O mannosylation of α-dystroglycan is essential for lymphocytic choriomeningitis virus receptor function

Journal of Virology

Volumn 79, Issue 22, 2005, Pages 14297-14308

  Imperiali, Mauro ^a   Thoma, Claudio ^a   Pavoni, Ernesto ^b   Brancaccio, Andrea ^b   Callewaert, Nico ^a   Oxenius, Annette ^a  

^a ETH ZURICH   (Switzerland)

^b CATHOLIC UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DYSTROGLYCAN; DYSTROGLYCAN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; LASSA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; O MANNOSYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SYMPTOMATOLOGY; VIRUS CELL INTERACTION; VIRUS INFECTIVITY;

ANIMALS; ARENAVIRIDAE INFECTIONS; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; DOGS; DYSTROGLYCANS; FIBROBLASTS; FLOW CYTOMETRY; GLYCOSYLATION; HUMANS; JURKAT CELLS; L CELLS (CELL LINE); LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MANNOSE; MICE; RECEPTORS, VIRUS;

ANIMALIA; ARENAVIRUS; LASSA FEVER VIRUS; LASSA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MAMMALIA;

EID: 27644582353     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.22.14297-14308.2005     Document Type: Article

References (55)

1. Akasaka-Manya, K., H. Manya, and T. Endo. 2004. Mutations of the POMT1 gene found in patients with Walker-Warburg syndrome lead to a defect of protein O-mannosylation. Biochem. Biophys. Res. Commun. 325: 75-79.
2. Barresi, R., D. E. Michele, M. Kanagawa, H. A. Harper, S. A. Dovico, J. S. Satz, S. A. Moore, W. Zhang, H. Schachter, J. P. Dumanski, R. D. Cohn, I. Nishino, and K. P. Campbell. 2004. LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat. Med. 10:696-703.
3. Battegay, M., S. Cooper, A. Althage, J. Banziger, H. Hengartner, and R. M. Zinkernagel. 1991. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33:191-198.
4. 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.
5. Bozic, D., F. Sciandra, D. Lamba, and A. Brancaccio. 2004. The structure of the N-terminal region of murine skeletal muscle alpha-dystroglycan discloses a modular architecture. J. Biol. Chem. 279:44812-44816.
6. Brancaccio, A., T. Schulthess, M. Gesemann, and J. Engel. 1995. Electron microscopic evidence for a mucin-like region in chick muscle alpha-dystroglycan. FEBS Lett. 368:139-142.
7. Bruns, M., J. Cihak, G. Muller, and F. Lehmann-Grube. 1983. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization. Virology 130:247-251.
8. Buchmeier, M. J., and M. B. Oldstone. 1979. Protein structure of lymphocytic choriomeningitis virus: evidence for a cell-associated precursor of the virion glycopeptides. Virology 99:111-120.
9. Buchmeier, M. J., R. M. Welsh, F. J. Dutko, and M. B. Oldstone. 1980. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30:275-331.
10. Camp, L. A., P. Chauhan, J. D. Farrar, and M. A. Lehrman. 1993. Defective mannosylation of glycosylphosphatidylinositol in Lec35 Chinese hamster ovary cells. J. Biol. Chem. 268:6721-6728.
11. 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 alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079-2081.
12. Chiba, A., K. Matsumura, H. Yamada, T. Inazu, T. Shimizu, S. Kusunoki, I. Kanazawa, A. Kobata, and T. Endo. 1997. Structures of sialylated O-linked oligosaccharides of bovine peripheral nerve alpha-dystroglycan. The role of a novel O-mannosyl-type oligosaccharide in the binding of alpha-dystroglycan with laminin. J. Biol. Chem. 272:2156-2162.
13. Chu, V. C., and G. R. Whittaker. 2004. Influenza virus entry and infection require host cell N-linked glycoprotein. Proc. Natl. Acad. Sci. USA 101: 18153-18158.
14. Cormand, B., H. Pihko, M. Bayes, L. Valanne, P. Santavuori, B. Talim, R. Gershoni-Baruch, A. Ahmad, H. van Bokhoven, H. G. Brunner, T. Voit, H. Topaloglu, W. B. Dobyns, and A. E. Lehesjoki. 2001. Clinical and genetic distinction between Walker-Warburg syndrome and muscle-eye-brain disease. Neurology 56:1059-1069.
15. Diesen, C., A. Saarinen, H. Pihko, C. Rosenlew, B. Cormand, W. B. Dobyns, J. Dieguez, L. Valanne, T. Joensuu, and A. E. Lehesjoki. 2004. POMGnT1 mutation and phenotypic spectrum in muscle-eye-brain disease. J. Med. Genet. 41:e115.
16. Doucey, M. A., D. Hess, R. Cacan, and J. Hofsteenge. 1998. Protein C-mannosylation is enzyme-catalysed and uses dolichyl-phosphate-mannose as a precursor. Mol. Biol. Cell 9:291-300.
17. Durbeej, M., and K. P. Campbell. 1999. Biochemical characterization of the epithelial dystroglycan complex. J. Biol. Chem. 274:26609-26616.
18. Endo, T. 1999. O-mannosyl glycans in mammals. Biochim. Biophys. Acta 1473:237-246.
19. Englund, P. T. 1993. The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu. Rev. Biochem. 62:121-138.
20. Ervasti, J. M., A. L. Burwell, and A. L. Geissler. 1997. Tissue-specific heterogeneity in alpha-dystroglycan sialoglycosylation. Skeletal muscle alpha-dystroglycan is a latent receptor for Vicia villosa agglutinin b4 masked by sialic acid modification. J. Biol. Chem. 272:22315-22321.
21. Ervasti, J. M., and K. P. Campbell. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121-1131.
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. Ferreira, L., E. Villar, and I. Munoz-Barroso. 2004. Gangliosides and N-glycoproteins function as Newcastle disease virus receptors. Int. J. Biochem. Cell Biol. 36:2344-2356.
24. Gee, S. H., R. W. Blacher, P. J. Douville, P. R. Provost, P. D. Yurchenco, and S. Carbonetto. 1993. Laminin-binding protein 120 from brain is closely related to the dystrophin-associated glycoprotein, dystroglycan, and binds with high affinity to the major heparin binding domain of laminin. J. Biol. Chem. 268:14972-14980.
25. Henry, M. D., and K. P. Campbell. 1999. Dystroglycan inside and out. Curr. Opin. Cell Biol. 11:602-607.
26. Herscovics, A., and P. Orlean. 1993. Glycoprotein biosynthesis in yeast. FASEB J. 7:540-550.
27. Hirschberg, C. B., and M. D. Snider. 1987. Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus. Annu. Rev. Biochem. 56:63-87.
28. Ibraghimov-Beskrovnaya, O., J. M. Ervasti, C. J. Leveille, C. A. Slaughter, S. W. Sernett, and K. P. Campbell. 1992. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
29. Ibraghimov-Beskrovnaya, O., A. Milatovich, T. Ozcelik, B. Yang, K. Koepnick, U. Francke, and K. P. Campbell. 1993. Human dystroglycan: skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum. Mol. Genet. 2:1651-1657.
30. Kornfeld, R., and S. Kornfeld. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664.
31. Kunz, S., J. M. Rojek, M. Kanagawa, C. F. Spiropoulou, R. Barresi, K. P. Campbell, and M. B. A. 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.
32. 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.
33. Kunz, S., N. Sevilla, J. M. Rojek, and M. B. Oldstone. 2004. Use of alternative receptors different than alpha-dystroglycan by selected isolates of lymphocytic choriomeningitis virus. Virology 325:432-445.
34. Maeda, Y., S. Tanaka, J. Hino, K. Kangawa, and T. Kinoshita. 2000. Human dolichol-phosphate-mannose synthase consists of three subunits, DPM1, DPM2 and DPM3. EMBO J. 19:2475-2482.
35. Maeda, Y., S. Tomita, R. Watanabe, K. Ohishi, and T. Kinoshita. 1998. DPM2 regulates biosynthesis of dolichol phosphate-mannose in mammalian cells: correct subcellular localization and stabilization of DPM1, and binding of dolichol phosphate. EMBO J. 17:4920-4929.
36. Manya, H., K. Sakai, K. Kobayashi, K. Taniguchi, M. Kawakita, T. Toda, and T. Endo. 2003. Loss-of-function of an N-acetylglucosaminyltransferase, POMGnT1, in muscle-eye-brain disease. Biochem. Biophys. Res. Commun. 306:93-97.
37. 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.
38. Michele, D. E., and K. P. Campbell. 2003. Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J. Biol. Chem. 278: 15457-15460.
39. Parekh, B. S., and M. J. Buchmeier. 1986. Proteins of lymphocytic choriomeningitis virus: antigenic topography of the viral glycoproteins. Virology 153:168-178.
40. Patnaik, S. K., and P. Stanley. 2005. Mouse large can modify complex N- and mucin O-glycans on alpha-dystroglycan to induce laminin binding. J. Biol. Chem. 280:20851-20859.
41. Pu, L., J. R. Scocca, B. K. Walker, and S. S. Krag. 2003. A single point mutation resulting in an adversely reduced expression of DPM2 in the Lec15.1 cells. Biochem. Biophys. Res. Commun. 312:555-561.
42. Rambukkana, A., H. Yamada, G. Zanazzi, T. Mathus, J. L. Salzer, P. D. Yurchenco, K. P. Campbell, and V. A. Fischetti. 1998. Role of alpha-dystroglycan as a Schwann cell receptor for Mycobacterium leprae. Science 282: 2076-2079.
43. Riviere, Y., R. Ahmed, P. J. Southern, M. J. Buchmeier, F. J. Dutko, and M. B. Oldstone. 1985. The S RNA segment of lymphocytic choriomeningitis virus codes for the nucleoprotein and glycoproteins 1 and 2. J. Virol. 53: 966-968.
44. Salvato, M. S., and E. M. Shimomaye. 1989. The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173:1-10.
45. Sasaki, T., H. Yamada, K. Matsumura, T. Shimizu, A. Kobata, and T. Endo. 1998. Detection of O-mannosyl glycans in rabbit skeletal muscle alpha-dystroglycan. Biochim. Biophys. Acta 1425:599-606.
46. Sevilla, N., S. Kunz, A. Holz, H. Lewicki, D. Homann, H. Yamada, K. P. Campbell, J. C. de La Torre, and M. B. Oldstone. 2000. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 192:1249-1260.
47. Singh, J., Y. Itahana, S. Knight-Krajewski, M. Kanagawa, K. P. Campbell, M. J. Bissell, and J. Muschler. 2004. Proteolytic enzymes and altered glycosylation modulate dystroglycan function in carcinoma cells. Cancer Res. 64:6152-6159.
48. Singh, M. K., F. V. Fuller-Pace, M. J. Buchmeier, and P. J. Southern. 1987. Analysis of the genomic L RNA segment from lymphocytic choriomeningitis virus. Virology 161:448-456.
49. Smelt, S. C., P. Borrow, S. Kunz, W. Cao, A. Tishon, H. Lewicki, K. P. Campbell, and M. B. Oldstone. 2001. Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor α-dystroglycan correlate with viral tropism and disease kinetics. J. Virol. 75:448-457.
50. Wang, J., G. J. Babcock, H. Choe, M. Farzan, J. Sodroski, and D. Gabuzda. 2004. N-linked glycosylation in the CXCR4 N-terminus inhibits binding to HIV-1 envelope glycoproteins. Virology 324:140-150.
51. Willer, T., B. Prados, J. M. Falcon-Perez, I. Renner-Muller, G. K. Przemeck, M. Lommel, A. Coloma, M. C. Valero, M. H. de Angelis, W. Tanner, E. Wolf, S. Strahl, and J. Cruces. 2004. Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc. Natl. Acad. Sci. USA 101:14126-14131.
52. Willer, T., M. C. Valero, W. Tanner, J. Cruces, and S. Strahl. 2003. O-mannosyl glycans: from yeast to novel associations with human disease. Curr. Opin. Struct. Biol. 13:621-630.
53. Williamson, R. A., M. D. Henry, K. J. Daniels, R. F. Hrstka, J. C. Lee, Y. Sunada, O. Ibraghimov-Beskrovnaya, and K. P. Campbell. 1997. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6:831-841.
54. Wilson, I. B., Y. Gavel, and G. von Heijne. 1991. Amino acid distributions around O-linked glycosylation sites. Biochem. J. 275:529-534.
55. Yoshida, A., K. Kobayashi, H. Manya, K. Taniguchi, H. Kano, M. Mizuno, T. Inazu, H. Mitsuhashi, S. Takahashi, M. Takeuchi, R. Herrmann, V. Straub, B. Talim, T. Voit, H. Topaloglu, T. Toda, and T. Endo. 2001. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev. Cell 1:717-724.