Herpes Simplex Virus Type 1 UL34 Gene Product Is Required for Viral Envelopment

doi:10.1128/JVI.74.1.117-129.2000

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Roller, R. J.
	Articles by DeSalvo, D.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Roller, R. J.
	Articles by DeSalvo, D.

Previous Article | Next Article

Journal of Virology, January 2000, p. 117-129, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Herpes Simplex Virus Type 1 U_L34 Gene Product Is Required for Viral Envelopment

Richard J. Roller,¹^,^* Yuping Zhou,¹ Renee Schnetzer,¹ John Ferguson,² and Diana DeSalvo¹

Department of Microbiology, University of Iowa, Iowa City, Iowa 52242,¹ and Department of Microbiology, Columbia University, New York, New York 10032²

Received 14 July 1999/Accepted 17 September 1999

The herpes simplex virus type 1 U_L34 gene encodes a protein that is conserved in all human herpesviruses. The associationof the U_L34 protein with membranes in the infected cell and itsexpression as a gamma-1 gene suggest a role in maturation or egressof the virus particle from the cell. To determine the functionof this gene product, we have constructed a recombinant virusthat fails to express the U_L34 protein. This recombinant virus,in which the U_L34 protein coding sequence has been replaced bygreen fluorescent protein, forms minute plaques and replicatesin single-step growth experiments to titers 3 to 5 log ordersof magnitude lower than wild-type or repair viruses. On Vero cells,the deletion virus synthesizes proteins of all kinetic classesin normal amounts. Electron microscopic and biochemical analysesshow that morphogenesis of the deletion virus proceeds normallyto the point of formation of DNA-containing nuclear capsids, butelectron micrographs show no enveloped virus particles in thecytoplasm or at the surface of infected cells, suggesting thatthe U_L34 protein is essential for efficient envelopment ofcapsids.

^* Corresponding author. Mailing address: Department of Microbiology, The University of Iowa, 3-752 Bowen Science Building, IowaCity, IA 52242. Phone: (319) 335-9958. Fax: (319) 335-9006. E-mail:richard-rolle{at}uiowa.edu.

Journal of Virology, January 2000, p. 117-129, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

Loret, S., Guay, G., Lippe, R. (2008). Comprehensive Characterization of Extracellular Herpes Simplex Virus Type 1 Virions. J. Virol. 82: 8605-8618 [Abstract] [Full Text]
Mou, F., Wills, E. G., Park, R., Baines, J. D. (2008). Effects of Lamin A/C, Lamin B1, and Viral US3 Kinase Activity on Viral Infectivity, Virion Egress, and the Targeting of Herpes Simplex Virus UL34-Encoded Protein to the Inner Nuclear Membrane. J. Virol. 82: 8094-8104 [Abstract] [Full Text]
Shanda, S. K., Wilson, D. W. (2008). UL36p Is Required for Efficient Transport of Membrane-Associated Herpes Simplex Virus Type 1 along Microtubules. J. Virol. 82: 7388-7394 [Abstract] [Full Text]
Kato, A., Tanaka, M., Yamamoto, M., Asai, R., Sata, T., Nishiyama, Y., Kawaguchi, Y. (2008). Identification of a Physiological Phosphorylation Site of the Herpes Simplex Virus 1-Encoded Protein Kinase Us3 Which Regulates Its Optimal Catalytic Activity In Vitro and Influences Its Function in Infected Cells. J. Virol. 82: 6172-6189 [Abstract] [Full Text]
Kuhn, J., Leege, T., Klupp, B. G., Granzow, H., Fuchs, W., Mettenleiter, T. C. (2008). Partial Functional Complementation of a Pseudorabies Virus UL25 Deletion Mutant by Herpes Simplex Virus Type 1 pUL25 Indicates Overlapping Functions of Alphaherpesvirus pUL25 Proteins. J. Virol. 82: 5725-5734 [Abstract] [Full Text]
Granato, M., Feederle, R., Farina, A., Gonnella, R., Santarelli, R., Hub, B., Faggioni, A., Delecluse, H.-J. (2008). Deletion of Epstein-Barr Virus BFLF2 Leads to Impaired Viral DNA Packaging and Primary Egress as Well as to the Production of Defective Viral Particles. J. Virol. 82: 4042-4051 [Abstract] [Full Text]
Nagel, C.-H., Dohner, K., Fathollahy, M., Strive, T., Borst, E. M., Messerle, M., Sodeik, B. (2008). Nuclear Egress and Envelopment of Herpes Simplex Virus Capsids Analyzed with Dual-Color Fluorescence HSV1(17+). J. Virol. 82: 3109-3124 [Abstract] [Full Text]
Camozzi, D., Pignatelli, S., Valvo, C., Lattanzi, G., Capanni, C., Dal Monte, P., Landini, M. P. (2008). Remodelling of the nuclear lamina during human cytomegalovirus infection: role of the viral proteins pUL50 and pUL53. J. Gen. Virol. 89: 731-740 [Abstract] [Full Text]
Coller, K. E., Lee, J. I-H., Ueda, A., Smith, G. A. (2007). The Capsid and Tegument of the Alphaherpesviruses Are Linked by an Interaction between the UL25 and VP1/2 Proteins. J. Virol. 81: 11790-11797 [Abstract] [Full Text]
Milbradt, J., Auerochs, S., Marschall, M. (2007). Cytomegaloviral proteins pUL50 and pUL53 are associated with the nuclear lamina and interact with cellular protein kinase C. J. Gen. Virol. 88: 2642-2650 [Abstract] [Full Text]
Leach, N., Bjerke, S. L., Christensen, D. K., Bouchard, J. M., Mou, F., Park, R., Baines, J., Haraguchi, T., Roller, R. J. (2007). Emerin Is Hyperphosphorylated and Redistributed in Herpes Simplex Virus Type 1-Infected Cells in a Manner Dependent on both UL34 and US3. J. Virol. 81: 10792-10803 [Abstract] [Full Text]
Fang, M., Dai, X., Theilmann, D. A. (2007). Autographa californica Multiple Nucleopolyhedrovirus EXON0 (ORF141) Is Required for Efficient Egress of Nucleocapsids from the Nucleus. J. Virol. 81: 9859-9869 [Abstract] [Full Text]
Mou, F., Forest, T., Baines, J. D. (2007). US3 of Herpes Simplex Virus Type 1 Encodes a Promiscuous Protein Kinase That Phosphorylates and Alters Localization of Lamin A/C in Infected Cells. J. Virol. 81: 6459-6470 [Abstract] [Full Text]
Klupp, B. G., Granzow, H., Fuchs, W., Keil, G. M., Finke, S., Mettenleiter, T. C. (2007). Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc. Natl. Acad. Sci. USA 104: 7241-7246 [Abstract] [Full Text]
Baines, J. D., Hsieh, C.-E., Wills, E., Mannella, C., Marko, M. (2007). Electron Tomography of Nascent Herpes Simplex Virus Virions. J. Virol. 81: 2726-2735 [Abstract] [Full Text]
Remillard-Labrosse, G., Guay, G., Lippe, R. (2006). Reconstitution of Herpes Simplex Virus Type 1 Nuclear Capsid Egress In Vitro. J. Virol. 80: 9741-9753 [Abstract] [Full Text]
Kato, A., Yamamoto, M., Ohno, T., Tanaka, M., Sata, T., Nishiyama, Y., Kawaguchi, Y. (2006). Herpes Simplex Virus 1-Encoded Protein Kinase UL13 Phosphorylates Viral Us3 Protein Kinase and Regulates Nuclear Localization of Viral Envelopment Factors UL34 and UL31. J. Virol. 80: 1476-1486 [Abstract] [Full Text]
Lotzerich, M., Ruzsics, Z., Koszinowski, U. H. (2006). Functional Domains of Murine Cytomegalovirus Nuclear Egress Protein M53/p38. J. Virol. 80: 73-84 [Abstract] [Full Text]
Park, R., Baines, J. D. (2006). Herpes Simplex Virus Type 1 Infection Induces Activation and Recruitment of Protein Kinase C to the Nuclear Membrane and Increased Phosphorylation of Lamin B. J. Virol. 80: 494-504 [Abstract] [Full Text]
Simpson-Holley, M., Colgrove, R. C., Nalepa, G., Harper, J. W., Knipe, D. M. (2005). Identification and Functional Evaluation of Cellular and Viral Factors Involved in the Alteration of Nuclear Architecture during Herpes Simplex Virus 1 Infection. J. Virol. 79: 12840-12851 [Abstract] [Full Text]
Leuzinger, H., Ziegler, U., Schraner, E. M., Fraefel, C., Glauser, D. L., Heid, I., Ackermann, M., Mueller, M., Wild, P. (2005). Herpes Simplex Virus 1 Envelopment Follows Two Diverse Pathways. J. Virol. 79: 13047-13059 [Abstract] [Full Text]
Farina, A., Feederle, R., Raffa, S., Gonnella, R., Santarelli, R., Frati, L., Angeloni, A., Torrisi, M. R., Faggioni, A., Delecluse, H.-J. (2005). BFRF1 of Epstein-Barr Virus Is Essential for Efficient Primary Viral Envelopment and Egress. J. Virol. 79: 3703-3712 [Abstract] [Full Text]
Gonnella, R., Farina, A., Santarelli, R., Raffa, S., Feederle, R., Bei, R., Granato, M., Modesti, A., Frati, L., Delecluse, H.-J., Torrisi, M. R., Angeloni, A., Faggioni, A. (2005). Characterization and Intracellular Localization of the Epstein-Barr Virus Protein BFLF2: Interactions with BFRF1 and with the Nuclear Lamina. J. Virol. 79: 3713-3727 [Abstract] [Full Text]
Liang, L., Baines, J. D. (2005). Identification of an Essential Domain in the Herpes Simplex Virus 1 UL34 Protein That Is Necessary and Sufficient To Interact with UL31 Protein. J. Virol. 79: 3797-3806 [Abstract] [Full Text]
Wild, P., Engels, M., Senn, C., Tobler, K., Ziegler, U., Schraner, E. M., Loepfe, E., Ackermann, M., Mueller, M., Walther, P. (2005). Impairment of Nuclear Pores in Bovine Herpesvirus 1-Infected MDBK Cells. J. Virol. 79: 1071-1083 [Abstract] [Full Text]
Rupp, B., Ruzsics, Z., Sacher, T., Koszinowski, U. H. (2005). Conditional Cytomegalovirus Replication In Vitro and In Vivo. J. Virol. 79: 486-494 [Abstract] [Full Text]
Bubeck, A., Wagner, M., Ruzsics, Z., Lotzerich, M., Iglesias, M., Singh, I. R., Koszinowski, U. H. (2004). Comprehensive Mutational Analysis of a Herpesvirus Gene in the Viral Genome Context Reveals a Region Essential for Virus Replication. J. Virol. 78: 8026-8035 [Abstract] [Full Text]
Douglas, M. W., Diefenbach, R. J., Homa, F. L., Miranda-Saksena, M., Rixon, F. J., Vittone, V., Byth, K., Cunningham, A. L. (2004). Herpes Simplex Virus Type 1 Capsid Protein VP26 Interacts with Dynein Light Chains RP3 and Tctex1 and Plays a Role in Retrograde Cellular Transport. J. Biol. Chem. 279: 28522-28530 [Abstract] [Full Text]
Reynolds, A. E., Liang, L., Baines, J. D. (2004). Conformational Changes in the Nuclear Lamina Induced by Herpes Simplex Virus Type 1 Require Genes UL31 and UL34. J. Virol. 78: 5564-5575 [Abstract] [Full Text]
Simpson-Holley, M., Baines, J., Roller, R., Knipe, D. M. (2004). Herpes Simplex Virus 1 UL31 and UL34 Gene Products Promote the Late Maturation of Viral Replication Compartments to the Nuclear Periphery. J. Virol. 78: 5591-5600 [Abstract] [Full Text]
Kopp, M., Granzow, H., Fuchs, W., Klupp, B., Mettenleiter, T. C. (2004). Simultaneous Deletion of Pseudorabies Virus Tegument Protein UL11 and Glycoprotein M Severely Impairs Secondary Envelopment. J. Virol. 78: 3024-3034 [Abstract] [Full Text]
Granzow, H., Klupp, B. G., Mettenleiter, T. C. (2004). The Pseudorabies Virus US3 Protein Is a Component of Primary and of Mature Virions. J. Virol. 78: 1314-1323 [Abstract] [Full Text]
Ryckman, B. J., Roller, R. J. (2004). Herpes Simplex Virus Type 1 Primary Envelopment: UL34 Protein Modification and the US3-UL34 Catalytic Relationship. J. Virol. 78: 399-412 [Abstract] [Full Text]
Klupp, B. G., Granzow, H., Fuchs, W., Mundt, E., Mettenleiter, T. C. (2004). Pseudorabies Virus UL3 Gene Codes for a Nuclear Protein Which Is Dispensable for Viral Replication. J. Virol. 78: 464-472 [Abstract] [Full Text]
Bjerke, S. L., Cowan, J. M., Kerr, J. K., Reynolds, A. E., Baines, J. D., Roller, R. J. (2003). Effects of Charged Cluster Mutations on the Function of Herpes Simplex Virus Type 1 UL34 Protein. J. Virol. 77: 7601-7610 [Abstract] [Full Text]
Krosky, P. M., Baek, M.-C., Coen, D. M. (2002). The Human Cytomegalovirus UL97 Protein Kinase, an Antiviral Drug Target, Is Required at the Stage of Nuclear Egress. J. Virol. 77: 905-914 [Abstract] [Full Text]
Muranyi, W., Haas, J., Wagner, M., Krohne, G., Koszinowski, U. H. (2002). Cytomegalovirus Recruitment of Cellular Kinases to Dissolve the Nuclear Lamina. Science 297: 854-857 [Abstract] [Full Text]
Reynolds, A. E., Wills, E. G., Roller, R. J., Ryckman, B. J., Baines, J. D. (2002). Ultrastructural Localization of the Herpes Simplex Virus Type 1 UL31, UL34, and US3 Proteins Suggests Specific Roles in Primary Envelopment and Egress of Nucleocapsids. J. Virol. 76: 8939-8952 [Abstract] [Full Text]
Koshizuka, T., Goshima, F., Takakuwa, H., Nozawa, N., Daikoku, T., Koiwai, O., Nishiyama, Y. (2002). Identification and Characterization of the UL56 Gene Product of Herpes Simplex Virus Type 2. J. Virol. 76: 6718-6728 [Abstract] [Full Text]
Dal Monte, P., Pignatelli, S., Zini, N., Maraldi, N. M., Perret, E., Prevost, M. C., Landini, M. P. (2002). Analysis of intracellular and intraviral localization of the human cytomegalovirus UL53 protein. J. Gen. Virol. 83: 1005-1012 [Abstract] [Full Text]
Klupp, B. G., Fuchs, W., Granzow, H., Nixdorf, R., Mettenleiter, T. C. (2002). Pseudorabies Virus UL36 Tegument Protein Physically Interacts with the UL37 Protein. J. Virol. 76: 3065-3071 [Abstract] [Full Text]
Mettenleiter, T. C. (2002). Herpesvirus Assembly and Egress. J. Virol. 76: 1537-1547 [Full Text]
Fuchs, W., Klupp, B. G., Granzow, H., Osterrieder, N., Mettenleiter, T. C. (2002). The Interacting UL31 and UL34 Gene Products of Pseudorabies Virus Are Involved in Egress from the Host-Cell Nucleus and Represent Components of Primary Enveloped but Not Mature Virions. J. Virol. 76: 364-378 [Abstract] [Full Text]
Demmin, G. L., Clase, A. C., Randall, J. A., Enquist, L. W., Banfield, B. W. (2001). Insertions in the gG Gene of Pseudorabies Virus Reduce Expression of the Upstream Us3 Protein and Inhibit Cell-to-Cell Spread of Virus Infection. J. Virol. 75: 10856-10869 [Abstract] [Full Text]
Desai, P., Sexton, G. L., McCaffery, J. M., Person, S. (2001). A Null Mutation in the Gene Encoding the Herpes Simplex Virus Type 1 UL37 Polypeptide Abrogates Virus Maturation. J. Virol. 75: 10259-10271 [Abstract] [Full Text]
Klupp, B. G., Granzow, H., Mundt, E., Mettenleiter, T. C. (2001). Pseudorabies Virus UL37 Gene Product Is Involved in Secondary Envelopment. J. Virol. 75: 8927-8936 [Abstract] [Full Text]
Klupp, B. G., Granzow, H., Mettenleiter, T. C. (2001). Effect of the pseudorabies virus US3 protein on nuclear membrane localization of the UL34 protein and virus egress from the nucleus. J. Gen. Virol. 82: 2363-2371 [Abstract] [Full Text]
Reynolds, A. E., Ryckman, B. J., Baines, J. D., Zhou, Y., Liang, L., Roller, R. J. (2001). UL31 and UL34 Proteins of Herpes Simplex Virus Type 1 Form a Complex That Accumulates at the Nuclear Rim and Is Required for Envelopment of Nucleocapsids. J. Virol. 75: 8803-8817 [Abstract] [Full Text]
Scott, E. S., O'Hare, P. (2001). Fate of the Inner Nuclear Membrane Protein Lamin B Receptor and Nuclear Lamins in Herpes Simplex Virus Type 1 Infection. J. Virol. 75: 8818-8830 [Abstract] [Full Text]
Yamauchi, Y., Shiba, C., Goshima, F., Nawa, A., Murata, T., Nishiyama, Y. (2001). Herpes simplex virus type 2 UL34 protein requires UL31 protein for its relocation to the internal nuclear membrane in transfected cells. J. Gen. Virol. 82: 1423-1428 [Abstract] [Full Text]
Lake, C. M., Hutt-Fletcher, L. M. (2000). Epstein-Barr Virus That Lacks Glycoprotein gN Is Impaired in Assembly and Infection. J. Virol. 74: 11162-11172 [Abstract] [Full Text]
Klupp, B. G., Granzow, H., Mettenleiter, T. C. (2000). Primary Envelopment of Pseudorabies Virus at the Nuclear Membrane Requires the UL34 Gene Product. J. Virol. 74: 10063-10073 [Abstract] [Full Text]
Shiba, C., Daikoku, T., Goshima, F., Takakuwa, H., Yamauchi, Y., Koiwai, O., Nishiyama, Y. (2000). The UL34 gene product of herpes simplex virus type 2 is a tail-anchored type II membrane protein that is significant for virus envelopment. J. Gen. Virol. 81: 2397-2405 [Abstract] [Full Text]
Ye, G.-J., Roizman, B. (2000). The essential protein encoded by the UL31 gene of herpes simplex virus 1 depends for its stability on the presence of UL34 protein. Proc. Natl. Acad. Sci. USA 97: 11002-11007 [Abstract] [Full Text]
Farina, A., Santarelli, R., Gonnella, R., Bei, R., Muraro, R., Cardinali, G., Uccini, S., Ragona, G., Frati, L., Faggioni, A., Angeloni, A. (2000). The BFRF1 Gene of Epstein-Barr Virus Encodes a Novel Protein. J. Virol. 74: 3235-3244 [Abstract] [Full Text]
Ye, G.-J., Vaughan, K. T., Vallee, R. B., Roizman, B. (2000). The Herpes Simplex Virus 1 UL34 Protein Interacts with a Cytoplasmic Dynein Intermediate Chain and Targets Nuclear Membrane. J. Virol. 74: 1355-1363 [Abstract] [Full Text]

J. Bacteriol.	Mol. Cell. Biol.	Microbiol. Mol. Biol. Rev.

Clin. Vaccine Immunol.	ALL ASM JOURNALS