1887

Journal of General Virology header logo

Volume 89, Issue 11

Post-translational modification of -dystroglycan is not critical for lymphocytic choriomeningitis virus receptor function Free

Abstract

-Dystroglycan (-DG) is a ubiquitously expressed molecule that has been identified as a cellular receptor for lymphocytic choriomeningitis virus (LCMV) and other arenaviruses. Recently, it was demonstrated that LCMV receptor function is critically dependent on post-translational modifications, namely glycosylation. In particular, it was shown that -mannosylation, a rare type of mammalian -linked glycosylation, is important in determining the binding of LCMV to its cellular receptor. All studies carried out so far showed a dependence on glycosylation in LCMV receptor function . This work extended these studies to two models of -DG hypoglycosylation. The results confirm earlier findings on the dependence of carbohydrate modifications in LCMV receptor function. However, experiments in animal models showed that this dependence was only very weak . It is likely that alternative receptors or alternative entry pathways may account for this attenuated phenotype.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.2008/004721-0
2008-11-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/11/2713.html?itemId=/content/journal/jgv/10.1099/vir.0.2008/004721-0&mimeType=html&fmt=ahah

References

  1. Barber D. L., Wherry E. J., Masopust D., Zhu B., Allison J. P., Sharpe A. H., Freeman G. J., Ahmed R. 2006; Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682–687 [CrossRef]
     [Google Scholar]
  2. Barresi R., Michele D. E., Kanagawa M., Harper H. A., Dovico S. A., Satz J. S., Moore S. A., Zhang W., Schachter H. other authors 2004; LARGE can functionally bypass α -dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat Med 10:696–703 [CrossRef]
     [Google Scholar]
  3. Battegay M., Cooper S., Althage A., Banziger J., Hengartner H., Zinkernagel R. M. 1991; Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J Virol Methods 33:191–198 [CrossRef]
     [Google Scholar]
  4. Beyer W. R., Popplau D., Garten W., von Laer D., Lenz O. 2003; Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P. J Virol 77:2866–2872 [CrossRef]
     [Google Scholar]
  5. Borrow P., Oldstone M. B. 1994; Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 198:1–9 [CrossRef]
     [Google Scholar]
  6. Brancaccio A., Schulthess T., Gesemann M., Engel J. 1995; Electron microscopic evidence for a mucin-like region in chick muscle α -dystroglycan. FEBS Lett 368:139–142 [CrossRef]
     [Google Scholar]
  7. Buchmeier M. J., Oldstone M. B. 1979; Protein structure of lymphocytic choriomeningitis virus: evidence for a cell-associated precursor of the virion glycopeptides. Virology 99:111–120 [CrossRef]
     [Google Scholar]
  8. Buchmeier M. J., Welsh R. M., Dutko F. J., Oldstone M. B. 1980; The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv Immunol 30:275–331
     [Google Scholar]
  9. Cao W., Henry M. D., Borrow P., Yamada H., Elder J. H., Ravkov E. V., Nichol S. T., Compans R. W., Campbell K. P., Oldstone M. B. 1998; Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282:2079–2081 [CrossRef]
     [Google Scholar]
  10. Chiba A., Matsumura K., Yamada H., Inazu T., Shimizu T., Kusunoki S., Kanazawa I., Kobata A., Endo T. 1997; Structures of sialylated O -linked oligosaccharides of bovine peripheral nerve α -dystroglycan. The role of a novel O -mannosyl-type oligosaccharide in the binding of α -dystroglycan with laminin. J Biol Chem 272:2156–2162 [CrossRef]
     [Google Scholar]
  11. Di Simone C., Buchmeier M. J. 1995; Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 209:3–9 [CrossRef]
     [Google Scholar]
  12. Di Simone C., Zandonatti M. A., Buchmeier M. J. 1994; Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike. Virology 198:455–465 [CrossRef]
     [Google Scholar]
  13. Ervasti J. M., Campbell K. P. 1991; Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121–1131 [CrossRef]
     [Google Scholar]
  14. Ervasti J. M., 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 [CrossRef]
     [Google Scholar]
  15. Fujimura K., Sawaki H., Sakai T., Hiruma T., Nakanishi N., Sato T., Ohkura T., Narimatsu H. 2005; LARGE2 facilitates the maturation of α -dystroglycan more effectively than LARGE. Biochem Biophys Res Commun 329:1162–1171 [CrossRef]
     [Google Scholar]
  16. Grewal P. K., Holzfeind P. J., Bittner R. E., Hewitt J. E. 2001; Mutant glycosyltransferase and altered glycosylation of α -dystroglycan in the myodystrophy mouse. Nat Genet 28:151–154 [CrossRef]
     [Google Scholar]
  17. Grewal P. K., McLaughlan J. M., Moore C. J., Browning C. A., Hewitt J. E. 2005; Characterization of the LARGE family of putative glycosyltransferases associated with dystroglycanopathies. Glycobiology 15:912–923 [CrossRef]
     [Google Scholar]
  18. Holt K. H., Crosbie R. H., Venzke D. P., Campbell K. P. 2000; Biosynthesis of dystroglycan: processing of a precursor propeptide. FEBS Lett 468:79–83 [CrossRef]
     [Google Scholar]
  19. Holzfeind P. J., Grewal P. K., Reitsamer H. A., Kechvar J., Lassmann H., Hoeger H., Hewitt J. E., Bittner R. E. 2002; Skeletal, cardiac and tongue muscle pathology, defective retinal transmission, and neuronal migration defects in the Largemyd mouse defines a natural model for glycosylation-deficient muscle–eye–brain disorders. Hum Mol Genet 11:2673–2687 [CrossRef]
     [Google Scholar]
  20. Ibraghimov-Beskrovnaya O., Ervasti J. M., Leveille C. J., Slaughter C. A., Sernett S. W., Campbell K. P. 1992; Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696–702 [CrossRef]
     [Google Scholar]
  21. Imperiali M., Thoma C., Pavoni E., Brancaccio A., Callewaert N., Oxenius A. 2005; O Mannosylation of α -dystroglycan is essential for lymphocytic choriomeningitis virus receptor function. J Virol 79:14297–14308 [CrossRef]
     [Google Scholar]
  22. Inaba K., Inaba M., Romani N., Aya H., Deguchi M., Ikehara S., Muramatsu S., Steinman R. M. 1992; Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176:1693–1702 [CrossRef]
     [Google Scholar]
  23. Kanagawa M., Saito F., Kunz S., Yoshida-Moriguchi T., Barresi R., Kobayashi Y. M., Muschler J., Dumanski J. P., Michele D. E. other authors 2004; Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell 117:953–964 [CrossRef]
     [Google Scholar]
  24. Kunz S., Edelmann K. H., de la Torre J. C., Gorney R., Oldstone M. B. 2003; Mechanisms for lymphocytic choriomeningitis virus glycoprotein cleavage, transport, and incorporation into virions. Virology 314:168–178 [CrossRef]
     [Google Scholar]
  25. Kunz S., Sevilla N., Rojek J. M., Oldstone M. B. 2004; Use of alternative receptors different than α -dystroglycan by selected isolates of lymphocytic choriomeningitis virus. Virology 325:432–445 [CrossRef]
     [Google Scholar]
  26. Kunz S., Rojek J. M., Kanagawa M., Spiropoulou C. F., Barresi R., Campbell K. P., Oldstone M. B. 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 [CrossRef]
     [Google Scholar]
  27. Lamers M. C., De Groot E. R., Roos D. 1981; Phagocytosis and degradation of DNA–anti-DNA complexes by human phagocytes II. Influence of the size of the complexes. Eur J Immunol 11:764–768 [CrossRef]
     [Google Scholar]
  28. Levedakou E. N., Chen X. J., Soliven B., Popko B. 2005; Disruption of the mouse Large gene in the enr and myd mutants results in nerve, muscle, and neuromuscular junction defects. Mol Cell Neurosci 28:757–769 [CrossRef]
     [Google Scholar]
  29. Liu J., Ball S. L., Yang Y., Mei P., Zhang L., Shi H., Kaminski H. J., Lemmon V. P., Hu H. 2006; A genetic model for muscle–eye–brain disease in mice lacking protein O -mannose 1,2- N -acetylglucosaminyltransferase (POMGnT1. Mech Dev 123:228–240 [CrossRef]
     [Google Scholar]
  30. Longman C., Brockington M., Torelli S., Jimenez-Mallebrera C., Kennedy C., Khalil N., Feng L., Saran R. K., Voit T. other authors 2003; Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of α -dystroglycan. Hum Mol Genet 12:2853–2861 [CrossRef]
     [Google Scholar]
  31. Michele D. E., Barresi R., Kanagawa M., Saito F., Cohn R. D., Satz J. S., Dollar J., Nishino I., Kelley R. I. other authors 2002; Post-translational disruption of dystroglycan–ligand interactions in congenital muscular dystrophies. Nature 418:417–422 [CrossRef]
     [Google Scholar]
  32. Ochsenbein A. F., Fehr T., Lutz C., Suter M., Brombacher F., Hengartner H., Zinkernagel R. M. 1999; Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156–2159 [CrossRef]
     [Google Scholar]
  33. Peyrard M., Seroussi E., Sandberg-Nordqvist A. C., Xie Y. G., Han F. Y., Fransson I., Collins J., Dunham I., Kost-Alimova M. other authors 1999; The human LARGE gene from 22q12.3-q13.1 is a new, distinct member of the glycosyltransferase gene family. Proc Natl Acad Sci U S A 96:598–603 [CrossRef]
     [Google Scholar]
  34. Rambukkana A., Yamada H., Zanazzi G., Mathus T., Salzer J. L., Yurchenco P. D., Campbell K. P., Fischetti V. A. 1998; Role of α -dystroglycan as a Schwann cell receptor for Mycobacterium leprae . Science 282:2076–2079 [CrossRef]
     [Google Scholar]
  35. Riviere Y., Ahmed R., Southern P. J., Buchmeier M. J., Dutko F. J., Oldstone M. B. 1985; The S RNA segment of lymphocytic choriomeningitis virus codes for the nucleoprotein and glycoproteins 1 and 2. J Virol 53:966–968
     [Google Scholar]
  36. Sabeti P. C., Varilly P., Fry B., Lohmueller J., Hostetter E., Cotsapas C., Xie X., Byrne E. H., McCarroll S. A. other authors 2007; Genome-wide detection and characterization of positive selection in human populations. Nature 449:913–918 [CrossRef]
     [Google Scholar]
  37. Salvato M. S., Shimomaye E. M. 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 [CrossRef]
     [Google Scholar]
  38. Salvato M., Shimomaye E., Oldstone M. B. 1989; The primary structure of the lymphocytic choriomeningitis virus L gene encodes a putative RNA polymerase. Virology 169:377–384 [CrossRef]
     [Google Scholar]
  39. Salvato M. S., Schweighofer K. J., Burns J., Shimomaye E. M. 1992; Biochemical and immunological evidence that the 11 kDa zinc-binding protein of lymphocytic choriomeningitis virus is a structural component of the virus. Virus Res 22:185–198 [CrossRef]
     [Google Scholar]
  40. Sevilla N., Kunz S., Holz A., Lewicki H., Homann D., Yamada H., Campbell K. P., de La Torre J. C., Oldstone M. B. 2000; Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J Exp Med 192:1249–1260 [CrossRef]
     [Google Scholar]
  41. Singh M. K., Fuller-Pace F. V., Buchmeier M. J., Southern P. J. 1987; Analysis of the genomic L RNA segment from lymphocytic choriomeningitis virus. Virology 161:448–456 [CrossRef]
     [Google Scholar]
  42. Smelt S. C., Borrow P., Kunz S., Cao W., Tishon A., Lewicki H., Campbell K. P., Oldstone M. B. 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 [CrossRef]
     [Google Scholar]
  43. Spiropoulou C. F., Kunz S., Rollin P. E., Campbell K. P., Oldstone M. B. 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 [CrossRef]
     [Google Scholar]
  44. Waldburger J. M., Suter T., Fontana A., Acha-Orbea H., Reith W. 2001; Selective abrogation of major histocompatibility complex class II expression on extrahematopoietic cells in mice lacking promoter IV of the class II transactivator gene. J Exp Med 194:393–406 [CrossRef]
     [Google Scholar]
  45. Weigle W. O. 1973; Immunological unresponsiveness. Adv Immunol 16:61–122
     [Google Scholar]
  46. Wilson I. B., Gavel Y., von Heijne G. 1991; Amino acid distributions around O -linked glycosylation sites. Biochem J 275:529–534
     [Google Scholar]
  47. Wolint P., Betts M. R., Koup R. A., Oxenius A. 2004; Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells. J Exp Med 199:925–936 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.2008/004721-0
Loading
Post-translational modification of α-dystroglycan is not critical for lymphocytic choriomeningitis virus receptor function in vivo
J. Gen. Virol. 89, 2713 (2008); https://doi.org/10.1099/vir.0.2008/004721-0
/content/journal/jgv/10.1099/vir.0.2008/004721-0
/content/journal/jgv/10.1099/vir.0.2008/004721-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error