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Abstract:

The endocytic uptake and intracellular trafficking for penetration of DENV-3 strain H-87 into Vero cells was analyzed by using several biochemical inhibitors and dominant negative mutants of cellular proteins. The results presented show that the infective entry of DENV-3 into Vero cells occurs through a non-classical endocytosis pathway dependent on low pH and dynamin, but non-mediated by clathrin. After uptake, DENV-3 transits through early endosomes to reach Rab 7-regulated late endosomes, and according with the half-time for ammonium chloride resistance viral nucleocapsid is released into the cytosol approximately at 12 min post-infection. Furthermore, the influence of the clathrin pathway in DENV-3 infective entry in other mammalian cell lines of human origin, such as A549, HepG2 and U937 cells, was evaluated demonstrating that variable entry pathways are employed depending on the host cell. Results show for the first time the simultaneous coexistence of infective and non -infective routes for DENV entry into the host cell, depending on the usage of clathrin-mediated endocytosis. © 2015 Piccini et al This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Registro:

Documento: Artículo
Título:Dengue-3 virus entry into vero cells: Role of clathrin-mediated endocytosis in the outcome of infection
Autor:Piccini, L.E.; Castilla, V.; Damonte, E.B.
Filiación:Laboratorio de Virología, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
IQUIBICEN, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ciudad Universitaria, Buenos Aires, Argentina
Palabras clave:ammonium chloride; clathrin; dynamin; Rab7 protein; clathrin; animal cell; Article; cell transport; controlled study; cytosol; dengue; Dengue virus 3; endocytosis; endosome; human; human cell; mammal cell; nonhuman; pH; virus cell interaction; virus entry; virus nucleocapsid; Aedes; animal; cell culture; Chlorocebus aethiops; dengue; Dengue virus; endocytosis; Hep-G2 cell line; metabolism; microbial sensitivity test; pathology; physiology; prognosis; U-937 cell line; Vero cell line; virology; Aedes; Animals; Cells, Cultured; Cercopithecus aethiops; Clathrin; Dengue; Dengue Virus; Endocytosis; Hep G2 Cells; Humans; Microbial Sensitivity Tests; Prognosis; U937 Cells; Vero Cells; Virus Internalization
Año:2015
Volumen:10
Número:10
DOI: http://dx.doi.org/10.1371/journal.pone.0140824
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CODEN:POLNC
CAS:ammonium chloride, 12125-02-9; dynamin; Rab7 protein, 185229-47-4; Clathrin
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v10_n10_p_Piccini

Referencias:

  • Halstead, S.B., Dengue (2007) Lancet., 370, pp. 1644-1652. , 17993365
  • Kyle, J.L., Harris, E., Global spread and persistence of dengue (2008) Annu Rev Microbiol., 62, pp. 71-92. , 18429680
  • Guzmán, M.G., Halstead, S.B., Artsob, H., Buchy, P., Farrar, J., Gubler, D.J., Dengue: A continuing global threat (2010) Nat Rev Microbiol., 8, pp. S7-S16. , 21079655
  • Sampath, A., Padmanabhan, R., Molecular targets for flavivirus drug discovery (2009) Antiviral Res., 81, pp. 6-15. , 18796313
  • Noble, C.G., Chen, Y.-L., Dong, H., Gu, F., Lim, S.P., Schul, W., Strategies for development of dengue virus inhibitors (2010) Antiviral Res., 85, pp. 450-462. , 20060421
  • Perera, R., Khaliq, M., Kuhn, R.J., Closing the door on flaviviruses: Entry as a target for antiviral drug design (2008) Antiviral Res., 80, pp. 11-22. , 18585795
  • Alen, M.M.F., Schols, D., Dengue virus entry as target for antiviral therapy (2012) J Trop Med., E, p. 628475
  • Haggani, A.A., Tilton, J.C., Entry inhibitors and their use in the treatment of HIV-1 infection (2013) Antiviral Res., 98, pp. 158-170. , 23541872
  • 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
  • Mosso, C., Galván-Mendoza, I.J., Ludert, J.E., Del Angel, R.M., Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT (2008) Virology., 378, pp. 193-199. , 18571214
  • Acosta, E.G., Castilla, V., Damonte, E.B., Infectious dengue-1 virus entry into mosquito C6/36 cells (2011) Virus Res., 160, pp. 163-179
  • Alhoot, M.A., Wang, S.M., Sekaran, S.D., Inhibition of dengue virus entry and multiplication into monocytes using RNA interference (2011) PLoS Negl Trop Dis., 5. , 22140591
  • Krishnan, M.N., Sukumaran, B., Pal, U., Agaise, H., Murray, J.L., Hodge, T.W., Rab 5 is required for the cellular entry of dengue and West Nile viruses (2007) J Virol., 81, pp. 4881-4885. , 17301152
  • Alhoot, M.A., Wang, S.M., Sekaran, S.D., RNA interference mediated inhibition of dengue virus multiplication and entry in HepG2 cells (2012) PLoS ONE., 7. , 22457813
  • Peng, T., Wang, J.L., Chen, W., Zhang, J.L., Gao, N., Chen, Z.T., Entry of dengue virus serotype 2 into ECV304 cells depends on clathrin-dependent endocytosis, but not on caveolae-dependent endocytosis (2009) Can J Microbiol., 55, pp. 139-145. , 19295646
  • Acosta, E.G., Castilla, V., Damonte, E.B., Alternative infectious entry pathways for dengue virus serotypes into mammalian cells (2009) Cell Microbiol., 11, pp. 1533-1549. , 19523154
  • Ang, F., Wong, A.P.Y., Mm-L, N., Chu, J.J.H., Small interference RNA profiling reveals the essential role of human membrane trafficking genes in mediating the infectious entry of dengue virus (2010) Virol J., 7, p. 24. , 20122152
  • Suksanpaisan, L., Susantad, T., Smith, D.R., Characterization of dengue virus entry into HepG2 cells (2009) J Biomed Sci., 16, p. 17. , 19272179
  • Van Der Schaar, H.M., Rust, M.J., Chen, C., Van Der Ende-Metselaar, H., Wilschut, J., Zhuang, X., Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells (2008) PLoS Pathog., 4. , 19096510
  • Messina, J.P., Brady, O.J., Scott, T.W., Zou, C., Pigott, D.M., Duda, K.A., Global spread of dengue virus types: Mapping the 70 year history (2014) Trends Microbiol., 22, pp. 138-146. , 24468533
  • Huang, C.Y., Kinney, R.M., Livengood, J.A., Bolling, B., Arguello, J.J., Luy, B.E., Genetic and phenotypic characterization of manufacturing seeds for a tetravalent dengue vaccine (DENVax) (2013) PLoS Negl Trop Dis., 7. , 23738026
  • Lee, H.-C., Yen, Y.-T., Chen, W.-Y., Wu-Hsieh, B.A., Wu, S.-C., Dengue type 4 live-attenuated vaccine viruses passaged in Vero cells affect genetic stability and dengue-induced hemorrhaging in mice (2011) PLoS ONE., 6. , 22053180
  • Sanchez, V., Gimenez, S., Tomlinson, B., Chan, P.K., Thomas, G.N., Forrat, R., Innate and adaptive cellular immunity in flavivirus-naïve human recipients of a live-attenuated dengue serotype 3 vaccine produced in Vero cells (VDV3) (2006) Vaccine., 24, pp. 4914-4926. , 16632108
  • Talarico, L.B., Damonte, E.B., Interference in dengue virus adsorption and uncoating by carrageenans (2007) Virology., 363, pp. 473-485. , 17337028
  • Wang, L.H., Rothberg, K.G., Anderson, R.G., Miss-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation (1993) J Cell Biol., 123, pp. 1107-1117. , 8245121
  • Schlegel, R., Dickson, R.B., Willingham, M.C., Pastan, I.H., Amantadine and dansylcadaverine inhibit vesicular stomatitis virus uptake and receptor-mediated endocytosis of alpha 2-macroglobulin (1982) Proc Natl Acad Sci USA., 79, pp. 2291-2295. , 6179094
  • Leppert, B.J., Mansfield, J.M., Paulnock, D.M., The soluble variant surface glycoprotein of African trypanosomes is recognized by a macrophage scavenger receptor and induces i kappa B alpha degradation independently of TRAF6-mediated TLR signaling (2007) J Immunol., 179, pp. 548-556. , 17579076
  • Zhu, Y.-Z., Xu, Q.-Q., Wu, D.-G., Ren, H., Zhao, P., Lao, W.-G., Japanese encephalitis virus enters rat neuroblastoma cells via a pH-dependent, dynamin and caveola-mediated endocytosis pathway (2012) J Virol., 24, pp. 13407-13422
  • Lee, R.C., Hapuarachchi, H.C., Chen, K.C., Hussain, K.M., Chen, H., Low, S.L., Mosquito cellular factors and functions in mediating the infectious entry of chikungunya virus (2013) PLoS Negl Trop Dis., 7. , 23409203
  • Benmerah, A., Bayrou, M., Cerf-Bensussan, N., Dautry-Varsat, A., Inhibition of clathrin-coated pit assembly by an Eps15 mutant (1999) J Cell Sci., 112, pp. 1303-1311. , 10194409
  • Mercer, J., Schelhaas, M., Helenius, A., Virus entry by endocytosis (2010) Annu Rev Biochem., 79, pp. 803-833. , 20196649
  • Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., Kirchhausen, T., Dynasore: A cell-permeable inhibitor of dynamin (2006) Dev Cell., 10, pp. 839-850. , 16740485
  • Oh, P., McIntosh, D.P., Schnitzer, J., Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fusion from the plasma membrane of endothelium (1998) J Cell Biol., 141, pp. 101-114. , 9531551
  • Sauvonnet, N., Dujeancourt, A., Dautry-Varsat, A., Cortactin and dynamin are required for the clathrin-independent endocytosis of (gamma) c cytokine receptor (2005) J Cell Sci., 168, pp. 155-163
  • Pelkmans, L., Secrets of caveolae-and lipid raft-mediated endocytosis revealed by mammalian viruses (2005) Biochem Biophys Acta., 1746, pp. 295-304. , 16126288
  • Ilangumaran, S., Hoessli, D.C., Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane (1998) Biochem J., 335, pp. 433-440. , 9761744
  • Zidovetzki, R., Levitan, I., Use of cyclodextrins to manipulate plasma membrane cholesterol content: Evidence, misconceptions and control strategies (2007) Biochim Biophys Acta., 1768, pp. 1311-1324. , 17493580
  • Anderson, H.A., Chen, Y., Norkin, L.C., Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae (1996) Mol Biol Cell., 7, pp. 1825-1834. , 8930903
  • Carro, A.C., Damonte, E.B., Requirement of cholesterol in the viral envelope fro dengue virus infection (2013) Virus Res., 174, pp. 78-87. , 23517753
  • Pelkmans, L., Kartenbeck, J., Helenius, A., Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER (2001) Nat Cell Biol., 3, pp. 473-483. , 11331875
  • Coyne, C.B., Bergelson, J.M., Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions (2006) Cell., 124, pp. 119-131. , 16413486
  • 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. , 28524
  • Guinea, R., Carrasco, L., Concanamycin A: A powerful inhibitor of enveloped animal virus entry into cells (1994) Biochem Biophys Res Commun., 201, pp. 1270-1278. , 8024571
  • Clemente, R., De La Torre, J.C., Cell entry of borna disease virus follows a clathrin-mediated endocitosis pathway that requires Rab5 and microtubules (2009) J Virol., 83, pp. 10406-10416. , 19656886
  • Lozach, P.-Y., Mancini, R., Bitto, D., Meier, R., Oestereich, L., Overby, A.K., Entry of bunyaviruses into mammalian cells (2010) Cell Host Microbe., 7, pp. 488-499. , 20542252
  • Feng, Y., Press, B., Wndinger-Ness, A., Rab7: An important regulator of late endocytic membrane traffic (1995) J Cell Biol., 131, pp. 1435-1452. , 8522602
  • Gorvel, J.P., Chavrier, P., Zerial, M., Gruenberg, J., Rab5 controls early endosome fusion in vitro (1991) Cell., 64, pp. 915-925. , 1900457
  • Hansen, C.G., Nichols, B.J., Molecular mechanisms of clathrin-independent endocytosis (2009) J Cell Sci., 122, pp. 1713-1721. , 19461071
  • Howes, M.T., Mayor, S., Parton, R.G., Molecules, mechanisms and cellular roles of clathrin-independent endocytosis (2010) Curr Opin Cell Biol., 22, pp. 519-527. , 20439156
  • Cruz-Oliveira, C., Freire, J.M., Conceição, T.M., Higa, L.M., Castanho, M.A., Da Poian, A.T., Receptors and routes of dengue VÍrus entry into the host cells (2015) FEMS Microbiol Rev., 39, pp. 155-170. , 25725010
  • Kalia, M., Khasa, R., Sharma, M., Nain, M., Vrati, S., Japanese encephalitis VÍrus infects neuronal cells through a clathrin-independent endocytic mechanism (2013) J Virol., 87, pp. 148-162. , 23055570
  • Schulz, W.L., Haj, A.K., Schiff, L.A., Reovirus uses multiple endocytic pathways for cell entry (2012) J Virol., 86, pp. 12665-12675. , 22973022
  • Permanyer, M., Ballana, E., Esté, J.A., Endocitosis of HIV: Anything goes (2010) Trends Microbiol., 18, pp. 543-551. , 20965729
  • Hasebe, R., Sasaki, M., Sawa, H., Wada, R., Umemura, T., Kimura, T., Infectious entry of equine herpesvirus-1 into host cells through different endocytic pathways (2009) Virology., 393, pp. 198-209. , 19720389
  • Spoden, G., Freitag, K., Hausmann, M., Boller, K., Sapp, M., Lambert, C., Clathrin-and caveolin-independent entry of human papillomavirus type 16-Involvement of tetraspanin-enriched microdomains (TEMs) (2008) PLoS ONE., 3. , 18836553
  • Karasneh, G.A., Shukla, D., Herpes simplex virus infects most cell types in vitro: Clues to its success (2011) Virol J., 8, p. 481. , 22029482
  • De Vries, E., Tscherne, D.M., Wienholts, M.J., Cobos-Jiménez, V., Scholte, F., García-Sastre, A., Dissection of the Influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway (2011) PLoS Pathog., 7. , 21483486
  • Aleksandrowicz, P., Marzi, A., Biedenkopf, N., Beimforde, N., Becker, S., Hoenen, T., Ebola virus enters host cells by macropynocytosis and clathrin-mediated endocytosis (2011) J Infect Dis., 204, pp. S957-967. , 21987776
  • Lozach, P.-Y., Huotari, J., Helenius, A., Late-penetrating viruses (2011) Curr Opin Virol., 1, pp. 35-43. , 22440565
  • Acosta, E.G., Castilla, V., Damonte, E.B., Differential requirements in endocytic trafficking for penetration of dengue virus (2012) PLoS ONE., 7. , 22970315
  • Zaitseva, E., Yang, S.-T., Melikov, K., Pourmal, S., Chernomordik, L.V., Dengue virus ensures its fusion in late endosomes using compartment-specific lipids (2010) PLoS Pathog., 6. , 20949067

Citas:

---------- APA ----------
Piccini, L.E., Castilla, V. & Damonte, E.B. (2015) . Dengue-3 virus entry into vero cells: Role of clathrin-mediated endocytosis in the outcome of infection. PLoS ONE, 10(10).
http://dx.doi.org/10.1371/journal.pone.0140824
---------- CHICAGO ----------
Piccini, L.E., Castilla, V., Damonte, E.B. "Dengue-3 virus entry into vero cells: Role of clathrin-mediated endocytosis in the outcome of infection" . PLoS ONE 10, no. 10 (2015).
http://dx.doi.org/10.1371/journal.pone.0140824
---------- MLA ----------
Piccini, L.E., Castilla, V., Damonte, E.B. "Dengue-3 virus entry into vero cells: Role of clathrin-mediated endocytosis in the outcome of infection" . PLoS ONE, vol. 10, no. 10, 2015.
http://dx.doi.org/10.1371/journal.pone.0140824
---------- VANCOUVER ----------
Piccini, L.E., Castilla, V., Damonte, E.B. Dengue-3 virus entry into vero cells: Role of clathrin-mediated endocytosis in the outcome of infection. PLoS ONE. 2015;10(10).
http://dx.doi.org/10.1371/journal.pone.0140824