Analysis of foot-and-mouth disease virus internalization events in cultured cells

Journal of Virology

Volumn 79, Issue 13, 2005, Pages 8506-8518

  O'Donnell, Vivian ^a,b   LaRocco, Michael ^b   Duque, Hernando ^c   Baxt, Barry ^b  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b PLUM ISLAND ANIMAL DISEASE CENTER   (United States)

^c UNITED STATES DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAVBETA6 INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; CAPSID PROTEIN; CD51 ANTIGEN; CLATHRIN; INTEGRIN RECEPTOR; MONENSIN; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; CELL CULTURE; CELL SURFACE; CONFOCAL MICROSCOPY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; FOOT AND MOUTH DISEASE VIRUS; GOLGI COMPLEX; INTERNALIZATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SEROTYPE; TEMPERATURE DEPENDENCE; VIRUS CAPSID; VIRUS REPLICATION;

ANTIBODIES, VIRAL; CELL LINE; FOOT-AND-MOUTH DISEASE VIRUS; HUMANS; KINETICS; MICROSCOPY, CONFOCAL; RECEPTORS, VIRUS; VIRUS REPLICATION;

FOOT-AND-MOUTH DISEASE VIRUS; MIRIDAE;

EID: 20744438160     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.13.8506-8518.2005     Document Type: Article

References (100)

1. Anderson, H. A., Y. Chen, and L. C. Norkin. 1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 7:1825-1834.
2. Basu, S. K., J. L. Goldstein, R. G. Anderson, and M. S. Brown. 1981. Monensin interrupts the recycling of low density lipoprotein receptors in human fibroblasts. Cell 24:493-502.
3. Baxt, B. 1987. Effect of lysosomotropic compounds on early events in foot-and-mouth disease virus replication. Virus Res. 7:257-271.
4. Baxt, B., and H. L. Bachrach. 1982. The adsorption and degradation of foot-and-mouth disease virus by isolated BHK-21 cell plasma membranes. Virology 116:391-405.
5. Baxt, B., and H. L. Bachrach. 1980. Early interactions of foot-and-mouth disease virus with cultured cells. Virology 104:42-55.
6. Baxt, B., and Y. Becker. 1990. The effect of peptides containing the arginine-glycine-aspartic acid sequence on the adsorption of foot-and-mouth disease virus to tissue culture cells. Virus Genes 4:73-83.
7. Baxt, B., and P. W. Mason. 1995. Foot-and-mouth disease virus undergoes restricted replication in macrophage cell cultures following Fc receptor-mediated adsorption. Virology 207:503-509.
8. Baxt, B., D. O. Morgan, B, H. Robertson, and C. A. Timpone. 1984. Epitopes on foot-and-mouth disease virus outer capsid protein VP1 involved in neutralization and cell attachment. J. Virol. 51:298-305.
9. Baxt, B., S. Neff, E. Rieder, and P. Mason. 2002. Foot-and-mouth disease virus-receptor interactions: role in pathogenesis and tissue culture adaptation, p. 115-123. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, D.C.
10. Baxt, B., and E. Rieder. 2004. Molecular aspects of foot-and-mouth disease virus virulence and host range: role of host cell receptors and viral factors, p. 145-172. In F. Sobrino and E. Domingo (ed.), Foot and mouth disease: current perspectives. Horizon Bioscience, Norfolk, England.
11. Bayer, N., D. Schober, M. Huttinger, D. Blaas, and R. Fuchs. 2001. Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J. Biol. Chem. 276:3952-3962.
12. Bella, J., and M. G. Rossmann. 1999. Rhinoviruses and their ICAM receptors. J. Struct. Biol. 128:69-74.
13. Belnap, D. M., D. J. Filman, B. L. Trus, N. Cheng, F. P. Booy, J. F. Conway, S. Curry, C. N. Hiremath, S. K. Tsang, A. C. Steven, and J. M. Hogle. 2000. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74:1342-1354.
14. Bergelson, J. M., M. P. Shepley, B. M. Chan, M. E. Hemler, and R. W. Finberg. 1992. Identification of the integrin VLA-2 as a receptor for echovirus 1. Science 255:1718-1720.
15. Bergelson, J. M., N. F. St. John, S. Kawaguchi, R. Pasqualini, F. Berdichevsky, M. E. Hemler, and R. W. Finberg. 1994. The I domain is essential for echovirus 1 interaction with VLA-2. Cell Adhes. Commun. 2:455-464.
16. 3) inhibit binding and infection of foot-and-mouth disease virus to cultured cells. J. Virol. 69: 2664-2666.
17. 3 avidity. J. Biol. Chem. 272:28757-28761.
18. Calderwood, D. A., Y. Fujioka, J. M. de Pereda, B. Garcia-Alvarez, T. Nakamoto, B. Margolis, C. J. McGlade, R. C. Liddington, and M. H. Ginsberg. 2003. Integrin β cytoplasmic domain interactions with phosphotyrosine- binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA 100:2272-2277.
19. Carrillo, E. C., C. Giachetti, and R. Campos. 1985. Early steps in FMDV replication: further analysis on the effects of chloroquine. Virology 147: 118-125.
20. Carrillo, E. C., C. Giachetti, and R. H. Campos. 1984. Effect of lysosomotropic agents on the foot-and-mouth disease virus replication. Virology 135: 542-545.
21. Cavanagh, D., D. J. Rowlands, and F. Brown. 1978. Early events in the interaction between foot-and mouth disease virus and primary pig kidney cells. J. Gen. Virol. 41:255-264.
22. Chen, W. J., J. L. Goldstein, and M. S. Brown. 1990. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265: 3116-3123.
23. Cheresh, D. A., and R. C. Spiro. 1987. Biosynthetic and functional properties of an Arg-Gly-Asp-directed receptor involved in human melanoma cell attachment to vitronectin, fibrinogen, and von Willebrand factor. J. Biol. Chem. 262:17703-17711.
24. Danthi, P., and M. Chow. 2004. Cholesterol removal by methyl-β-cyclodextrin inhibits poliovirus entry. J. Virol. 78:33-41.
25. DeTulleo, L., and T. Kirchhausen. 1998. The clathrin endocytic pathway in viral infection. EMBO J. 17:4585-4593.
26. Devaney, M. A., V. N. Vakharia, R. E. Lloyd, E. Ehrenfeld, and M. J. Grubman. 1988. Leader protein of foot-and-mouth disease virus is required for cleavage of the p220 component of the cap-binding protein complex. J. Virol. 62:4407-4409.
27. v integrin utilization by type A and O viruses. J. Virol. 77:2500-2511.
28. 6 integrins. J. Virol. 78:9773-9781.
29. Dustin, M. L., and T. A. Springer. 1991. Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. Annu. Rev. Immunol. 9:27-66.
30. Fox, G., N. R. Parry, P. V. Barnett, B. McGinn, D. J. Rowlands, and F. Brown. 1989. The cell attachment site on foot-and-mouth disease virus includes the amino acid sequence RGD (arginine-glycine-aspartic acid). J. Gen. Virol. 70:625-637.
31. Pricks, C. E., and J. M. Hogle. 1990. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64:1934-1945.
32. Gomez Yafal, A., G. Kaplan, V. R. Racaniello, and J. M. Hogle. 1993. Characterization of poliovirus conformational alteration mediated by soluble cell receptors. Virology 197:501-505.
33. Grubman, M. J., and B. Baxt. 2004. Foot-and-mouth disease. Clin. Microbiol. Rev. 17:465-493.
34. Henley, J. R., E. W. Krueger, B. J. Oswald, and M. A. McNiven. 1998. Dynamin-mediated internalization of caveolae. J. Cell Biol. 141:85-99.
35. Huber, M., M. Brabec, N. Bayer, D. Blaas, and R. Fuchs. 2001. Elevated endosomal pH in HeLa cells overexpressing mutant dynamin can affect infection by pH-sensitive viruses. Traffic 2:727-736.
36. 8 functions as a receptor for foot-and-mouth disease virus: role of the β-chain cytodomain in integrin-mediated infection. J. Virol. 78:4533-4540.
37. Jackson, T., F. M. Ellard, R. A. Ghazaleh, S. M. Brookes, W. E. Blakemore, A. H. Corteyn, D. I. Stuart, J. W. Newman, and A. M. King. 1996. Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J. Virol. 70:5282-5287.
38. Jackson, T., A. M. King, D. I. Stuart, and E. Fry. 2003. Structure and receptor binding. Virus Res. 91:33-46.
39. 1 is a receptor for foot-and-mouth disease virus. J. Virol. 76:935-941.
40. 6 is a receptor for foot-and-mouth disease virus. J. Virol. 74:4949-4956.
41. Joki-Korpela, P., V. Marjomaki, C. Krogerus, J. Heino, and T. Hyypia. 2001. Entry of human parechovirus 1. J. Virol. 75:1958-1967.
42. Kaplan, G., M. S. Freistadt, and V. R. Racaniello. 1990. Neutralization of poliovirus by cell receptors expressed in insect cells. J. Virol. 64:4697-4702.
43. Kirchweger, R., E. Ziegler, B. J. Lamphear, D. Waters, H. D. Liebig, W. Sommergruber, F. Sobrino, C. Hohenadl, D. Blaas, R. E. Rhoads, and T. Skern. 1994. Foot-and-mouth disease virus leader proteinase: purification of the Lb form and determination of its cleavage site on eIF-4g. J. Virol. 68: 5677-5684.
44. Klausner, R. D., J. G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
45. Knipe, T., E. Rieder, B. Baxt, G. Ward, and P. W. Mason. 1997. Characterization of synthetic foot-and-mouth disease virus provirions separates acid-mediated disassembly from infectivity. J. Virol. 71:2851-2856.
46. Leippert, M., E. Beck, F. Weiland, and E. Pfaff. 1997. Point mutations within the βG-βH loop of foot-and-mouth disease virus O1K affect virus attachment to target cells. J. Virol. 71:1046-1051.
47. Lippincott-Schwartz, J., L. Yuan, C. Tipper, M. Amherdt, L. Orci, and R. D. Klausner. 1991. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67:601-616.
48. Lippincott-Schwartz, J., L. C. Yuan, J. S. Bonifacino, and R. D. Klausner. 1989. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56: 801-813.
49. Marjomaki, V., V. Pietiainen, H. Matilainen, P. Upla, J. Ivaska, L. Nissinen, H. Reunanen, P. Huttunen, T. Hyypia, and J. Heino. 2002. Internalization of echovirus 1 in caveolae. J. Virol. 76:1856-1865.
50. Martin-Belmonte, F., J. A. Martinez-Menarguez, J. F. Aranda, J. Ballesta, M. C. de Marco, and M. A. Alonso. 2003. MAL regulates clathrin-mediated endocytosis at the apical surface of Madin-Darby canine kidney cells. J. Cell Biol. 163:155-164.
51. Mason, P. W., B. Baxt, F. Brown, J. Harber, A. Murdin, and E. Wimmer. 1993. Antibody-complexed foot-and-mouth disease virus, but not poliovirus, can infect normally insusceptible cells via the Fc receptor. Virology 192: 568-577.
52. Mason, P. W., E. Rieder, and B. Baxt. 1994. RGD sequence of foot-and-mouth disease virus is essential for infecting cells via the natural receptor but can be bypassed by an antibody-dependent enhancement pathway. Proc. Natl. Acad. Sci. USA 91:1932-1936.
53. Meier, O., K. Boucke, S. V. Hammer, S. Keller, R. P. Stidwill, S. Hemmi, and U. F. Greber. 2002. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158: 1119-1131.
54. Meier, O., and U. F. Greber. 2003. Adenovirus endocytosis. J. Gene Med. 5:451-462.
55. Merrifield, C. J., M. E. Feldman, L. Wan, and W. Almers. 2002. Imaging actin and dynamin recruitment during invagination of single dathrin-coated pits. Nat. Cell Biol. 4:691-698.
56. Miettinen, H. M., K. Matter, W. Hunziker, J. K. Rose, and I. Mellman. 1992. Fc receptor endocytosis is controlled by a cytoplasmic domain determinant that actively prevents coated pit localization. J. Cell Biol. 116: 875-888.
57. 6 in infection by foot-and-mouth disease virus. J. Virol. 75:4158-4164.
58. 3 to function as a receptor for foot-and-mouth disease virus is not dependent on the presence of complete subunit cytoplasmic domains. J. Virol. 75:527-532.
59. 3 subunit. J. Virol. 74:7298-7306.
60. 3 as its receptor. J. Virol. 72:3587-3594.
61. v integrins in adenovirus cell entry and gene delivery. Microbiol. Mol. Biol. Rev. 63:725-734.
62. O'Donnell, V. K., J. M. Pacheco, T. M. Henry, and P. W. Mason. 2001. Subcellular distribution of the foot-and-mouth disease virus 3A protein in cells infected with viruses encoding wild-type and bovine-attenuated forms of 3A. Virology 287:151-162.
63. Pelkmans, L., and A. Helenius. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
64. Pietiainen, V., V. Marjomaki, P. Upla, L. Pelkmans, A. Helenius, and T. Hyypia. 2004. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol. Biol. Cell 15:4911-4925.
65. Prchla, E., E. Kuechler, D. Blaas, and R. Fuchs. 1994. Uncoating of human rhinovirus serotype 2 from late endosomes. J. Virol. 68:3713-3723.
66. Prchla, E., C. Plank, E. Wagner, D. Blaas, and R. Fuchs. 1995. Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol. 131:111-123.
67. Pulli, T., E. Koivunen, and T. Hyypia. 1997. Cell-surface interactions of echovirus 22. J. Biol. Chem. 272:21176-21180.
68. Reilly, J. F., E. Mizukoshi, and P. A. Maher. 2004. Ligand dependent and independent internalization and nuclear translocation of fibroblast growth factor (FGF) receptor 1. DNA Cell Biol. 23:538-548.
69. Richardson, D. R., and P. Ponka. 1997. The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim. Biophys. Acta 1331:1-40.
70. Rieder, E., A. Berinstein, B. Baxt, A. Rang, and P. W. Mason. 1996. Propagation of an attenuated virus by design: engineering a novel receptor for a noninfectious foot-and-mouth disease virus. Proc. Natl. Acad. Sci. USA 93:10428-10433.
71. Rieder, E., T. Bunch, F. Brown, and P. W. Mason. 1993. Genetically engineered foot-and-mouth disease viruses with poly(C) tracts of two nucleotides are virulent in mice. J. Virol. 67:5139-5145.
72. 3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11: 1392-1402.
73. 3 integrin and regulates cell spreading on vitronectin. J. Biol. Chem. 278:1975-1985.
74. 3 integrin, the vitronectin receptor. Virology 203:357-365.
75. Sa-Carvalho, D., E. Rieder, B. Baxt, R. Rodarte, A. Tanuri, and P. W. Mason. 1997. Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J. Virol. 71: 5115-5123.
76. Schober, D., P. Kronenberger, E. Prchla, D. Blaas, and R. Fuchs. 1998. Major and minor receptor group human rhinoviruses penetrate from endosomes by different mechanisms. J. Virol. 72:1354-1364.
77. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
78. Smith, A. E., and A. Helenius. 2004. How viruses enter animal cells. Science 304:237-242.
79. Staunton, D. E., A. Gaur, P. Y. Chan, and T. A. Springer. 1992. Internalization of a major group human rhinovirus does not require cytoplasmic or transmembrane domains of ICAM-1. J. Immunol. 148:3271-3274.
80. Stave, J. W., J. L. Card, and D. O. Morgan. 1986. Analysis of foot-and-mouth disease virus type O1 Brugge neutralization epitopes using monoclonal antibodies. J. Gen. Virol. 67:2083-2092.
81. Stuart, A. D., H. E. Eustace, T. A. McKee, and T. D. Brown. 2002. A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J. Virol. 76:9307-9322.
82. Triantafilou, K., D. Fradelizi, K. Wilson, and M. Triantafilou. 2002. GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J. Virol. 76:633-643.
83. Triantafilou, K., and M. Triantafilou. 2001. A biochemical approach reveals cell-surface molecules utilised by Picornaviridae: Human Parechovirus 1 and Echovirus 1. J. Cell Biochem. 80:373-381.
84. Triantafilou, K., and M. Triantafilou. 2004. Lipid-raft-dependent Coxsackievirus B4 internalization and rapid targeting to the Golgi. Virology 326: 6-19.
85. Triantafilou, K., and M. Triantafilou. 2003. Lipid raft microdomains: key sites for Coxsackievirus A9 infectious cycle. Virology 317:128-135.
86. 1 as receptors. J. Virol. 74:5856-5862.
87. 3, but do not require the RGD sequence of the CAV-9 VP1 protein. Hum. Immunol. 61: 453-459.
88. 3 molecules in the coxsackievirus A9 infectious cycle. J. Gen. Virol. 80: 2591-2600.
89. Triantafilou, M., K. M. Wilson, and K. Triantafilou. 2001. Identification of echovirus 1 and coxsackievirus A9 receptor molecules via a novel flow cytometric quantification method. Cytometry 43:279-289.
90. Tsang, S. K., B. M. McDermott, V. R. Racaniello, and J. M. Hogle. 2001. Kinetic analysis of the effect of poliovirus receptor on viral uncoating: the receptor as a catalyst. J. Virol. 75:4984-4989.
91. Urrutia, R., J. R. Henley, T. Cook, and M. A. McNiven. 1997. The dynamins: redundant or distinct functions for an expanding family of related GTPases? Proc. Natl. Acad. Sci. USA 94:377-384.
92. van Dam, E. M., and W. Stoorvogel. 2002. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol. Biol. Cell 13:169-182.
93. 1 integrin does not depend on "NPXY" signals. Biochem. Biophys. Res. Commun. 199:603-611.
94. 5. J. Virol. 74:2731-2739.
95. Wang, K., S. Huang, A. Kapoor-Munshi, and G. Nemerow. 1998. Adenovirus internalization and infection require dynamin. J. Virol. 72:3455-3458.
96. Wang, L. H., K. G. Rothberg, and R. G. Anderson. 1993. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 123:1107-1117.
97. 6 in cell attachment to fibronectin. Heterologous expression of intact and secreted forms of the receptor. J. Biol. Chem. 269:6940-6948.
98. 3 integrin recycling and delivery to nascent focal adhesions. EMBO J. 23:2531-2543.
99. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity 8:723-732.
100. vβ3 in complex with an Arg-Gly-Asp ligand. Science 296:151-155.