Cellular entry of lymphocytic choriomeningitis virus

Journal of Virology

Volumn 82, Issue 3, 2008, Pages 1505-1517

  Rojek, Julian M ^a   Perez, Mar ^b   Kunz, Stefan ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DYSTROGLYCAN; CAVEOLIN; CELL RECEPTOR; CHOLESTEROL; CLATHRIN; GUANOSINE TRIPHOSPHATASE;

ACTIN FILAMENT; ANIMAL CELL; ARENAVIRUS; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; JUNIN VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMBRANE VESICLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE;

ACTINS; ANIMALS; CAVEOLINS; CELL LINE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CHOLESTEROL; CLATHRIN; CRICETINAE; DYNAMINS; DYSTROGLYCANS; ENDOCYTOSIS; HUMANS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MESOCRICETUS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

ARENAVIRUS; JUNIN VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS;

EID: 38349137425     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01331-07     Document Type: Article

References (80)

1. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160:521-540.
2. Barresi, R., and K. P. Campbell. 2006. Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119:199-207.
3. Bender, F. C., J. C. Whitbeck, M. Ponce de Leon, H. Lou, R. J. Eisenberg, and G. H. Cohen. 2003. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 77:9542-9552.
4. Benmerah, A., M. Bayrou, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112:1303-1311.
5. Benmerah, A., C. Lamaze, B. Begue, S. L. Schmid, A. Dautry-Varsat, and N. Cerf-Bensussan. 1998. AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol. 140:1055-1062.
6. Borrow, P., and M. B. Oldstone. 1992. Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J. Virol. 66:7270-7281.
7. Borrow, P., and M. B. Oldstone. 1994. Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198:1-9.
8. Buchmeier, M. J., J. C. de la Torre, and C. J. Peters. 2007. Arenaviridae: the viruses and their replication, p. 1791-1828. In D. L. Knipe and P. M. Howley (ed.), Fields virology, 5th ed. Lippincott-Raven, Philadelphia, PA.
9. Buchmeier, M. J., H. A. Lewicki, O. Tomori, and M. B. Oldstone. 1981. Monoclonal antibodies to lymphocytic choriomeningitis and pichinde viruses: generation, characterization, and cross-reactivity with other arenaviruses. Virology 113:73-85.
10. Cao, W., M. D. Henry, P. Borrow, H. Yamada, J. H. Elder, E. V. Ravkov, S. T. Nichol, R. W. Compans, K. P. Campbell, and M. B. Oldstone. 1998. Identification of α-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079-2081.
11. Castilla, V., S. E. Mersich, N. A. Candurra, and E. B. Damonte. 1994. The entry of Junin virus into Vero cells. Arch. Virol. 136:363-374.
12. Choi, K. S., H. Aizaki, and M. M. Lai. 2005. Murine coronavirus requires lipid rafts for virus entry and cell-cell fusion but not for virus release. J. Virol. 79:9862-9871.
13. Conner, S. D., and S. L. Schmid. 2003. Regulated portals of entry into the cell. Nature 422:37-44.
14. Coyne, C. B., and J. M. Bergelson. 2006. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124:119-131.
15. Damke, H., T. Baba, D. E. Warnock, and S. L. Schmid. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934.
16. Damm, E. M., L. Pelkmans, J. Kartenbeck, A. Mezzacasa, T. Kurzchalia, and A. Helenius. 2005. Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168:477-488.
17. Danthi, P., and M. Chow. 2004. Cholesterol removal by methyl-β-cyclodextrin inhibits poliovirus entry. J. Virol. 78:33-41.
18. Di Simone, C., and M. J. Buchmeier. 1995. Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 209:3-9.
19. Di Simone, C., M. A. Zandonatti, and M. J. Buchmeier. 1994. Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike. Virology 198:455-465.
20. Döhner, K., and B. Sodeik. 2005. The role of the cytoskeleton during viral infection. Curr. Top. Microbiol. Immunol. 285:67-108.
21. Dutko, F. J., and M. B. Oldstone. 1983. Genomic and biological variation among commonly used lymphocytic choriomeningitis virus strains. J. Gen. Virol. 64:1689-1698.
22. Ervasti, J. M., and K. P. Campbell. 1993. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122:809-823.
23. Eschli, B., K. Quirin, A. Wepf, J. Weber, R. Zinkernagel, and H. Hengartner. 2006. Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J. Virol. 80:5897-5907.
24. Fischer, S. A., M. B. Graham, M. J. Kuehnert, C. N. Kotton, A. Srinivasan, F. M. Marty, J. A. Comer, J. Guarner, C. D. Paddock, D. L. DeMeo, W. J. Shieh, B. R. Erickson, U. Bandy, A. DeMaria, Jr., J. P. Davis, F. L. Delmonico, B. Pavlin, A. Likos, M. J. Vincent, T. K. Sealy, C. S. Goldsmith, D. B. Jernigan, P. E. Rollin, M. M. Packard, M. Patel, C. Rowland, R. F. Helfand, S. T. Nichol, J. A. Fishman, T. Ksiazek, and S. R. Zaki. 2006. Transmission of lymphocytic choriomeningitis virus by organ transplantation. N. Engl. J. Med. 354:2235-2249.
25. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
26. Gallaher, W. R., C. DiSimone, and M. J. Buchmeier. 2001. The viral transmembrane superfamily: possible divergence of arenavirus and filovirus glycoproteins from a common RNA virus ancestor. BMC Microbiol. 1:1.
27. Geisbert, T. W., and P. B. Jahrling. 2004. Exotic emerging viral diseases: progress and challenges. Nat. Med. 10:S110-S121.
28. Gilbert, J., and T. Benjamin. 2004. Uptake pathway of polyomavirus via ganglioside GD1a. J. Virol. 78:12259-12267.
29. Gosselin-Grenet, A. S., G. Mottet-Osman, and L. Roux. 2006. From assembly to virus particle budding: pertinence of the detergent resistant membranes. Virology 344:296-303.
30. Greber, U. F., and M. Way. 2006. A superhighway to virus infection. Cell 124:741-754.
31. Helenius, A. 2007. Virus entry and uncoating, p. 99-118. In D. L. Knipe and P. M. Howley (ed.), Fields virology, 5th ed. Lippincott-Raven, Philadelphia, PA.
32. Jamieson, D. J., A. P. Kourtis, M. Bell, and S. A. Rasmussen. 2006. Lymphocytic choriomeningitis virus: an emerging obstetric pathogen? Am. J. Obstet. Gynecol. 194:1532-1536.
33. Kirkham, M., A. Fujita, R. Chadda, S. J. Nixon, T. V. Kurzchalia, D. K. Sharma, R. E. Pagano, J. F. Hancock, S. Mayor, and R. G. Parton. 2005. Uitrastructurai identification of uncoated caveolin-independent eariy endocytic vehicles. J. Cell Biol. 168:465-476.
34. Kirkham, M., and R. G. Parton. 2005. Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim. Biophys. Acta 1746:349-363.
35. Kunz, S., J. Rojek, M. Perez, C. Spiropoulou, and M. B. Oldstone. 2005. Characterization of the interaction of Lassa fever virus with its cellular receptor α-dystroglycan. J. Virol. 79:5979-5987.
36. Kunz, S., J. Rojek, C. Spiropoulou, R. Barresi, K. P. Campbell, and M. B. Oldstone. 2005. Posttranslational modification of α-dystroglycan, the cellular receptor for arenaviruses by the glycosyltransferase LARGE is critical for virus binding. J. Virol. 79:14282-14296.
37. Kunz, S., N. Sevilla, D. B. McGavern, K. P. Campbell, and M. B. Oldstone. 2001. Molecular analysis of the interaction of LCMV with its cellular receptor α-dystroglycan. J. Cell Biol. 155:301-310.
38. Kunz, S., N. Sevilla, J. M. Rojek, and M. B. Oldstone. 2004. Use of alternative receptors different than α-dystroglycan by selected isolates of lymphocytic choriomeningitis virus. Virology 325:432-445.
39. Kunz, S., U. Ziegler, B. Kunz, and P. Sonderegger. 1996. Intracellular signaling is changed after clustering of the neural cell adhesion molecules axonin-1 and NgCAM during neurite fasciculation. J. Cell Biol. 135:253-267.
40. Lefrancois, L., and D. S. Lyles. 1982. 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 121:168-174.
41. Marsh, M., and A. Helenius. 1989. Virus entry into animal cells. Adv. Virus Res. 36:107-151.
42. Marsh, M., and A. Helenius. 2006. Virus entry: open sesame. Cell 124:729-740.
43. Martinez, M. G., S. M. Cordo, and N. A. Candurra. 2007. Characterization of Junin arenavirus cell entry. J. Gen. Virol. 88:1776-1784.
44. McCormick, J. B., and S. P. Fisher-Hoch. 2002. Lassa fever. Curr. Top. Microbiol. Immunol. 262:75-109.
45. Michele, D. E., R. Barresi, M. Kanagawa, F. Saito, R. D. Cohn, J. S. Satz, J. Dollar, I. Nishino, R. I. Kelley, H. Somer, V. Straub, K. D. Mathews, S. A. Moore, and K. P. Campbell. 2002. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418: 417-422.
46. Müller, S., R. Gellers, and S. Gunther. 2007. Analysis of gene expression in Lassa virus-infected HuH-7 cells. J. Gen. Virol. 88:1568-1575.
47. Nakabayashi, H., K. Taketa, K. Miyano, T. Yamane, and J. Sato. 1982. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42:3858-3863.
48. Nichols, B. J. 2002. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4:374-378.
49. Oh, P., D. P. McIntosh, and J. E. Schnitzer. 1998. 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. 141:101-114.
50. Oldstone, M. B. 2002. Biology and pathogenesis of lymphocytic choriomeningitis virus infection. Curr. Top. Microbiol. Immunol. 263:83-117.
51. Parton, R. G., and A. A. Richards. 2003. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4:724-738.
52. Pelkmans, L., T. Burli, M. Zerial, and A. Helenius. 2004. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane trafficking. Cell 118:767-780.
53. Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
54. Pelkmans, L., D. Puntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535-539.
55. Perez, M., R. Clemente, C. S. Robison, E. Jeetendra, H. R. Jayakar, M. A. Whitt, and J. C. de la Torre. 2007. Generation and characterization of a recombinant vesicular stomatitis virus expressing the glycoprotein of Borna disease virus. J. Virol. 81:5527-5536.
56. Perez, M., M. Watanabe, M. A. Whitt, and J. C. de la Torre. 2001. N-terminal domain of Borna disease virus G (p56) protein is sufficient for virus receptor recognition and cell entry. J. Virol. 75:7078-7085.
57. Pietiäinen, 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.
58. Radoshitzky, S. R., J. Abraham, C. F. Spiropoulou, J. H. Kuhn, D. Nguyen, W. Li, J. Nagel, P. J. Schmidt, J. H. Nunberg, N. C. Andrews, M. Farzan, and H. Choe. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92-96.
59. Robison, C. S., and M. A. Whitt. 2000. The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J. Virol. 74:2239-2246.
60. Rodal, S. K., G. Skretting, O. Garred, F. Vilhardt, B. van Deurs, and K. Sandvig. 1999. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10:961-974.
61. Rojek, J. M., C. F. Spiropoulou, K. P. Campbell, and S. Kunz. 2007. Old World and clade C New World arenaviruses mimic the molecular mechanism of receptor recognition used by α-dystroglycan's host-derived ligands. J. Virol. 81:5685-5695.
62. Rose, J. K., and M. A. Whitt. 2001. Rhabdoviridae: the viruses and their replication, p. 1221-1244. In B. N. Fields and D. M. Knipe (ed.), Fields virology, 4th ed. Lippincott-Raven, Philadelphia, PA.
63. Sánchez, A. B., M. Perez, T. Cornu, and J. C. de la Torre. 2005. RNA interference-mediated virus clearance from cells both acutely and chronically infected with the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 79:11071-11081.
64. Schmid, S. L., and L. L. Carter. 1990. ATP is required for receptor-mediated endocytosis in intact cells. J. Cell Biol. 111:2307-2318.
65. Schnell, M. J., L. Buonocore, E. Kretzschmar, E. Johnson, and J. K. Rose. 1996. Foreign glycoproteins expressed from recombinant vesicular stomatitis viruses are incorporated efficiently into virus particles. Proc. Natl. Acad. Sci. USA 93:11359-11365.
66. Shah, W. A., H. Peng, and S. Carbonetto. 2006. Role of non-raft cholesterol in lymphocytic choriomeningitis virus infection via α-dystroglycan. J. Gen. Virol. 87:673-678.
67. Sieczkarski, S. B., and G. R. Whittaker. 2002. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76: 10455-10464.
68. Simons, K., and W. L. Vaz. 2004. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33:269-295.
69. Smith, A. E., and A. Helenius. 2004. How viruses enter animal cells. Science 304:237-242.
70. Spiropoulou, C. F., S. Kunz, P. E. Rollin, K. P. Campbell, and M. B. Oldstone. 2002. New World arenavirus clade C, but not clade A and B viruses, utilizes α-dystroglycan as its major receptor. J. Virol. 76:5140-5146.
71. Stang, E., J. Kartenbeck, and R. G. Parton. 1997. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 8:47-57.
72. Subtil, A., I. Gaidarov, K. Kobylarz, M. A. Lampson, J. H. Keen, and T. E. McGraw. 1999. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. USA 96:6775-6780.
73. Sun, X., V. K. Yau, B. J. Briggs, and G. R. Whittaker. 2005. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338:53-60.
74. Takada, A., C. Robison, H. Goto, A. Sanchez, K. G. Murti, M. A. Whitt, and Y. Kawaoka. 1997. A system for functional analysis of Ebola virus glycoprotein. Proc. Natl. Acad. Sci. USA 94:14764-14769.
75. Thorp, E. B., and T. M. Gallagher. 2004. Requirements for CEACAMs and cholesterol during murine coronavirus cell entry. J. Virol. 78:2682-2692.
76. van der Bliek, A. M., T. E. Redelmeier, H. Damke, E. J. Tisdale, E. M. Meyerowitz, and S. L. Schmid. 1993. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol. 122:553-563.
77. Weber, E. L., and M. J. Buchmeier. 1988. Fine mapping of a peptide sequence containing an antigenic site conserved among arenaviruses. Virology 164:30-38.
78. Yancey, P. G., W. V. Rodrigueza, E. P. Kilsdonk, G. W. Stoudt, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1996. Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271:16026-16034.
79. Yarar, D., C. M. Waterman-Storer, and S. L. Schmid. 2005. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol. Biol. Cell 16:964-975.
80. York, J., and J. H. Nunberg. 2006. Role of the stable signal peptide of Junin arenavirus envelope glycoprotein in pH-dependent membrane fusion. J. Virol. 80:7775-7780.