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Abstract:

The λ-carrageenan (λ-car) is a potent and selective inhibitor of dengue virus (DENV) infection targeted to virus adsorption and internalization, due to the structural similarities with the mammalian cell receptor heparan sulfate. To further characterize the antiviral activity of λ-car, the selection and the phenotypic and genomic features of λ-car resistant DENV-2 variants are studied here in comparison to control virus. Resistant variants were rapidly selected in Vero cells after three passages in presence of the drug. No difference was detected in the growth profiles in Vero and C6/36 cells between resistant and control viruses. By contrast, the kinetics of adsorption and internalization of resistant variants in Vero cells was significantly diminished whereas entry to C6/36 cells was unaffected. By plaque purification and sequence analysis of the population, two types of resistant clones were found: some clones presented two mutations in E protein, K126E, and F422L; but other equally λ-car resistant clones had no mutations in E. Furthermore, no mutations were found in other viral proteins like prM, C, or NS1. The genomic disparity in E protein was also associated to differences in phenotype stability. The stable genomic resistance here described provides information about determinants in E protein involved in receptor binding and membrane fusion for uncoating. © 2016 Wiley Periodicals, Inc.

Registro:

Documento: Artículo
Título:Characterization of in vitro dengue virus resistance to carrageenan
Autor:Talarico, L.B.; Damonte, E.B.
Filiación:Laboratory of Virology, Faculty of Sciences, Department of Biological Chemistry, University of Buenos Aires, Buenos Aires, Argentina
IQUIBICEN-National Research Council (CONICET), Ciudad Universitaria, Buenos Aires, Argentina
Palabras clave:Antiviral resistance; Carrageenans; Dengue virus; Sulfated polysaccharides; Virus entry; ammonium chloride; carrageenan; dextran sulfate; heparin; polysaccharide sulfate; antivirus agent; carrageenan; E protein TH Sman, Dengue virus; NS1 protein, Dengue virus type 2; viral protein; virus envelope protein; animal cell; antiviral activity; antiviral resistance; Article; conformational transition; controlled study; dengue; Dengue virus; Dengue virus 2; gene sequence; in vitro study; nonhuman; phenotype; receptor binding; Vero cell line; virus attachment; virus entry; virus isolation; animal; cell line; Chlorocebus aethiops; Dengue virus; drug effects; genetics; genotype; mutation; physiology; virus genome; virus replication; Animals; Antiviral Agents; Carrageenan; Cell Line; Cercopithecus aethiops; Dengue Virus; Drug Resistance, Viral; Genome, Viral; Genotype; Mutation; Phenotype; Vero Cells; Viral Envelope Proteins; Viral Nonstructural Proteins; Viral Proteins; Virus Replication
Año:2016
Volumen:88
Número:7
Página de inicio:1120
Página de fin:1129
DOI: http://dx.doi.org/10.1002/jmv.24457
Título revista:Journal of Medical Virology
Título revista abreviado:J. Med. Virol.
ISSN:01466615
CODEN:JMVID
CAS:ammonium chloride, 12125-02-9; carrageenan, 9000-07-1, 9049-05-2, 9061-82-9, 9064-57-7; dextran sulfate, 9011-18-1, 9042-14-2; heparin, 37187-54-5, 8057-48-5, 8065-01-8, 9005-48-5; polysaccharide sulfate, 79933-28-1; Antiviral Agents; Carrageenan; E protein TH Sman, Dengue virus; NS1 protein, Dengue virus type 2; Viral Envelope Proteins; Viral Nonstructural Proteins; Viral Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01466615_v88_n7_p1120_Talarico

Referencias:

  • Acosta, E.G., Piccini, L.E., Talarico, L.B., Castilla, V., Damonte, E.B., Changes in antiviral susceptibility to entry inhibitors and endocytic uptake of dengue-2 virus serially passaged in Vero or C6/36 cells (2014) Virus Res, 184, pp. 39-43
  • Alen, M.M.F., Dallmeier, K., Balzarini, J., Neyts, J., Schols, D., Crucial role of the N-glycans on the viral E-envelope glycoprotein in DC-SIGN-mediated dengue virus infection (2012) Antiviral Res, 96, pp. 280-287
  • Añez, G., Men, R., Eckels, K.H., Lai, C.-J., Passage of dengue virus type 4 vaccine candidates in fetal rhesus lung cells selects heparin-sensitive variants that result in loss of infectivity and immunogenicity in rhesus macaques (2009) J Virol, 83, pp. 10384-10394
  • Avirutnan, P., Zhang, L., Punyadee, N., Manuyakom, A., Puttikhunt, C., Kasinrerk, W., Malasit, P., Diamond, M.S., Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E (2007) PLoS Pathogens, 3, p. e183
  • Bhatt, S., Gething, P.W., Brady, O.J., Messina, J.P., Farlow, A.W., Moyes, C.L., Drake, J.M., Hay, S.I., The global distribution and burden of dengue (2013) Nature, 496, pp. 504-507
  • Castilla, V., Piccini, L.E., Damonte, E.B., Dengue virus entry and trafficking: Perspectives as antiviral target for prevention and therapy (2015) Future Virol, 10, pp. 625-645
  • Chen, Y., Maguire, T., Hileman, R.E., Fromm, J.R., Esko, J.D., Linhardt, R.J., Marks, R.M., Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate (1997) Nat Med, 3, pp. 866-871
  • Crill, W.D., Roehrig, J.T., Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells (2001) J Virol, 75, pp. 7769-7773
  • Dalrymple, N., Mackow, E.R., Productive dengue virus infection of human endothelial cells is directed by heparin sulfate-containing proteoglycan receptors (2011) J Virol, 85, pp. 9478-9485
  • Flipse, J., Wilschut, J., Smit, J.M., Molecular mechanisms involved in antibody-dependent enhancement of dengue virus infection in humans (2013) Traffic, 14, pp. 25-35
  • Germi, R., Crance, J.M., Garin, D., Guimet, J., Lortat-Jacob, H., Ruigrok, R.W., Zarski, J.P., Drouet, E., Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus (2002) Virology, 292, pp. 162-168
  • Guzmán, M.G., Halstead, S.B., Artsob, H., Buchy, P., Farrar, J., Gubler, D.J., Hunsperger, E., Peeling, R.W., Dengue: A continuing global threat (2010) Nat Rev Microbiol, 8, pp. S7-16
  • Halstead, S.B., Dengue (2007) Lancet, 370, pp. 1644-1652
  • Hilgard, P., Stockert, R., Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes (2000) Hepatology, 32, pp. 1069-1077
  • Hung, J.J., Hsieh, M.T., Young, M.J., Kao, C.L., King, C.C., Chang, W., An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells (2004) J Virol, 78, pp. 378-388
  • Hung, S.L., Lee, P.L., Chen, H.W., Chen, L.K., Kao, C.L., King, C.C., Analysis of the steps involved in Dengue virus entry into host cells (1999) Virology, 257, pp. 156-167
  • Ichiyama, K., Gopala Reddy, S.B., Zhang, L.F., Chin, W.X., Muschin, T., Heinig, L., Suzuki, Y., Yamamoto, N., Sulfated polysaccharide, curdlan sulfate, efficiently prevents entry/fusion and restricts antibody-dependent enhancement of dengue virus infection in vitro: A possible candidate for clinical application (2013) PLoS Negl Trop Dis, 7, p. e2188
  • Kuhn, R.J., Zhang, W., Rossmann, M.G., Pletnev, S.V., Corver, J., Lenches, E., Jones, C.T., Strauss, E.G., Structure of dengue virus: Implications for flavivirus organization, maturation, and fusion (2002) Cell, 108, pp. 717-725
  • Lee, E., Wright, P.J., Davidson, A., Lobigs, M., Virulence attenuation of Dengue virus due to augmented glycosaminoglycan-binding affinity and restriction in extraneural dissemination (2006) J Gen Virol, 87, pp. 2791-2801
  • Martinez-Barragan, J.J., del Angel, R.M., Identification of a putative coreceptor on Vero cells that participates in dengue 4 virus infection (2001) J Virol, 75, pp. 7818-7827
  • Modis, Y., Ogata, S., Clements, D., Harrison, S.C., A ligand-binding pocket in the dengue virus envelope glycoprotein (2003) Proc Natl Acad Sci USA, 100, pp. 6986-6991
  • Modis, Y., Ogata, S., Clements, D., Harrison, S.C., Structure of the dengue virus envelope protein after membrane fusion (2004) Nature, 427, pp. 313-319
  • Modis, Y., Ogata, S., Clements, D., Harrison, S.C., Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein (2005) J Virol, 79, pp. 1223-1231
  • Nicholas, K.B., Nicholas, H.B., Jr., Deerfield, D.W., II, Genedoc: A tool for editing and annotating multiple sequence alignments (1997) EMB NEW NEWS, 4, p. 14
  • Ohkuma, S., Poole, B., Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents (1978) Proc Natl Acad Sci USA, 75, pp. 3327-3331
  • Prestwood, T.R., Prigozhin, D.M., Sharar, K.L., Zellweger, R.M., Shresta, S., A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads (2008) J Virol, 82, pp. 8411-8421
  • Pujol, C.A., Ray, S., Ray, B., Damonte, E.B., Antiviral activity against dengue virus of diverse classes of algalsulfated polysaccharides (2012) Int J Biol Macromol, 51, pp. 412-416
  • Roehrig, J.T., Butrapet, S., Liss, N.M., Bennett, S.L., Luy, B.E., Childers, T., Boroughs, K.L., Huang, C.Y., Mutation of the dengue virus type 2 envelope protein heparan sulfate binding sites or the domain III lateral ridge blocks replication in Vero cells prior to membrane fusion (2013) Virology, 441, pp. 114-125
  • Smit, J.M., Moesker, B., Rodenhuis-Zybert, I., Wilschut, J., Flavivirus cell entry and membrane fusion (2011) Viruses, 3, pp. 160-171
  • Stiasny, K., Heinz, F.X., Flavivirus membrane fusion (2006) J Gen Virol, 87, pp. 2755-2766
  • Talarico, L.B., Damonte, E.B., Interference in dengue virus adsorption and uncoating by carrageenans (2007) Virology, 363, pp. 473-485
  • Talarico, L.B., Noseda, M.D., Ducatti, D.R.B., Duarte, M.E.R., Damonte, E.B., Differential inhibition of dengue virus infection in mammalian and mosquito cells by iota-carrageenan (2011) J Gen Virol, 92, pp. 1332-1342
  • Talarico, L.B., Pujol, C.A., Zibetti, R.G., Faria, P.C., Noseda, M.D., Duarte, M.E., Damonte, E.B., The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell (2005) Antiviral Res, 66, pp. 103-110
  • Tatusova, T.A., Madden, T.L., BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences (1999) FEMS Microbiol Lett, 174, pp. 247-250
  • Thaisomboonsuk, B.K., Clayson, E.T., Pantuwatana, S., Vaughn, D.W., Endy, T.P., Characterization of dengue-2 virus binding to surfaces of mammalian and insect cells (2005) Am J Trop Med Hyg, 72, pp. 375-383
  • Vervaeke, P., Alen, M., Noppen, S., Schols, D., Oreste, P., Liekens, S., Sulfated Escherichia coli K5 polysaccharide derivatives inhibit dengue virus infection of human microvascular endothelial cells by interacting with the viral envelope protein E domain II (2013) PLoS ONE, 8, p. e74035
  • Watterson, D., Kobe, B., Young, P.R., Residues in domain III of the dengue virus envelope glycoprotein involved in cell-surface glycosaminoglycan binding (2012) J Gen Virol, 93, pp. 72-82

Citas:

---------- APA ----------
Talarico, L.B. & Damonte, E.B. (2016) . Characterization of in vitro dengue virus resistance to carrageenan. Journal of Medical Virology, 88(7), 1120-1129.
http://dx.doi.org/10.1002/jmv.24457
---------- CHICAGO ----------
Talarico, L.B., Damonte, E.B. "Characterization of in vitro dengue virus resistance to carrageenan" . Journal of Medical Virology 88, no. 7 (2016) : 1120-1129.
http://dx.doi.org/10.1002/jmv.24457
---------- MLA ----------
Talarico, L.B., Damonte, E.B. "Characterization of in vitro dengue virus resistance to carrageenan" . Journal of Medical Virology, vol. 88, no. 7, 2016, pp. 1120-1129.
http://dx.doi.org/10.1002/jmv.24457
---------- VANCOUVER ----------
Talarico, L.B., Damonte, E.B. Characterization of in vitro dengue virus resistance to carrageenan. J. Med. Virol. 2016;88(7):1120-1129.
http://dx.doi.org/10.1002/jmv.24457