Binding of Lassa virus perturbs extracellular matrix-induced signal transduction via dystroglycan

Cellular Microbiology

Volumn 14, Issue 7, 2012, Pages 1122-1134

  Rojek, Jillian M ^d,e   Moraz, Marie Laurence ^a   Pythoud, Christelle ^a   Rothenberger, Sylvia ^a   Van der Goot, F Gisou ^b   Campbell, Kevin P ^c   Kunz, Stefan ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b EPFL   (Switzerland)

^c UNIVERSITY OF IOWA   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 6 BETA 1 INTEGRIN; BETA1 INTEGRIN; DYSTROGLYCAN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; EXTRACELLULAR MATRIX; LASSA VIRUS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANTIGENS, CD29; CELL LINE; DYSTROGLYCANS; EXTRACELLULAR MATRIX; HUMANS; LASSA VIRUS; MODELS, BIOLOGICAL; RECEPTORS, VIRUS; SIGNAL TRANSDUCTION; VIRUS ATTACHMENT;

ARENAVIRUS; LASSA VIRUS;

EID: 84862529684     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01784.x     Document Type: Article

References (57)

1. Baranowski, E., Ruiz-Jarabo, C.M., Pariente, N., Verdaguer, N., and Domingo, E. (2003) Evolution of cell recognition by viruses: a source of biological novelty with medical implications. Adv Virus Res 62: 19-111.
2. Barresi, R., and Campbell, K.P. (2006) Dystroglycan: from biosynthesis to pathogenesis of human disease. J Cell Sci 119: 199-207.
3. Barresi, R., Michele, D.E., Kanagawa, M., Harper, H.A., Dovicio, S.A., Satz, J.S., etal. (2004) LARGE can functionally bypass alpha-dystrolycan glycosylation defects in distinct congential muscular dystrophy. Nat Med 10: 696-703.
4. Beyer, W.R., Popplau, D., Garten, W., von Laer, D., and Lenz, O. (2003) Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J Virol 77: 2866-2872.
5. Borrow, P., and Oldstone, M.B. (1994) Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198: 1-9.
6. Buchmeier, M.J., Torre, J.C., and Peters, C.J. (2007) Arenaviridae: the viruses and their replication. In Fields Virology. Knipe, D.L., and Howley, P.M. (eds). Philadelphia: Lippincott-Raven, pp. 1791-1828.
7. Cao, W., Henry, M.D., Borrow, P., Yamada, H., Elder, J.H., Ravkov, E.V., etal. (1998) Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus [see comments]. Science 282: 2079-2081.
8. Cavaldesi, M., Macchia, G., Barca, S., Defilippi, P., Tarone, G., and Petrucci, T.C. (1999) Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction. J Neurochem 72: 1648-1655.
9. Ffrench-Constant, C., and Colognato, H. (2004) Integrins: versatile integrators of extracellular signals. Trends Cell Biol 14: 678-686.
10. Delwel, G.O., de Melker, A.A., Hogervorst, F., Jaspars, L.H., Fles, D.L., Kuikman, I., etal. (1994) Distinct and overlapping ligand specificities of the alpha 3A beta 1 and alpha 6A beta 1 integrins: recognition of laminin isoforms. Mol Biol Cell 5: 203-215.
11. Durbeej, M., Henry, M.D., Ferletta, M., Campbell, K.P., and Ekblom, P. (1998) Distribution of dystroglycan in normal adult mouse tissues. J Histochem Cytochem 46: 449-457.
12. Ervasti, J.M., and Campbell, K.P. (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66: 1121-1131.
13. Ervasti, J.M., and Campbell, K.P. (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823.
14. Eschli, B., Quirin, K., Wepf, A., Weber, J., Zinkernagel, R., and Hengartner, H. (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.
15. Fassler, R., and Meyer, M. (1995) Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 9: 1896-1908.
16. Fassler, R., Pfaff, M., Murphy, J., Noegel, A.A., Johansson, S., Timpl, R., and Albrecht, R. (1995) Lack of beta 1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J Cell Biol 128: 979-988.
17. Ferletta, M., Kikkawa, Y., Yu, H., Talts, J.F., Durbeej, M., Sonnenberg, A., etal. (2003) Opposing roles of integrin alpha6Abeta1 and dystroglycan in laminin-mediated extracellular signal-regulated kinase activation. Mol Biol Cell 14: 2088-2103.
18. Fisher-Hoch, S.P., Mitchell, S.W., Sasso, D.R., Lange, J.V., Ramsey, R., and McCormick, J.B. (1987) Physiological and immunologic disturbances associated with shock in a primate model of Lassa fever. J Infect Dis 155: 465-474.
19. Geisbert, T.W., and Jahrling, P.B. (2004) Exotic emerging viral diseases: progress and challenges. Nat Med 10: S110-S121.
20. Giancotti, F.G., and Ruoslahti, E. (1999) Integrin signaling. Science 285: 1028-1032.
21. Henry, M.D., and Campbell, K.P. (1998) A role for dystroglycan in basement membrane assembly. Cell 95: 859-870.
22. Henry, M.D., Satz, J.S., Brakebusch, C., Costell, M., Gustafsson, E., Fassler, R., and Campbell, K.P. (2001) Distinct roles for dystroglycan, beta1 integrin and perlecan in cell surface laminin organization. J Cell Sci 114: 1137-1144.
23. Hohenester, E., Tisi, D., Talts, J.F., and Timpl, R. (1999) The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol Cell 4: 783-792.
24. Igonet, S., Vaney, M.C., Vonhrein, C., Bricogne, G., Stura, E.A., Hengartner, H., etal. (2011) X-ray structure of the arenavirus glycoprotein GP2 in its postfusion hairpin conformation. Proc Natl Acad Sci USA 108: 19967-19972.
25. Kanagawa, M., and Toda, T. (2006) The genetic and molecular basis of muscular dystrophy: roles of cell-matrix linkage in the pathogenesis. J Hum Genet 13: 13.
26. Kanagawa, M., Saito, F., Kunz, S., Yoshida-Moriguchi, T., Barresi, R., Kobayashi, Y.M., etal. (2004) Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell 117: 953-964.
27. Kunz, S. (2009) The role of the vascular endothelium in arenavirus haemorrhagic fevers. Thromb Haemost 102: 1024-1029.
28. Kunz, S., Sevilla, N., McGavern, D.B., Campbell, K.P., and Oldstone, M.B. (2001) Molecular analysis of the interaction of LCMV with its cellular receptor [alpha]-dystroglycan. J Cell Biol 155: 301-310.
29. Kunz, S., Campbell, K.P., and Oldstone, M.B. (2003) Alpha-dystroglycan can mediate arenavirus infection in the absence of beta-dystroglycan. Virology 316: 213-220.
30. Kunz, S., Calder, L., and Oldstone, M.B. (2004) Electron microscopy of an alpha-dystroglycan fragment containing receptor sites for lymphocytic choriomeningitis virus and laminin, and use of the receptoid body as a reagent to neutralize virus. Virology 325: 207-215.
31. Kunz, S., Rojek, J., Perez, M., Spiropoulou, C., and Oldstone, M.B. (2005a) Characterization of the interaction of Lassa fever virus with its cellular receptor α-dystroglycan. J Virol 79: 5979-5987.
32. Kunz, S., Rojek, J., Spiropoulou, C., Barresi, R., Campbell, K.P., and Oldstone, M.B. (2005b) Post-translational modification of alpha-dystroglycan, the cellular receptor for arenaviruses by the glycosyltransferase LARGE is critical for virus binding. J Virol 79: 14282-14296.
33. Lenz, O., ter Meulen, J., Klenk, H.D., Seidah, N.G., and Garten, W. (2001) The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc Natl Acad Sci USA 98: 12701-12705.
34. McCormick, J.B., and Fisher-Hoch, S.P. (2002) Lassa fever. Curr Top Microbiol Immunol 262: 75-109.
35. Marsh, M., and Helenius, A. (2006) Virus entry: open sesame. Cell 124: 729-740.
36. Michele, D.E., Barresi, R., Kanagawa, M., Saito, F., Cohn, R.D., Satz, J.S., etal. (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418: 417-422.
37. Moore, C.J., and Winder, S.J. (2010) Dystroglycan versatility in cell adhesion: a tale of multiple motifs. Cell Commun Signal 8: 3.
38. Moraz, M.L., and Kunz, S. (2011) Pathogenesis of arenavirus hemorrhagic fevers. Expert Rev Anti Infect Ther 9: 49-59.
39. Ohkuma, S., and Poole, B. (1978) Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci USA 75: 3327-3331.
40. Ohkuma, S., and Poole, B. (1981) Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances. J Cell Biol 90: 656-664.
41. Oldstone, M.B., and Campbell, K.P. (2011) Decoding arenavirus pathogenesis: essential roles for alpha-dystroglycan-virus interactions and the immune response. Virology 411: 170-179.
42. Quirin, K., Eschli, B., Scheu, I., Poort, L., Kartenbeck, J., and Helenius, A. (2008) Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 378: 21-33.
43. Reignier, T., Oldenburg, J., Noble, B., Lamb, E., Romanowski, V., Buchmeier, M.J., and Cannon, P.M. (2006) Receptor use by pathogenic arenaviruses. Virology 353: 111-120.
44. Rojek, J.M., Spiropoulou, C.F., and Kunz, S. (2006) Characterization of the cellular receptors for the South American hemorrhagic fever viruses Junin, Guanarito, and Machupo. Virology 349: 476-491.
45. Rojek, J.M., Spiropoulou, C.F., Campbell, K.P., and Kunz, S. (2007a) Old World and Clade C New World arenaviruses mimic the molecular mechanism of receptor recognition used by {alpha}-dystroglycan's host-derived ligands. J Virol 81: 5685-5695.
46. Rojek, J.M., Campbell, K.P., Oldstone, M.B., and Kunz, S. (2007b) Old World arenavirus infection interferes with the expression of functional {alpha}-dystroglycan in the host cell. Mol Biol Cell 29: 29.
47. Rojek, J.M., Perez, M., and Kunz, S. (2008a) Cellular entry of lymphocytic choriomeningitis virus. J Virol 82: 1505-1517.
48. Rojek, J.M., Sanchez, A.B., Nguyen, N.T., de la Torre, J.C., and Kunz, S. (2008b) Different mechanisms of cell entry by human-pathogenic Old World and New World arenaviruses. J Virol 82: 7677-7687.
49. Rojek, J.M., Lee, A.M., Nguyen, N., Spiropoulou, C.F., and Kunz, S. (2008c) Site 1 protease is required for proteolytic processing of the glycoproteins of the South American hemorrhagic fever viruses Junin, Machupo, and Guanarito. J Virol 82: 6045-6051.
50. Shimojima, M., Stroher, U., Ebihara, H., Feldmann, H., and Kawaoka, Y. (2012) Identification of cell surface molecules involved in dystroglycan-independent Lassa virus cell entry. J Virol 86: 2067-2078.
51. Smith, A.E., and Helenius, A. (2004) How viruses enter animal cells. Science 304: 237-242.
52. Spence, H.J., Dhillon, A.S., James, M., and Winder, S.J. (2004) Dystroglycan, a scaffold for the ERK-MAP kinase cascade. EMBO Rep 5: 484-489.
53. Spiropoulou, C.F., Kunz, S., Rollin, P.E., Campbell, K.P., and Oldstone, M.B. (2002) New World arenavirus clade C, but not clade A and B viruses, utilizes alpha-dystroglycan as its major receptor. J Virol 76: 5140-5146.
54. Walker, D.H., McCormick, J.B., Johnson, K.M., Webb, P.A., Komba-Kono, G., Elliott, L.H., and Gardner, J.J. (1982) Pathologic and virologic study of fatal Lassa fever in man. Am J Pathol 107: 349-356.
55. Weber, E.L., and Buchmeier, M.J. (1988) Fine mapping of a peptide sequence containing an antigenic site conserved among arenaviruses. Virology 164: 30-38.
56. Wei, J., Shaw, L.M., and Mercurio, A.M. (1998) Regulation of mitogen-activated protein kinase activation by the cytoplasmic domain of the alpha6 integrin subunit. J Biol Chem 273: 5903-5907.
57. Yang, B., Jung, D., Motto, D., Meyer, J., Koretzky, G., and Campbell, K.P. (1995) SH3 domain-mediated interaction of dystroglycan and Grb2. J Biol Chem 270: 11711-11714.