Abstract
ABSTRACTEgress of four important alphaherpesviruses, equine herpesvirus 1 (EHV-1), herpes simplex virus type 1 (HSV-1), infectious laryngotracheitis virus (ILTV), and pseudorabies virus (PrV), was investigated by electron microscopy of infected cell lines of different origins. In all virus-cell systems analyzed, similar observations were made concerning the different stages of virion morphogenesis. After intranuclear assembly, nucleocapsids bud at the inner leaflet of the nuclear membrane, resulting in enveloped particles in the perinuclear space that contain a sharply bordered rim of tegument and a smooth envelope surface. Egress from the perinuclear cisterna primarily occurs by fusion of the primary envelope with the outer leaflet of the nuclear membrane, which has been visualized for HSV-1 and EHV-1 for the first time. The resulting intracytoplasmic naked nucleocapsids are enveloped at membranes of thetrans-Golgi network (TGN), as shown by immunogold labeling with a TGN-specific antiserum. Virions containing their final envelope differ in morphology from particles within the perinuclear cisterna by visible surface projections and a diffuse tegument. Particularly striking was the addition of a large amount of tegument material to ILTV capsids in the cytoplasm. Extracellular virions were morphologically identical to virions within Golgi-derived vesicles, but distinct from virions in the perinuclear space. Studies with gB- and gH-deleted PrV mutants indicated that these two glycoproteins, which are essential for virus entry and direct cell-to-cell spread, are dispensable for egress. Taken together, our studies indicate that the deenvelopment-reenvelopment process of herpesvirus maturation also occurs in EHV-1, HSV-1, and ILTV and that membrane fusion processes occurring during egress are substantially different from those during entry and direct viral cell-to-cell spread.
References
61
Referenced
226
10.1099/0022-1317-77-9-2277
10.1128/JVI.73.7.5364-5372.1999
10.1128/jvi.70.7.4311-4316.1996
10.1128/JVI.72.4.3330-3339.1998
10.1128/jvi.62.1.159-167.1988
10.1128/jvi.65.3.1589-1595.1991
10.1073/pnas.90.7.2798
10.1523/JNEUROSCI.13-06-02515.1993
10.1111/j.1365-2818.1982.tb00362.x
10.1128/jvi.2.1.48-55.1968
10.1006/viro.1995.0073
- Felluga B. Electron microscopic observations on pseudorabies virus development in a line of pig kidney cells.Ann. Sclavo 5 1963 412 424 / Ann. Sclavo / Electron microscopic observations on pseudorabies virus development in a line of pig kidney cells by Felluga B. (1963)
10.1099/0022-1317-81-3-627
10.1128/jvi.66.8.5002-5012.1992
10.1128/jvi.68.10.6372-6390.1994
10.1007/978-3-642-84850-6_16
10.1159/000150509
10.1128/jvi.64.4.1507-1516.1990
10.1128/jvi.71.3.2072-2082.1997
-
Guo P. Scholz E. Turek J. Nodgreen R. Maloney B. Assembly pathway of avian infectious laryngotracheitis virus.Am. J. Vet. Res. 54 1993 2031 2039
(
10.2460/ajvr.1993.54.12.2031
) / Am. J. Vet. Res. / Assembly pathway of avian infectious laryngotracheitis virus by Guo P. (1993) 10.1128/jvi.69.8.4994-5010.1995
10.3181/00379727-116-29392
10.1016/0042-6822(83)90122-8
10.1128/jvi.43.3.1102-1112.1982
10.1128/jvi.62.8.2701-2711.1988
10.1016/0042-6822(59)90068-6
- Kawaguchi T. Nomura K. Hirayama Y. Kitagawa T. Establishment and characterization of a chicken hepatocellular carcinoma cell line, LMH.Cancer Res. 47 1987 4460 4464 / Cancer Res. / Establishment and characterization of a chicken hepatocellular carcinoma cell line, LMH by Kawaguchi T. (1987)
10.1128/JVI.73.4.3014-3022.1999
10.1128/JVI.74.15.6760-6768.2000
10.1007/BF01242992
10.1007/BF00685200
10.1099/0022-1317-73-2-269
-
Mettenleiter T. C. Aujeszky's disease (pseudorabies) virus: the virus and molecular pathogenesis—state of the art, June 1999.Vet. Res. 31 2000 99 115
(
10.1051/vetres:2000110
) / Vet. Res. / Aujeszky's disease (pseudorabies) virus: the virus and molecular pathogenesis—state of the art, June 1999 by Mettenleiter T. C. (2000) 10.1093/oxfordjournals.jmicro.a023436
- Nii S. Electron microscopic study on the development of herpesviruses.J. Electron Microsc. 41 1992 414 423 / J. Electron Microsc. / Electron microscopic study on the development of herpesviruses by Nii S. (1992)
10.1128/jvi.2.5.517-536.1968
10.1128/JVI.74.15.7137-7145.2000
10.1006/viro.1996.0652
10.1128/jvi.66.2.894-905.1992
10.1128/jvi.66.6.3888-3892.1992
10.1177/35.6.3033063
-
Radsak K. Kern H. Reis B. Reschke M. Mockenhaupt T. Eickmann M. Human cytomegalovirus—aspects of viral morphogenesis and of processing and transport of viral glycoproteins DNA tumor viruses: oncogenic mechanisms. Barbanti-Brodano G. 1995 295 312 Plenum Press New York N.Y
(
10.1007/978-1-4899-1100-1_16
) 10.1007/BF01718317
10.1083/jcb.116.1.85
10.1099/0022-1317-73-2-277
10.1128/jvi.64.12.6308-6313.1990
- Roizman B. Sears A. E. Herpes simplex viruses and their replication Fields virology 3rd ed. Fields B. N. Knipe D. M. Howley P. M. 2 1996 2231 2295 Lippincott-Raven Publishers Philadelphia, Pa / Fields virology / Herpes simplex viruses and their replication by Roizman B. (1996)
10.1128/jvi.71.1.17-24.1997
10.1099/0022-1317-80-1-57
10.1083/jcb.136.5.1007
10.1006/smvy.1993.1012
- Spear P. G. Wittels M. Fuller A. O. WuDunn D. Johnson R. Herpes simplex virus: pathway of entry into cells Cell biology of viral entry replication and pathogenesis. Compans R. W. Helenius A. Oldstone M. B. A. 1988 163 175 Alan R. Liss New York N.Y
10.1099/0022-1317-72-3-661
10.1099/0022-1317-36-2-345
10.1016/S0923-2516(07)80008-2
10.1016/S0923-2516(07)80009-4
10.1128/jvi.66.1.554-561.1992
- van Regenmortel H. V. M. Fauquet C. M. Bishop D. H. L. Carstens E. Estes M. K. Lemon S. Maniloff J. Mayo M. A. McGeoch D. Pringle C. R. Wickner R. B. Virus taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses. 2000 Academic Press New York N.Y
10.1128/jvi.65.3.1066-1081.1991
10.1128/JVI.73.11.9515-9520.1999
10.1128/jvi.69.12.7951-7959.1995
Dates
Type | When |
---|---|
Created | 23 years ago (July 27, 2002, 5:55 a.m.) |
Deposited | 8 months, 1 week ago (Dec. 8, 2024, 2:42 p.m.) |
Indexed | 2 weeks, 3 days ago (Aug. 3, 2025, 7:01 p.m.) |
Issued | 24 years, 4 months ago (April 15, 2001) |
Published | 24 years, 4 months ago (April 15, 2001) |
Published Print | 24 years, 4 months ago (April 15, 2001) |
@article{Granzow_2001, title={Egress of Alphaherpesviruses: Comparative Ultrastructural Study}, volume={75}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.75.8.3675-3684.2001}, DOI={10.1128/jvi.75.8.3675-3684.2001}, number={8}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Granzow, Harald and Klupp, Barbara G. and Fuchs, Walter and Veits, Jutta and Osterrieder, Nikolaus and Mettenleiter, Thomas C.}, year={2001}, month=apr, pages={3675–3684} }