Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1989 Sep 1;262(2):479–484. doi: 10.1042/bj2620479

Temporal aspects of O-glycosylation of glycoprotein C from herpes simplex virus type-1.

F Serafini-Cessi 1, F Dall'Olio 1, N Malagolini 1, G Campadelli-Fiume 1
PMCID: PMC1133293  PMID: 2552998

Abstract

Herpes simplex virus type-1 glycoprotein C (gC1) contains several O-linked oligosaccharides clustered near N-linked chains, and Pronase digestion produces glycopeptides carrying both oligosaccharide types. We have taken advantage of this fact to investigate the temporal relationship between the initiation of O-linked chains and the processing of N-linked oligosaccharides. gC1 was isolated from herpes-simplex-virus-infected BHK (baby-hamster kidney) cells after short labelling periods with [3H]glucosamine, and the labelled Pronase-cleaved glycopeptides fractionated on concanavalin A-Sepharose. N-[3H]Acetylgalactosamine, mostly convertible into free N-[3H]acetylgalactosaminitol on mild alkaline-borohydride treatment, was found in glycopeptides with an affinity to concanavalin A-Sepharose corresponding to that of glycopeptides carrying Man8GlcNAc2 or larger N-linked chains. Since there is evidence that the processing of N-linked chains up to Man8GlcNAc2 involves enzymes located in the rough endoplasmic reticulum, current results strongly suggest that gC1 acquires O-linked N-acetylgalactosamine before the glycoprotein routing to the Golgi apparatus. The addition of the second sugar to the nascent O-linked chain appeared to occur after a relatively long lag time.

Full text

PDF
479

Images in this article

482Fig. 3.
on p.482

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abeijon C., Hirschberg C. B. Subcellular site of synthesis of the N-acetylgalactosamine (alpha 1-0) serine (or threonine) linkage in rat liver. J Biol Chem. 1987 Mar 25;262(9):4153–4159. [PubMed] [Google Scholar]
  2. Baenziger J. U., Fiete D. Structural determinants of concanavalin A specificity for oligosaccharides. J Biol Chem. 1979 Apr 10;254(7):2400–2407. [PubMed] [Google Scholar]
  3. Bergh M. L., Koppen P., van den Eijnden D. H. High-pressure liquid chromatography of sialic acid-containing oligosaccharides. Carbohydr Res. 1981 Aug 1;94(2):225–229. doi: 10.1016/s0008-6215(00)80720-x. [DOI] [PubMed] [Google Scholar]
  4. Cummings R. D., Kornfeld S., Schneider W. J., Hobgood K. K., Tolleshaug H., Brown M. S., Goldstein J. L. Biosynthesis of N- and O-linked oligosaccharides of the low density lipoprotein receptor. J Biol Chem. 1983 Dec 25;258(24):15261–15273. [PubMed] [Google Scholar]
  5. Dall'Olio F., Malagolini N., Campadelli-Fiume G., Serafini-Cessi F. Glycosylation pattern of herpes simplex virus type 2 glycoprotein G from precursor species to the mature form. Arch Virol. 1987;97(3-4):237–249. doi: 10.1007/BF01314424. [DOI] [PubMed] [Google Scholar]
  6. Dall'Olio F., Malagolini N., Speziali V., Campadelli-Fiume G., Serafini-Cessi F. Sialylated oligosaccharides O-glycosidically linked to glycoprotein C from herpes simplex virus type 1. J Virol. 1985 Oct;56(1):127–134. doi: 10.1128/jvi.56.1.127-134.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edge A. S., Spiro R. G. Presence of sulfate in N-glycosidically linked carbohydrate units of calf thyroid plasma membrane glycoproteins. J Biol Chem. 1984 Apr 25;259(8):4710–4713. [PubMed] [Google Scholar]
  8. Elhammer A., Kornfeld S. Two enzymes involved in the synthesis of O-linked oligosaccharides are localized on membranes of different densities in mouse lymphoma BW5147 cells. J Cell Biol. 1984 Jul;99(1 Pt 1):327–331. doi: 10.1083/jcb.99.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frink R. J., Eisenberg R., Cohen G., Wagner E. K. Detailed analysis of the portion of the herpes simplex virus type 1 genome encoding glycoprotein C. J Virol. 1983 Feb;45(2):634–647. doi: 10.1128/jvi.45.2.634-647.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Godelaine D., Spiro M. J., Spiro R. G. Processing of the carbohydrate units of thyroglobulin. J Biol Chem. 1981 Oct 10;256(19):10161–10168. [PubMed] [Google Scholar]
  11. Hanover J. A., Elting J., Mintz G. R., Lennarz W. J. Temporal aspects of the N- and O-glycosylation of human chorionic gonadotropin. J Biol Chem. 1982 Sep 10;257(17):10172–10177. [PubMed] [Google Scholar]
  12. Hughes R. C., Mills G. Analysis by lectin affinity chromatography of N-linked glycans of BHK cells and ricin-resistant mutants. Biochem J. 1983 Jun 1;211(3):575–587. doi: 10.1042/bj2110575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Johnson D. C., Spear P. G. O-linked oligosaccharides are acquired by herpes simplex virus glycoproteins in the Golgi apparatus. Cell. 1983 Mar;32(3):987–997. doi: 10.1016/0092-8674(83)90083-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
  15. Krusius T., Finne J., Rauvala H. The structural basis of the different affinities of two types of acidic N-glycosidic glycopeptides for concanavalin A--sepharose. FEBS Lett. 1976 Nov 15;72(1):117–120. doi: 10.1016/0014-5793(76)80911-8. [DOI] [PubMed] [Google Scholar]
  16. McGeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., McNab D., Perry L. J., Scott J. E., Taylor P. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol. 1988 Jul;69(Pt 7):1531–1574. doi: 10.1099/0022-1317-69-7-1531. [DOI] [PubMed] [Google Scholar]
  17. Patzelt C., Weber B. Early O-glycosidic glycosylation of proglucagon in pancreatic islets: an unusual type of prohormonal modification. EMBO J. 1986 Sep;5(9):2103–2108. doi: 10.1002/j.1460-2075.1986.tb04472.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Roth J. Cytochemical localization of terminal N-acetyl-D-galactosamine residues in cellular compartments of intestinal goblet cells: implications for the topology of O-glycosylation. J Cell Biol. 1984 Feb;98(2):399–406. doi: 10.1083/jcb.98.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Serafini-Cessi F., Dall'Olio F., Pereira L., Campadelli-Fiume G. Processing of N-linked oligosaccharides from precursor- to mature-form herpes simplex virus type 1 glycoprotein gC. J Virol. 1984 Sep;51(3):838–844. doi: 10.1128/jvi.51.3.838-844.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Serafini-Cessi F., Dall'Olio F., Scannavini M., Costanzo F., Campadelli-Fiume G. N-acetylgalactosaminyltransferase activity involved in O-glycosylation of herpes simplex virus type 1 glycoproteins. J Virol. 1983 Oct;48(1):325–329. doi: 10.1128/jvi.48.1.325-329.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Serafini-Cessi F., Malagolini N., Dall'Olio F., Pereira L., Campadelli-Fiume G. Oligosaccharide chains of herpes simplex virus type 2 glycoprotein gG.2. Arch Biochem Biophys. 1985 Aug 1;240(2):866–876. doi: 10.1016/0003-9861(85)90097-9. [DOI] [PubMed] [Google Scholar]
  22. Spear P. G. Membrane proteins specified by herpes simplex viruses. I. Identification of four glycoprotein precursors and their products in type 1-infected cells. J Virol. 1976 Mar;17(3):991–1008. doi: 10.1128/jvi.17.3.991-1008.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Spielman J., Rockley N. L., Carraway K. L. Temporal aspects of O-glycosylation and cell surface expression of ascites sialoglycoprotein-1, the major cell surface sialomucin of 13762 mammary ascites tumor cells. J Biol Chem. 1987 Jan 5;262(1):269–275. [PubMed] [Google Scholar]
  24. Strous G. J. Initial glycosylation of proteins with acetylgalactosaminylserine linkages. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2694–2698. doi: 10.1073/pnas.76.6.2694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tooze S. A., Tooze J., Warren G. Site of addition of N-acetyl-galactosamine to the E1 glycoprotein of mouse hepatitis virus-A59. J Cell Biol. 1988 May;106(5):1475–1487. doi: 10.1083/jcb.106.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES