Previous Article | Next Article 
Journal of Virology, February 2000, p. 1355-1363, Vol. 74, No. 3
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
The Herpes Simplex Virus 1 UL34 Protein
Interacts with a Cytoplasmic Dynein Intermediate Chain and Targets
Nuclear Membrane
Guo-Jie
Ye,1
Kevin T.
Vaughan,2
Richard B.
Vallee,2 and
Bernard
Roizman1,*
The Marjorie B. Kovler Viral Oncology
Laboratories, The University of Chicago, Chicago, Illinois
60637,1 and The University of
Massachusetts Medical School, IV Biotech, Worcester, Massachusetts
016052
Received 16 September 1999/Accepted 4 November 1999
To express the function encoded in its genome, the herpes simplex
virus 1 capsid-tegument structure released by deenvelopment during
entry into cells must be transported retrograde to the nuclear pore
where viral DNA is released into the nucleus. This path is essential in
the case of virus entering axons of dorsal root ganglia. The objective
of the study was to identify the viral proteins that may be involved in
the transport. We report the following findings. (i) The neuronal
isoform of the intermediate chain (IC-1a) of the dynein complex pulled
down, from lysates of [35S]methionine-labeled infected
cells, two viral proteins identified as the products of
UL34 and UL31 open reading frames,
respectively. UL34 protein is a virion protein associated
with cellular membranes and phosphorylated by the viral kinase
US3. UL31 protein is a largely insoluble,
evenly dispersed nuclear phosphoprotein required for optimal processing
and packaging of viral DNA into preformed capsids. Reciprocal pulldown
experiments verified the interaction of IC-1a and UL34
protein. In similar experiments, UL34 protein was found to
interact with UL31 protein and the major capsid protein ICP5. (ii) To determine whether UL34 protein is transported
to the nuclear membrane, a requirement if it is involved in transport, the UL34 protein was inserted into a baculovirus vector
under the cytomegalovirus major early promoter. Cells infected with the
recombinant baculovirus expressed UL34 protein in a
dose-dependent manner, and the UL34 protein localized
primarily in the nuclear membrane. An unexpected finding was that
UL34-expressing cells showed a dissociation of the inner
and outer nuclear membranes reminiscent of the morphologic changes seen
in cells productively infected with herpes simplex virus 1. UL34, like many other viral proteins, may have multiple
functions expressed both early and late in infection.
*
Corresponding author. Mailing address: The Marjorie B. Kovler Viral Oncology Laboratories, The University of Chicago, 910 E. 58th St., Chicago, IL 60637. Phone: (773) 702-1898. Fax: (773) 702-1631. E-mail: bernard{at}cummings.uchicago.edu.
Journal of Virology, February 2000, p. 1355-1363, Vol. 74, No. 3
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Zhang, J., Nagel, C.-H., Sodeik, B., Lippe, R.
(2009). Early, Active, and Specific Localization of Herpes Simplex Virus Type 1 gM to Nuclear Membranes. J. Virol.
83: 12984-12997
[Abstract]
[Full Text]
-
Hall, J., Karplus, P. A., Barbar, E.
(2009). Multivalency in the Assembly of Intrinsically Disordered Dynein Intermediate Chain. J. Biol. Chem.
284: 33115-33121
[Abstract]
[Full Text]
-
Wills, E., Mou, F., Baines, J. D.
(2009). The UL31 and UL34 Gene Products of Herpes Simplex Virus 1 Are Required for Optimal Localization of Viral Glycoproteins D and M to the Inner Nuclear Membranes of Infected Cells. J. Virol.
83: 4800-4809
[Abstract]
[Full Text]
-
Krautwald, M., Fuchs, W., Klupp, B. G., Mettenleiter, T. C.
(2009). Translocation of Incoming Pseudorabies Virus Capsids to the Cell Nucleus Is Delayed in the Absence of Tegument Protein pUL37. J. Virol.
83: 3389-3396
[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]
-
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]
-
Antinone, S. E., Shubeita, G. T., Coller, K. E., Lee, J. I., Haverlock-Moyns, S., Gross, S. P., Smith, G. A.
(2006). The Herpesvirus Capsid Surface Protein, VP26, and the Majority of the Tegument Proteins Are Dispensable for Capsid Transport toward the Nucleus.. J. Virol.
80: 5494-5498
[Abstract]
[Full Text]
-
Lee, G. E., Murray, J. W., Wolkoff, A. W., Wilson, D. W.
(2006). Reconstitution of Herpes Simplex Virus Microtubule-Dependent Trafficking In Vitro. J. Virol.
80: 4264-4275
[Abstract]
[Full Text]
-
Luxton, G. W. G., Lee, J. I-H., Haverlock-Moyns, S., Schober, J. M., Smith, G. A.
(2006). The Pseudorabies Virus VP1/2 Tegument Protein Is Required for Intracellular Capsid Transport. J. Virol.
80: 201-209
[Abstract]
[Full Text]
-
Takemoto, M., Koike, M., Mori, Y., Yonemoto, S., Sasamoto, Y., Kondo, K., Uchiyama, Y., Yamanishi, K.
(2005). Human Herpesvirus 6 Open Reading Frame U14 Protein and Cellular p53 Interact with Each Other and Are Contained in the Virion. J. Virol.
79: 13037-13046
[Abstract]
[Full Text]
-
Poon, A. P. W., Roizman, B.
(2005). Herpes Simplex Virus 1 ICP22 Regulates the Accumulation of a Shorter mRNA and of a Truncated US3 Protein Kinase That Exhibits Altered Functions. J. Virol.
79: 8470-8479
[Abstract]
[Full Text]
-
Luxton, G. W. G., Haverlock, S., Coller, K. E., Antinone, S. E., Pincetic, A., Smith, G. A.
(2005). From the Cover: Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. USA
102: 5832-5837
[Abstract]
[Full Text]
-
Bechtel, J. T., Winant, R. C., Ganem, D.
(2005). Host and Viral Proteins in the Virion of Kaposi's Sarcoma-Associated Herpesvirus. J. Virol.
79: 4952-4964
[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]
-
Naranatt, P. P., Krishnan, H. H., Smith, M. S., Chandran, B.
(2005). Kaposi's Sarcoma-Associated Herpesvirus Modulates Microtubule Dynamics via RhoA-GTP-Diaphanous 2 Signaling and Utilizes the Dynein Motors To Deliver Its DNA to the Nucleus. J. Virol.
79: 1191-1206
[Abstract]
[Full Text]
-
Smith, G. A., Pomeranz, L., Gross, S. P., Enquist, L. W.
(2004). Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc. Natl. Acad. Sci. USA
101: 16034-16039
[Abstract]
[Full Text]
-
Kelkar, S. A., Pfister, K. K., Crystal, R. G., Leopold, P. L.
(2004). Cytoplasmic Dynein Mediates Adenovirus Binding to Microtubules. J. Virol.
78: 10122-10132
[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]
-
Chattopadhyay, M., Goss, J., Wolfe, D., Goins, W. C., Huang, S., Glorioso, J. C., Mata, M., Fink, D. J.
(2004). Protective effect of herpes simplex virus-mediated neurotrophin gene transfer in cisplatin neuropathy. Brain
127: 929-939
[Abstract]
[Full Text]
-
Clase, A. C., Lyman, M. G., del Rio, T., Randall, J. A., Calton, C. M., Enquist, L. W., Banfield, B. W.
(2003). The Pseudorabies Virus Us2 Protein, a Virion Tegument Component, Is Prenylated in Infected Cells. J. Virol.
77: 12285-12298
[Abstract]
[Full Text]
-
Suikkanen, S., Aaltonen, T., Nevalainen, M., Valilehto, O., Lindholm, L., Vuento, M., Vihinen-Ranta, M.
(2003). Exploitation of Microtubule Cytoskeleton and Dynein during Parvoviral Traffic toward the Nucleus. J. Virol.
77: 10270-10279
[Abstract]
[Full Text]
-
Grieshaber, S. S., Grieshaber, N. A., Hackstadt, T.
(2003). Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process. J. Cell Sci.
116: 3793-3802
[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]
-
Mahajan, S. S., Little, M. M., Vazquez, R., Wilson, A. C.
(2002). Interaction of HCF-1 with a Cellular Nuclear Export Factor. J. Biol. Chem.
277: 44292-44299
[Abstract]
[Full Text]
-
Susalka, S. J., Nikulina, K., Salata, M. W., Vaughan, P. S., King, S. M., Vaughan, K. T., Pfister, K. K.
(2002). The Roadblock Light Chain Binds a Novel Region of the Cytoplasmic Dynein Intermediate Chain. J. Biol. Chem.
277: 32939-32946
[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]
-
Dohner, K., Wolfstein, A., Prank, U., Echeverri, C., Dujardin, D., Vallee, R., Sodeik, B.
(2002). Function of Dynein and Dynactin in Herpes Simplex Virus Capsid Transport. Mol. Biol. Cell
13: 2795-2809
[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]
-
Willard, M.
(2002). Rapid Directional Translocations in Virus Replication. J. Virol.
76: 5220-5232
[Abstract]
[Full Text]
-
Tai, C.-Y., Dujardin, D. L., Faulkner, N. E., Vallee, R. B.
(2002). Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. JCB
156: 959-968
[Abstract]
[Full Text]
-
Diefenbach, R. J., Miranda-Saksena, M., Diefenbach, E., Holland, D. J., Boadle, R. A., Armati, P. J., Cunningham, A. L.
(2002). Herpes Simplex Virus Tegument Protein US11 Interacts with Conventional Kinesin Heavy Chain. J. Virol.
76: 3282-3291
[Abstract]
[Full Text]
-
van Leeuwen, H., Elliott, G., O'Hare, P.
(2002). Evidence of a Role for Nonmuscle Myosin II in Herpes Simplex Virus Type 1 Egress. J. Virol.
76: 3471-3481
[Abstract]
[Full Text]
-
Ogawa-Goto, K., Irie, S., Omori, A., Miura, Y., Katano, H., Hasegawa, H., Kurata, T., Sata, T., Arao, Y.
(2002). An Endoplasmic Reticulum Protein, p180, Is Highly Expressed in Human Cytomegalovirus-Permissive Cells and Interacts with the Tegument Protein Encoded by UL48. J. Virol.
76: 2350-2362
[Abstract]
[Full Text]
-
Ma, S., Chisholm, R. L.
(2002). Cytoplasmic dynein-associated structures move bidirectionally in vivo. J. Cell Sci.
115: 1453-1460
[Abstract]
[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]
-
Mebatsion, T.
(2001). Extensive Attenuation of Rabies Virus by Simultaneously Modifying the Dynein Light Chain Binding Site in the P Protein and Replacing Arg333 in the G Protein. J. Virol.
75: 11496-11502
[Abstract]
[Full Text]
-
Poisson, N., Real, E., Gaudin, Y., Vaney, M.-C., King, S., Jacob, Y., Tordo, N., Blondel, D.
(2001). Molecular basis for the interaction between rabies virus phosphoprotein P and the dynein light chain LC8: dissociation of dynein-binding properties and transcriptional functionality of P. J. Gen. Virol.
82: 2691-2696
[Abstract]
[Full Text]
-
Alonso, C., Miskin, J., Hernaez, B., Fernandez-Zapatero, P., Soto, L., Canto, C., Rodriguez-Crespo, I., Dixon, L., Escribano, J. M.
(2001). African Swine Fever Virus Protein p54 Interacts with the Microtubular Motor Complex through Direct Binding to Light-Chain Dynein. J. Virol.
75: 9819-9827
[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]
-
Sciortino, M.-T., Suzuki, M., Taddeo, B., Roizman, B.
(2001). RNAs Extracted from Herpes Simplex Virus 1 Virions: Apparent Selectivity of Viral but Not Cellular RNAs Packaged in Virions. J. Virol.
75: 8105-8116
[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]
-
Lilley, C. E., Groutsi, F., Han, Z., Palmer, J. A., Anderson, P. N., Latchman, D. S., Coffin, R. S.
(2001). Multiple Immediate-Early Gene-Deficient Herpes Simplex Virus Vectors Allowing Efficient Gene Delivery to Neurons in Culture and Widespread Gene Delivery to the Central Nervous System In Vivo. J. Virol.
75: 4343-4356
[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]
-
Raux, H., Flamand, A., Blondel, D.
(2000). Interaction of the Rabies Virus P Protein with the LC8 Dynein Light Chain. J. Virol.
74: 10212-10216
[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]
-
Advani, S. J., Weichselbaum, R. R., Roizman, B.
(2000). The role of cdc2 in the expression of herpes simplex virus genes. Proc. Natl. Acad. Sci. USA
10.1073/pnas.200375297v1
[Abstract]
[Full Text]
-
Advani, S. J., Weichselbaum, R. R., Roizman, B.
(2000). The role of cdc2 in the expression of herpes simplex virus genes. Proc. Natl. Acad. Sci. USA
97: 10996-11001
[Abstract]
[Full Text]