infection of human endothelial cells. J Med Virol 70: 610-616.
26. Talavera D, Castillo AM, Dominguez MC, Gutierrez AE, Meza I, (2004) IL8 release, tight junction and cytoskeleton dynamic reorganization conducive to permeability increase are induced by dengue virus infection of microvascular endothelial monolayers. J Gen Virol 85: 1801-1813.
27. Huang YH, Lei HY, Liu HS, Lin YS, Liu CC, et al. (2000) Dengue virus infects human endothelial cells and induces IL-6 and IL-8 production. Am J Trop Med Hyg 63: 71-75.
28. Bosch I, Xhaja K, Estevez L, Raines G, Melichar H, et al. (2002) Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J Virol 76: 5588-5597.
29. Cardier JE, Mariño E, Romano E, Taylor P, Liprandi F, et al. (2005) Proinflammatory factors present in sera from patients with acute dengue infection induce activation and apoptosis of human microvascular endothelial cells: possible role of TNF-alpha in endothelial cell damage in dengue. Cytokine 30: 359-365.
30. Srikiatkhachorn A, Ajariyakhajorn C, Endy TP, Kalayanarooj S, Libraty DH, et al. (2007) Virus-induced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic fever. J Virol 81: 1592-1600.
31. Jiang Z, Tang X, Xiao R, Jiang L, Chen X, (2007) Dengue virus regulates the expression of haemostasis-related molecules in human vein endothelial cells. J Infect 55: 23-28.
32. Chen LC, Shyu HW, Lin HM, Lei HY, Lin YS, et al. (2009) Dengue virus induces thrombomodulin expression in human endothelial cells and monocytes in vitro. J Infect 58: 368-374.
33. Yeh TM, Liu SH, Lin KC, Kuo C, Kuo SY, et al. (2013) Dengue virus enhances thrombomodulin and ICAM-1 expression through the macrophage migration inhibitory factor induction of the MAPK and PI3K signaling pathways. PloS One 8: 55018.
34. Cabello-Gutierrez C, Manjarrez-Zavala ME, Huerta-Zepeda A, Cime-Castillo J, Monroy-Martinez V, et al. (2009) Modification of the cytoprotective protein C pathway during Dengue virus infection of human endothelial vascular cells. Thromb Haemost 101: 916-928.
35. Krishnamurti C, Peat RA, Cutting MA, Rothwell SW, (2002) Platelet adhesion to dengue-2 virus-infected endothelial cells. Am J Trop Med Hyg 66: 435-441.
36. Zhang JL, Wang JL, Gao N, Chen ZT, Tian YP, et al. (2007) Up-regulated expression of beta3 integrin induced by dengue virus serotype 2 infection associated with virus entry into human dermal microvascular endothelial cells. Biochem Biophys Res Commun 356: 763-768.
37. Basu A, Chaturvedi UC, (2008) Vascular endothelium: the battlefield of dengue viruses. FEMS Immunol Med Microbiol 53: 287-299.
38. Dalrymple NA, Mackow ER, (2012) Roles for endothelial cells in dengue virus infection. Adv Virol 2012: 840654.
39. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, et al. (1992) HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683-690.
40. Vicenzi E, Gatti A, Ghezzi S, Oreste P, Zoppetti G, et al. (2003) Broad spectrum inhibition of HIV-1 infection by sulfated K5 Escherichia coli polysaccharide derivatives. AIDS 17: 177-181.
41. Pinna D, Oreste P, Coradin T, Kajaste-Rudnitski A, Ghezzi S, et al. (2008) Inhibition of herpes simplex virus types 1 and 2 in vitro infection by sulfated derivatives of Escherichia coli K5 polysaccharide. Antimicrob Agents Chemother 52: 3078-3084.
42. Lembo D, Donalisio M, Rusnati M, Bugatti A, Cornaglia M, et al. (2008) Sulfated K5 Escherichia coli polysaccharide derivatives as wide-range inhibitors of genital types of human papillomavirus. Antimicrob Agents Chemother 52: 1374-1381.
43. Mercorelli B, Oreste P, Sinigalia E, Muratore G, Lembo D, et al. (2010) Sulfated derivatives of Escherichia coli K5 capsular polysaccharide are potent inhibitors of human cytomegalovirus. Antimicrob Agents Chemother 54: 4561-4567.
44. Vann WF, Schmidt MA, Jann B, Jann K, (1981) The structure of the capsular polysaccharide (K5 antigen) of urinary-tract-infective Escherichia coli 010:K5:H4. A polymer similar to desulfo-heparin. Eur J Biochem 116: 359-364.
45. Rusnati M, Vicenzi E, Donalisio M, Oreste P, Landolfo S, et al. (2009) Sulfated K5 Escherichia coli polysaccharide derivatives: A novel class of candidate antiviral microbicides. Pharmacol Ther 123: 310-322.
46. Matrosovich M, Matrosovich T, Garten W, Klenk HD, (2006) New low-viscosity overlay medium for viral plaque assays. Virol J 3: 63.
47. Leali D, Belleri M, Urbinati C, Coltrini D, Oreste P, et al. (2001) Fibroblast growth factor-2 antagonist activity and angiostatic capacity of sulfated Escherichia coli K5 polysaccharide derivatives. J Biol Chem 276: 37900-37908.
48. Van Damme EJ, Kaku H, Perini F, Goldstein IJ, Peeters B, et al. (1991) Biosynthesis, primary structure and molecular cloning of snowdrop (Galanthus nivalis L.) lectin. Eur J Biochem 202: 23-30.
49. Alen MM, De Burghgraeve T, Kaptein SJ, Balzarini J, Neyts J, et al. (2011) Broad antiviral activity of carbohydrate-binding agents against the four serotypes of dengue virus in monocyte-derived dendritic cells. PLoS One 6: e21658.
50. Aird WC, (2007) Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 100: 158-173.
51. Avirutnan P, Zhang L, Punyadee N, Manuyakorn A, Puttikhunt C, et al. (2007) Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PloS Pathog. 3: 183.
52. Bashirova AA, Geijtenbeek TB, van Duijnhoven GC, van Vliet SJ, Eilering JB, et al. (2001) A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J Exp Med 193: 671-678.
53. Mas-Moruno C, Rechenmacher F, Kessler H, (2010) Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer Agents Med Chem. 2010 10: 753-768.
54. Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD, et al. (1997) Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3: 866-871.
55. Hung SL, Lee PL, Chen HW, Chen LK, Kao CL, et al. (1999) Analysis of the steps involved in Dengue virus entry into host cells. Virology 257: 156-167.
56. Hilgard P, Stockert R, (2000) Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32: 1069-1077.
57. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, et al. (2002) Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology 292: 162-168.
58. Lin YL, Lei HY, Lin YS, Yeh TM, Chen SH, et al. (2002) Heparin inhibits dengue-2 virus infection of five human liver cell lines. Antiviral Res 56: 93-96.
59. Kato D, Era S, Watanabe I, Arihara M, Sugiura N, et al. (2010) Antiviral activity of chondroitin sulphate E targeting dengue virus envelope protein. Antiviral Res 88: 236-243.
60. Bishop JR, Schuksz M, Esko JD, (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446: 1030-1037.
61. Tripathi CK, Banga J, Mishra V, (2012) Microbial heparin/heparan sulphate lyases: potential and applications. Appl Microbiol Biotechnol 94: 307-321.
62. Lüscher-Mattli M, (2000) Polyanions - a lost chance in the fight against HIV and other virus diseases? Antivir Chem Chemother 11: 249-259.
63. Oreste P, Zoppetti G, (2012) Semi-synthetic heparinoids. Handb Exp Pharmacol 207: 403-422.
64. Zhu W, Li J, Liang G, (2011) How does cellular heparan sulfate function in viral pathogenicity? Biomed Environ Sci 24: 81-87.
65. de Witte L, Bobardt M, Chatterji U, Degeest G, David G, et al. (2007) Syndecan-3 is a dendritic cell-specific attachment receptor for HIV-1. PNAS 104: 19464-19469.
66. de Jong MA, de Witte L, Bolmstedt A, van Kooyk Y, Geijtenbeek TB, (2008) Dendritic cells mediate herpes simplex virus infection and transmission through the C-type lectin DC-SIGN. J Gen Virol 89: 2398-2409.
67. Watterson D, Kobe B, Young PR, (2012) Residues in domain III of the dengue virus envelope glycoprotein involved in cell-surface glycosaminoglycan binding. J Gen Virol 93: 72-82.