DOI: 10.1128/jvi.72.4.3330-3339.1998. Herpes Simplex Virus gD and Virions Accumulate in Endosomes by Mannose 6-Phosphate-Dependent and -Independent Mechanisms

Herpes Simplex Virus gD and Virions Accumulate in Endosomes by Mannose 6-Phosphate-Dependent and -Independent Mechanisms

10.1128/jvi.72.4.3330-3339.1998

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACT Herpes simplex virus (HSV) glycoprotein D (gD) is modified with mannose 6-phosphate (M6P) and binds to M6P receptors (MPRs). MPRs are involved in the well-characterized pathway by which lysosomal enzymes are directed to lysosomes via a network of endosomal membranes. Based on the impaired ability of HSV to form plaques under conditions in which glycoproteins could not interact with MPRs, we proposed that MPRs may function during HSV egress or cell-to-cell spread (C. R. Brunetti, R. L. Burke, B. Hoflack, T. Ludwig, K. S. Dingwell, and D. C. Johnson, J. Virol. 69:3517–3528, 1995). To further analyze M6P modification and intracellular trafficking of gD in the absence of other HSV proteins, adenovirus (Ad) vectors were used to express soluble and membrane-anchored forms of gD. Both membrane-bound and soluble gD were modified with M6P residues and were localized to endosomes that contained the 275-kDa MPR or the transferrin receptor. Similar results were observed in HSV-infected cells. Cell fractionation experiments showed that gD was not present in lysosomes. However, a mutant form of gD and another HSV glycoprotein, gI, that were not modified with M6P were also found in endosomes in HSV-infected cells. Moreover, a substantial fraction of the HSV nucleocapsid protein VP6 was found in endosomes, consistent with accumulation of virions in an endosomal compartment. Therefore, it appears that HSV glycoproteins and virions are directed to endosomes, by M6P-dependent as well as by M6P-independent mechanisms, either as part of the virus egress pathway or by endocytosis from the cell surface.

Bibliography

Brunetti, C. R., Dingwell, K. S., Wale, C., Graham, F. L., & Johnson, D. C. (1998). Herpes Simplex Virus gD and Virions Accumulate in Endosomes by Mannose 6-Phosphate-Dependent and -Independent Mechanisms. Journal of Virology, 72(4), 3330â3339.

Authors 5

Craig R. Brunetti (first)
Kevin S. Dingwell (additional)
Cathy Wale (additional)
Frank L. Graham (additional)
David C. Johnson (additional)

References 76 Referenced 42

10.1016/0042-6822(84)90349-0
10.1002/j.1460-2075.1996.tb00998.x
10.1006/viro.1995.1184
10.1016/S0021-9258(18)54505-1
10.1073/pnas.91.19.8802
10.1128/jvi.70.7.4311-4316.1996
Brunetti C. R. Unpublished data.
10.1128/jvi.69.6.3517-3528.1995
10.1016/S0021-9258(17)32521-8
Brunetti C. R. S. Kornfeld and D. C. Johnson. Unpublished data.
10.1128/jvi.62.1.159-167.1988
10.1073/pnas.90.7.2798
10.1128/jvi.65.3.1589-1595.1991
10.1016/S0021-9258(18)50099-5
10.1128/jvi.34.2.521-531.1980
10.1016/S0022-5320(70)80014-4
Darlington R. W. Moss L. H. The envelope of herpesvirus.Prog. Med. Virol. 11 1969 16 45 / Prog. Med. Virol. / The envelope of herpesvirus by Darlington R. W. (1969)
10.1007/BF01323238
Dingwell K. S. Unpublished data.
10.1128/jvi.68.2.834-845.1994
10.1128/jvi.66.8.5002-5012.1992
10.1128/jvi.63.10.4264-4276.1989
10.1099/0022-1317-18-1-21
10.1128/jvi.68.10.6372-6390.1994
10.1083/jcb.123.1.99
10.1099/0022-1317-36-1-59
10.1083/jcb.105.3.1227
10.1016/S0092-8674(88)80026-6
10.1016/0955-0674(95)80013-1
10.1038/375411a0
10.1016/S1067-2389(06)80034-8
10.1083/jcb.97.2.508
10.1073/pnas.93.5.1836
10.1002/bies.950180508
10.1128/jvi.69.9.5401-5413.1995
10.1128/jvi.63.5.2325-2334.1989
10.1128/jvi.64.6.2569-2576.1990
10.1128/jvi.62.4.1347-1354.1988
10.1128/jvi.62.12.4605-4612.1988
10.1128/jvi.43.3.1102-1112.1982
10.1128/jvi.63.2.819-827.1989
10.1128/jvi.62.8.2701-2711.1988
10.1146/annurev.bi.61.070192.001515
Kornfeld S. Personal communication.
10.1089/dna.1.1984.3.23
10.1128/jvi.62.5.1486-1494.1988
10.1016/S0962-8924(96)10057-X
10.1016/S0092-8674(00)81363-X
10.1042/bst0240133
10.1146/annurev.bi.60.070191.001353
10.1006/jmbi.1993.1406
10.1128/jvi.71.5.4042-4054.1997
10.1006/viro.1995.1192
10.1016/0014-5793(94)00499-4
10.1002/ijc.2910150104
10.1016/S0962-8924(96)10048-9
10.1083/jcb.130.6.1297
10.1038/2061374a0
10.1016/0092-8674(88)90532-6
10.1016/0042-6822(69)90126-3
10.1083/jcb.132.4.577
10.1083/jcb.116.5.1273
10.1128/jvi.63.12.5184-5193.1989
10.1128/jvi.65.8.4432-4441.1991
Spear P. G. Membrane fusion induced by herpes simplex virus Viral fusion mechanisms. Bentz J. 1993 201 232 CRC Press Boca Raton Fla
10.1159/000149251
10.1073/pnas.72.10.4081
10.1016/0042-6822(67)90043-8
10.1128/jvi.69.6.3690-3703.1995
10.1073/pnas.89.23.11508
10.1006/viro.1994.1252
10.1126/science.6289440
10.1128/jvi.65.3.1066-1081.1991
10.1128/jvi.71.8.6083-6093.1997
10.1016/0092-8674(84)90414-8
10.1128/jvi.70.10.6563-6575.1996

Dates

Type	When
Created	5 years, 7 months ago (Dec. 31, 2019, 1:10 p.m.)
Deposited	3 years, 5 months ago (March 4, 2022, 9:53 p.m.)
Indexed	1 year, 6 months ago (Jan. 23, 2024, 4:24 p.m.)
Issued	27 years, 4 months ago (April 1, 1998)
Published	27 years, 4 months ago (April 1, 1998)
Published Print	27 years, 4 months ago (April 1, 1998)

Funders 0

None

BibTeX

@article{Brunetti_1998, title={Herpes Simplex Virus gD and Virions Accumulate in Endosomes by Mannose 6-Phosphate-Dependent and -Independent Mechanisms}, volume={72}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.72.4.3330-3339.1998}, DOI={10.1128/jvi.72.4.3330-3339.1998}, number={4}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Brunetti, Craig R. and Dingwell, Kevin S. and Wale, Cathy and Graham, Frank L. and Johnson, David C.}, year={1998}, month=apr, pages={3330–3339} }

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