Productive entry of type C foot-and-mouth disease virus into susceptible cultured cells requires clathrin and is dependent on the presence of plasma membrane cholesterol

Virology

Volumn 369, Issue 1, 2007, Pages 105-118

  Martín Acebes, Miguel A ^a   González Magaldi, Mónica ^a   Sandvig, Kirsten ^d   Sobrino, Francisco ^a,b   Armas Portela, Rosario ^a,c  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; CAVEOLIN 1; CHOLESTEROL; CLATHRIN; CONCANAMYCIN A; METHYL BETA CYCLODEXTRIN; NYSTATIN; SUCROSE;

ACIDITY; ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENDOCYTOSIS; FOOT AND MOUTH DISEASE VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; VESICULAR STOMATITIS VIRUS; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION; VIRUS TYPING;

AMMONIUM CHLORIDE; ANIMALS; ANTIVIRAL AGENTS; CAVEOLAE; CELL LINE; CLATHRIN; CLATHRIN-COATED VESICLES; CRICETINAE; ENDOCYTOSIS; FOOT-AND-MOUTH DISEASE VIRUS; MACROLIDES; MEMBRANE LIPIDS; NYSTATIN; SWINE; VESICULOVIRUS; VIRUS INTERNALIZATION;

FOOT-AND-MOUTH DISEASE VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 35648989044     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.07.021     Document Type: Article

References (83)

1. Acharya R., Fry E., Stuart D., Fox G., Rowlands D., and Brown F. The three-dimensional structure of foot-and-mouth disease virus at 2.9 A resolution. Nature 337 6209 (1989) 709-716
2. Al-Younes H.M., Rudel T., and Meyer T.F. Characterization and intracellular trafficking pattern of vacuoles containing Chlamydia pneumoniae in human epithelial cells. Cell. Microbiol. 1 3 (1999) 237-247
3. Baranowski E., Sevilla N., Verdaguer N., Ruiz-Jarabo C.M., Beck E., and Domingo E. Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J. Virol. 72 8 (1998) 6362-6372
4. Barteling S.J. Modern inactivated foot-and-mouth disease (FMD) vaccines: historical background and key elements in production and use. In: Domingo F.S.a.E. (Ed). Foot-and-Mouth Disease: Current Prospectives (2004), Horizon Bioscience, Norfolk
5. Baxt B. Effect of lysosomotropic compounds on early events in foot-and-mouth disease virus replication. Virus Res. 7 3 (1987) 257-271
6. Belsham G.J. Translation and replication of FMDV RNA. Curr. Top. Microbiol. Immunol. 288 (2005) 43-70
7. Berinstein A., Roivainen M., Hovi T., Mason P.W., and Baxt B. Antibodies to the vitronectin receptor (integrin alpha V beta 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 69 4 (1995) 2664-2666
8. Berryman S., Clark S., Monaghan P., and Jackson T. Early events in integrin alphavbeta6-mediated cell entry of foot-and-mouth disease virus. J. Virol. 79 13 (2005) 8519-8534
9. Brown F. Problems with BHK 21 cells. Dev. Biol. Stand. 93 (1998) 85-88
10. Bubeck D., Filman D.J., and Hogle J.M. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat. Struct., Mol. Biol. 12 7 (2005) 615-618
11. Burman A., Clark S., Abrescia N.G., Fry E.E., Stuart D.I., and Jackson T. Specificity of the VP1 GH loop of foot-and-mouth disease virus for {alpha}v integrins. J. Virol. 80 19 (2006) 9798-9810
12. Carrillo E.C., Giachetti C., and Campos R.H. Effect of lysosomotropic agents on the foot-and-mouth disease virus replication. Virology 135 2 (1984) 542-545
13. Curry S., Abrams C.C., Fry E., Crowther J.C., Belsham G.J., Stuart D.I., and King A.M. Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J. Virol. 69 1 (1995) 430-438
14. Chen Y., and Norkin L.C. Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae. Exp. Cell Res. 246 1 (1999) 83-90
15. Chinnapen D.J., Chinnapen H., Saslowsky D., and Lencer W.I. Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol. Lett. 266 (2007) 129-137
16. Chu J.J., and Ng M.L. Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J. Biol. Chem. 279 52 (2004) 54533-54541
17. Chung S.K., Kim J.Y., Kim I.B., Park S.I., Paek K.H., and Nam J.H. Internalization and trafficking mechanisms of coxsackievirus B3 in HeLa cells. Virology 333 1 (2005) 31-40
18. Damm E.M., and Pelkmans L. Systems biology of virus entry in mammalian cells. Cell. Microbiol. 8 8 (2006) 1219-1227
19. Damm E.M., Pelkmans L., Kartenbeck J., Mezzacasa A., Kurzchalia T., and Helenius A. Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168 3 (2005) 477-488
20. Danthi P., and Chow M. Cholesterol removal by methyl-beta-cyclodextrin inhibits poliovirus entry. J. Virol. 78 1 (2004) 33-41
21. DeTulleo L., and Kirchhausen T. The clathrin endocytic pathway in viral infection. EMBO J. 17 16 (1998) 4585-4593
22. Dimitrov D.S. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev., Microbiol. 2 2 (2004) 109-122
23. Domingo E., Escarmis C., Baranowski E., Ruiz-Jarabo C.M., Carrillo E., Nunez J.I., and Sobrino F. Evolution of foot-and-mouth disease virus. Virus Res. 91 1 (2003) 47-63
24. Garcia-Briones M., Rosas M.F., Gonzalez-Magaldi M., Martin-Acebes M.A., Sobrino F., and Armas-Portela R. Differential distribution of non-structural proteins of foot-and-mouth disease virus in BHK-21 cells. Virology 349 2 (2006) 409-421
25. Gilbert J.M., and Benjamin T.L. Early steps of polyomavirus entry into cells. J. Virol. 74 18 (2000) 8582-8588
26. Hewat E.A., Verdaguer N., Fita I., Blakemore W., Brookes S., King A., Newman J., Domingo E., Mateu M.G., and Stuart D.I. Structure of the complex of an Fab fragment of a neutralizing antibody with foot-and-mouth disease virus: positioning of a highly mobile antigenic loop. EMBO J. 16 7 (1997) 1492-1500
27. Hogle J.M. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56 (2002) 677-702
28. Huber M., Brabec M., Bayer N., Blaas D., and Fuchs R. Elevated endosomal pH in HeLa cells overexpressing mutant dynamin can affect infection by pH-sensitive viruses. Traffic 2 10 (2001) 727-736
29. Iversen T.G., Skretting G., van Deurs B., and Sandvig K. Clathrin-coated pits with long, dynamin-wrapped necks upon expression of a clathrin antisense RNA. Proc. Natl. Acad. Sci. U.S.A. 100 9 (2003) 5175-5180
30. Jackson T., Sheppard D., Denyer M., Blakemore W., and King A.M. The epithelial integrin alphavbeta6 is a receptor for foot-and-mouth disease virus. J. Virol. 74 11 (2000) 4949-4956
31. Jackson T., Mould A.P., Sheppard D., and King A.M. Integrin alphavbeta1 is a receptor for foot-and-mouth disease virus. J. Virol. 76 3 (2002) 935-941
32. Jackson T., Clark S., Berryman S., Burman A., Cambier S., Mu D., Nishimura S., and King A.M. Integrin alphavbeta8 functions as a receptor for foot-and-mouth disease virus: role of the beta-chain cytodomain in integrin-mediated infection. J. Virol. 78 9 (2004) 4533-4540
33. Joki-Korpela P., Marjomaki V., Krogerus C., Heino J., and Hyypia T. Entry of human parechovirus 1. J. Virol. 75 4 (2001) 1958-1967
34. Keller P., and Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140 6 (1998) 1357-1367
35. Kurzchalia T.V., Dupree P., and Monier S. VIP21-Caveolin, a protein of the trans-Golgi network and caveolae. FEBS Lett. 346 1 (1994) 88-91
36. Lakadamyali M., Rust M.J., and Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124 5 (2006) 997-1009
37. Lamaze C., Dujeancourt A., Baba T., Lo C.G., Benmerah A., and Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7 3 (2001) 661-671
38. Lea S., Hernandez J., Blakemore W., Brocchi E., Curry S., Domingo E., Fry E., Abu-Ghazaleh R., King A., Newman J., et al. The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2 2 (1994) 123-139
39. Le Blanc I., Luyet P.P., Pons V., Ferguson C., Emans N., Petiot A., Mayran N., Demaurex N., Faure J., Sadoul R., Parton R.G., and Gruenberg J. Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7 7 (2005) 653-664
40. Lefrancois L., and Lyles D.S. The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology 121 1 (1982) 168-174
41. Lukacs G.L., Segal G., Kartner N., Grinstein S., and Zhang F. Constitutive internalization of cystic fibrosis transmembrane conductance regulator occurs via clathrin-dependent endocytosis and is regulated by protein phosphorylation. Biochem. J. 328 Pt 2 (1997) 353-361
42. Marjomaki V., Pietiainen V., Matilainen H., Upla P., Ivaska J., Nissinen L., Reunanen H., Huttunen P., Hyypia T., and Heino J. Internalization of echovirus 1 in caveolae. J. Virol. 76 4 (2002) 1856-1865
43. Marsh M., and Helenius A. Virus entry: open sesame. Cell 124 4 (2006) 729-740
44. Mateu M.G. Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res. 38 1 (1995) 1-24
45. Mateu M.G., Rocha E., Vicente O., Vayreda F., Navalpotro C., Andreu D., Pedroso E., Giralt E., Enjuanes L., and Domingo E. Reactivity with monoclonal antibodies of viruses from an episode of foot-and-mouth disease. Virus Res. 8 3 (1987) 261-274
46. Matlin K.S., Reggio H., Helenius A., and Simons K. Pathway of vesicular stomatitis virus entry leading to infection. J. Mol. Biol. 156 3 (1982) 609-631
47. Millan J., Puertollano R., Fan L., and Alonso M.A. Caveolin and MAL, two protein components of internal detergent-insoluble membranes, are in distinct lipid microenvironments in MDCK cells. Biochem. Biophys. Res. Commun. 233 3 (1997) 707-712
48. Monaghan P., Gold S., Simpson J., Zhang Z., Weinreb P.H., Violette S.M., Alexandersen S., and Jackson T. The alpha(v)beta6 integrin receptor for Foot-and-mouth disease virus is expressed constitutively on the epithelial cells targeted in cattle. J. Gen. Virol. 86 Pt 10 (2005) 2769-2780
49. Neff S., Sa-Carvalho D., Rieder E., Mason P.W., Blystone S.D., Brown E.J., and Baxt B. Foot-and-mouth disease virus virulent for cattle utilizes the integrin alpha(v)beta3 as its receptor. J. Virol. 72 5 (1998) 3587-3594
50. Nicola A.V., McEvoy A.M., and Straus S.E. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J. Virol. 77 9 (2003) 5324-5332
51. Nunez J.I., Baranowski E., Molina N., Ruiz-Jarabo C.M., Sanchez C., Domingo E., and Sobrino F. A single amino acid substitution in nonstructural protein 3A can mediate adaptation of foot-and-mouth disease virus to the guinea pig. J. Virol. 75 8 (2001) 3977-3983
52. O'Donnell V., LaRocco M., Duque H., and Baxt B. Analysis of foot-and-mouth disease virus internalization events in cultured cells. J. Virol. 79 13 (2005) 8506-8518
53. Oh P., McIntosh D.P., and Schnitzer J.E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141 1 (1998) 101-114
54. Pelkmans L., Fava E., Grabner H., Hannus M., Habermann B., Krausz E., and Zerial M. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436 7047 (2005) 78-86
55. Peres C., Yart A., Perret B., Salles J.P., and Raynal P. Modulation of phosphoinositide 3-kinase activation by cholesterol level suggests a novel positive role for lipid rafts in lysophosphatidic acid signalling. FEBS Lett. 534 1-3 (2003) 164-168
56. Pietiainen V., Marjomaki V., Upla P., Pelkmans L., Helenius A., and Hyypia T. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol. Biol. Cell 15 11 (2004) 4911-4925
57. Richterova Z., Liebl D., Horak M., Palkova Z., Stokrova J., Hozak P., Korb J., and Forstova J. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J. Virol. 75 22 (2001) 10880-10891
58. Rigaut K.D., Birk D.E., and Lenard J. Intracellular distribution of input vesicular stomatitis virus proteins after uncoating. J. Virol. 65 5 (1991) 2622-2628
59. Rodal S.K., Skretting G., Garred O., Vilhardt F., van Deurs B., and Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10 4 (1999) 961-974
60. Roseberry A.G., and Hosey M.M. Internalization of the M2 muscarinic acetylcholine receptor proceeds through an atypical pathway in HEK293 cells that is independent of clathrin and caveolae. J. Cell Sci. 114 Pt 4 (2001) 739-746
61. Rowlands D.J. Foot-and-mouth disease. Special issue. Virus Res. 91 1 (2003)
62. Sandvig K., Olsnes S., Petersen O.W., and van Deurs B. Acidification of the cytosol inhibits endocytosis from coated pits. J. Cell Biol. 105 2 (1987) 679-689
63. Schober D., Kronenberger P., Prchla E., Blaas D., and Fuchs R. Major and minor receptor group human rhinoviruses penetrate from endosomes by different mechanisms. J. Virol. 72 2 (1998) 1354-1364
64. Sieczkarski S.B., and Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83 Pt 7 (2002) 1535-1545
65. Sieczkarski S.B., and Whittaker G.R. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76 20 (2002) 10455-10464
66. Sieczkarski S.B., and Whittaker G.R. Viral entry. Curr. Top. Microbiol. Immunol. 285 (2005) 1-23
67. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 6633 (1997) 569-572
68. Skretting G., Torgersen M.L., van Deurs B., and Sandvig K. Endocytic mechanisms responsible for uptake of GPI-linked diphtheria toxin receptor. J. Cell Sci. 112 Pt 22 (1999) 3899-3909
69. Smith A.E., and Helenius A. How viruses enter animal cells. Science 304 5668 (2004) 237-242
70. Snyers L., Zwickl H., and Blaas D. Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis. J. Virol. 77 9 (2003) 5360-5369
71. Sobrino F., Davila M., Ortin J., and Domingo E. Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128 2 (1983) 310-318
72. In: Sobrino F., and Domingo E. (Eds). Foot-and-Mouth Disease. Current Perspectives (2004), Horizon Bioscience, Norfolk, UK
73. Stuart A.D., Eustace H.E., McKee T.A., and Brown T.D. A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J. Virol. 76 18 (2002) 9307-9322
74. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., and McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. U.S.A. 96 12 (1999) 6775-6780
75. Sun X., Yau V.K., Briggs B.J., and Whittaker G.R. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338 1 (2005) 53-60
76. Sutmoller P., Barteling S.S., Olascoaga R.C., and Sumption K.J. Control and eradication of foot-and-mouth disease. Virus Res. 91 1 (2003) 101-144
77. Toja M., Escarmis C., and Domingo E. Genomic nucleotide sequence of a foot-and-mouth disease virus clone and its persistent derivatives. Implications for the evolution of viral quasispecies during a persistent infection. Virus Res. 64 2 (1999) 161-171
78. Torgersen M.L., Skretting G., van Deurs B., and Sandvig K. Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 114 Pt. 20 (2001) 3737-3747
79. Upla P., Marjomaki V., Kankaanpaa P., Ivaska J., Hyypia T., Van Der Goot F.G., and Heino J. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15 2 (2004) 625-636
80. Urs N.M., Jones K.T., Salo P.D., Severin J.E., Trejo J., and Radhakrishna H. A requirement for membrane cholesterol in the beta-arrestin- and clathrin-dependent endocytosis of LPA1 lysophosphatidic acid receptors. J. Cell Sci. 118 Pt. 22 (2005) 5291-5304
81. van Vlijmen H.W., Curry S., Schaefer M., and Karplus M. Titration calculations of foot-and-mouth disease virus capsids and their stabilities as a function of pH. J. Mol. Biol. 275 2 (1998) 295-308
82. Verdaguer N., Mateu M.G., Andreu D., Giralt E., Domingo E., and Fita I. Structure of the major antigenic loop of foot-and-mouth disease virus complexed with a neutralizing antibody: direct involvement of the Arg-Gly-Asp motif in the interaction. EMBO J. 14 8 (1995) 1690-1696
83. Wettey F.R., Hawkins S.F., Stewart A., Luzio J.P., Howard J.C., and Jackson A.P. Controlled elimination of clathrin heavy-chain expression in DT40 lymphocytes. Science 297 5586 (2002) 1521-1525