Abstract
Envelope glycoproteins of varicella zoster virus (VZV) contain mannose 6-phosphate (Man6P) residues. We now report that Man6P competitively and selectively inhibits infection of cells in vitro by cell-free VZV; furthermore, dephosphorylation of VZV by exposure to alkaline phosphatase rapidly destroys infectivity. Cells are also protected from VZV in a concentration-dependent manner by heparin (ED50 = 0.23 micrograms/ml; 95% confidence limits = 0.16-0.26 microgram/ml) but not by chondroitin sulfate. Both heparin and Man6P are protective only when present about the time of inoculation. Heparin but not Man6P interferes with the attachment of VZV to cell surfaces; moreover, VZV binds to heparin-affinity columns. These data are compatible with a working hypothesis, whereby VZV attaches to cell surfaces by binding to a heparin sulfate proteoglycan. This binding stabilizes VZV, making possible a low-affinity interaction with another Man6P-dependent receptor, which is necessary for viral entry.
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- Baba M., Snoeck R., Pauwels R., de Clercq E. Sulfated polysaccharides are potent and selective inhibitors of various enveloped viruses, including herpes simplex virus, cytomegalovirus, vesicular stomatitis virus, and human immunodeficiency virus. Antimicrob Agents Chemother. 1988 Nov;32(11):1742–1745. doi: 10.1128/aac.32.11.1742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bezouska K., Yuen C. T., O'Brien J., Childs R. A., Chai W., Lawson A. M., Drbal K., Fiserová A., Pospísil M., Feizi T. Oligosaccharide ligands for NKR-P1 protein activate NK cells and cytotoxicity. Nature. 1994 Nov 10;372(6502):150–157. doi: 10.1038/372150a0. [DOI] [PubMed] [Google Scholar]
- Brunetti C. R., Burke R. L., Kornfeld S., Gregory W., Masiarz F. R., Dingwell K. S., Johnson D. C. Herpes simplex virus glycoprotein D acquires mannose 6-phosphate residues and binds to mannose 6-phosphate receptors. J Biol Chem. 1994 Jun 24;269(25):17067–17074. [PubMed] [Google Scholar]
- Esko J. D. Genetic analysis of proteoglycan structure, function and metabolism. Curr Opin Cell Biol. 1991 Oct;3(5):805–816. doi: 10.1016/0955-0674(91)90054-3. [DOI] [PubMed] [Google Scholar]
- Esko J. D., Stewart T. E., Taylor W. H. Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci U S A. 1985 May;82(10):3197–3201. doi: 10.1073/pnas.82.10.3197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Forbes J. T., Bretthauer R. K., Oeltmann T. N. Mannose 6-, fructose 1-, and fructose 6-phosphates inhibit human natural cell-mediated cytotoxicity. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5797–5801. doi: 10.1073/pnas.78.9.5797. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuller A. O., Spear P. G. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5454–5458. doi: 10.1073/pnas.84.15.5454. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gabel C. A., Dubey L., Steinberg S. P., Sherman D., Gershon M. D., Gershon A. A. Varicella-zoster virus glycoprotein oligosaccharides are phosphorylated during posttranslational maturation. J Virol. 1989 Oct;63(10):4264–4276. doi: 10.1128/jvi.63.10.4264-4276.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gabel C. A., Foster S. A. Mannose 6-phosphate receptor-mediated endocytosis of acid hydrolases: internalization of beta-glucuronidase is accompanied by a limited dephosphorylation. J Cell Biol. 1986 Nov;103(5):1817–1827. doi: 10.1083/jcb.103.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gershon A. A., Sherman D. L., Zhu Z., Gabel C. A., Ambron R. T., Gershon M. D. Intracellular transport of newly synthesized varicella-zoster virus: final envelopment in the trans-Golgi network. J Virol. 1994 Oct;68(10):6372–6390. doi: 10.1128/jvi.68.10.6372-6390.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haubeck H. D., Kölsch E., Imort M., Hasilik A., von Figura K. Natural killer cell-mediated cytotoxicity does not depend on recognition of mannose 6-phosphate residues. J Immunol. 1985 Jan;134(1):65–69. [PubMed] [Google Scholar]
- Herold B. C., WuDunn D., Soltys N., Spear P. G. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J Virol. 1991 Mar;65(3):1090–1098. doi: 10.1128/jvi.65.3.1090-1098.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ito M., Baba M., Sato A., Pauwels R., De Clercq E., Shigeta S. Inhibitory effect of dextran sulfate and heparin on the replication of human immunodeficiency virus (HIV) in vitro. Antiviral Res. 1987 Jul;7(6):361–367. doi: 10.1016/0166-3542(87)90018-0. [DOI] [PubMed] [Google Scholar]
- Johnson D. C., Burke R. L., Gregory T. Soluble forms of herpes simplex virus glycoprotein D bind to a limited number of cell surface receptors and inhibit virus entry into cells. J Virol. 1990 Jun;64(6):2569–2576. doi: 10.1128/jvi.64.6.2569-2576.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson K. F., Kornfeld S. A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J Biol Chem. 1992 Aug 25;267(24):17110–17115. [PubMed] [Google Scholar]
- Kari B., Gehrz R. A human cytomegalovirus glycoprotein complex designated gC-II is a major heparin-binding component of the envelope. J Virol. 1992 Mar;66(3):1761–1764. doi: 10.1128/jvi.66.3.1761-1764.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mettenleiter T. C., Zsak L., Zuckermann F., Sugg N., Kern H., Ben-Porat T. Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J Virol. 1990 Jan;64(1):278–286. doi: 10.1128/jvi.64.1.278-286.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitsuya H., Looney D. J., Kuno S., Ueno R., Wong-Staal F., Broder S. Dextran sulfate suppression of viruses in the HIV family: inhibition of virion binding to CD4+ cells. Science. 1988 Apr 29;240(4852):646–649. doi: 10.1126/science.2452480. [DOI] [PubMed] [Google Scholar]
- Neyts J., Snoeck R., Schols D., Balzarini J., Esko J. D., Van Schepdael A., De Clercq E. Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology. 1992 Jul;189(1):48–58. doi: 10.1016/0042-6822(92)90680-n. [DOI] [PubMed] [Google Scholar]
- Shieh M. T., WuDunn D., Montgomery R. I., Esko J. D., Spear P. G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol. 1992 Mar;116(5):1273–1281. doi: 10.1083/jcb.116.5.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ueno R., Kuno S. Dextran sulphate, a potent anti-HIV agent in vitro having synergism with zidovudine. Lancet. 1987 Jun 13;1(8546):1379–1379. doi: 10.1016/s0140-6736(87)90681-7. [DOI] [PubMed] [Google Scholar]
- Vahlne A., Svennerholm B., Lycke E. Evidence for herpes simplex virus type-selective receptors on cellular plasma membranes. J Gen Virol. 1979 Jul;44(1):217–225. doi: 10.1099/0022-1317-44-1-217. [DOI] [PubMed] [Google Scholar]
- Weller T. H. Varicella and herpes zoster. Changing concepts of the natural history, control, and importance of a not-so-benign virus. N Engl J Med. 1983 Dec 8;309(23):1434–1440. doi: 10.1056/NEJM198312083092306. [DOI] [PubMed] [Google Scholar]
- Wickham T. J., Mathias P., Cheresh D. A., Nemerow G. R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell. 1993 Apr 23;73(2):309–319. doi: 10.1016/0092-8674(93)90231-e. [DOI] [PubMed] [Google Scholar]
- Yayon A., Klagsbrun M., Esko J. D., Leder P., Ornitz D. M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 1991 Feb 22;64(4):841–848. doi: 10.1016/0092-8674(91)90512-w. [DOI] [PubMed] [Google Scholar]