Skip to main content
Top
Published in: Archives of Virology 9/2016

01-09-2016 | Original Article

Characterization of the nuclear import signal of herpes simplex virus 1 UL31

Authors: Mingsheng Cai, Daixiong Chen, Zhancheng Zeng, Hang Yang, Si Jiang, Xiaowei Li, Jingying Mai, Tao Peng, Meili Li

Published in: Archives of Virology | Issue 9/2016

Login to get access

Abstract

The herpes simplex virus 1 (HSV-1) UL31 protein is a multifunctional nucleoprotein that is important for viral infection; however, little is known concerning its subcellular localization signal. Here, by transfection with a series of HSV-1 UL31 deletion mutants fused to enhanced yellow fluorescent protein (EYFP), a bipartite nuclear localization signal (NLS) was identified and mapped to amino acids (aa) 1 to 27 (MYDTDPHRRGSRPGPYHGKERRRSRSS). Additionally, fluorescence results showed that the predicted nuclear export signal (NES) might be nonfunctional, and the functional NES of UL31 might require a specific conformation. Taken together, these results would provide significant information for the study of the biological function of UL31 during HSV-1 infection.
Literature
1.
go back to reference Ali SA, Steinkasserer A (1995) PCR-ligation-PCR mutagenesis: a protocol for creating gene fusions and mutations. Biotechniques 18:746–750PubMed Ali SA, Steinkasserer A (1995) PCR-ligation-PCR mutagenesis: a protocol for creating gene fusions and mutations. Biotechniques 18:746–750PubMed
2.
go back to reference Blaho JA, Mitchell C, Roizman B (1994) An amino acid sequence shared by the herpes simplex virus 1 alpha regulatory proteins 0, 4, 22, and 27 predicts the nucleotidylylation of the UL21, UL31, UL47, and UL49 gene products. J Biol Chem 269:17401–17410PubMed Blaho JA, Mitchell C, Roizman B (1994) An amino acid sequence shared by the herpes simplex virus 1 alpha regulatory proteins 0, 4, 22, and 27 predicts the nucleotidylylation of the UL21, UL31, UL47, and UL49 gene products. J Biol Chem 269:17401–17410PubMed
3.
go back to reference Cai MS, Wang S, Xing JJ, Zheng CF (2011) Characterization of the nuclear import and export signals, and subcellular transport mechanism of varicella-zoster virus ORF9. J Gen Virol 92:621–626CrossRefPubMed Cai MS, Wang S, Xing JJ, Zheng CF (2011) Characterization of the nuclear import and export signals, and subcellular transport mechanism of varicella-zoster virus ORF9. J Gen Virol 92:621–626CrossRefPubMed
4.
go back to reference Cai MS, Jiang S, Zeng ZC, Li XW, Mo CC, Yang YJ, Chen CK, Xie PP, Bian Y, Wang JL, Huang JL, Chen DX, Peng T, Li ML (2016) Probing the nuclear import signal and nuclear transport molecular determinants of PRV ICP22. Cell Biosci 6:3CrossRefPubMedPubMedCentral Cai MS, Jiang S, Zeng ZC, Li XW, Mo CC, Yang YJ, Chen CK, Xie PP, Bian Y, Wang JL, Huang JL, Chen DX, Peng T, Li ML (2016) Probing the nuclear import signal and nuclear transport molecular determinants of PRV ICP22. Cell Biosci 6:3CrossRefPubMedPubMedCentral
5.
go back to reference Cai MS, Si J, Li XW, Zeng ZC, Li ML (2016) Characterization of the nuclear import mechanisms of HSV-1 UL31. Biol Chem 397:555–561CrossRefPubMed Cai MS, Si J, Li XW, Zeng ZC, Li ML (2016) Characterization of the nuclear import mechanisms of HSV-1 UL31. Biol Chem 397:555–561CrossRefPubMed
6.
go back to reference Chang YE, Roizman B (1993) The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J Virol 67:6348–6356PubMedPubMedCentral Chang YE, Roizman B (1993) The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J Virol 67:6348–6356PubMedPubMedCentral
7.
go back to reference Chang YE, Van Sant C, Krug PW, Sears AE, Roizman B (1997) The null mutant of the U(L)31 gene of herpes simplex virus 1: construction and phenotype in infected cells. J Virol 71:8307–8315PubMedPubMedCentral Chang YE, Van Sant C, Krug PW, Sears AE, Roizman B (1997) The null mutant of the U(L)31 gene of herpes simplex virus 1: construction and phenotype in infected cells. J Virol 71:8307–8315PubMedPubMedCentral
9.
go back to reference Funk C, Ott M, Raschbichler V, Nagel CH, Binz A, Sodeik B, Bauerfeind R, Bailer SM (2015) The herpes simplex virus protein pUL31 escorts nucleocapsids to sites of nuclear egress, a process coordinated by its N-terminal domain. PLoS Pathog 11:e1004957CrossRefPubMedPubMedCentral Funk C, Ott M, Raschbichler V, Nagel CH, Binz A, Sodeik B, Bauerfeind R, Bailer SM (2015) The herpes simplex virus protein pUL31 escorts nucleocapsids to sites of nuclear egress, a process coordinated by its N-terminal domain. PLoS Pathog 11:e1004957CrossRefPubMedPubMedCentral
11.
go back to reference Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC (2007) Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci USA 104:7241–7246CrossRefPubMedPubMedCentral Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC (2007) Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci USA 104:7241–7246CrossRefPubMedPubMedCentral
12.
go back to reference Li ML, Cui W, Mo CC, Wang JL, Zhao ZY, Cai MS (2014) Cloning, expression, purification, antiserum preparation and its characteristics of the truncated UL6 protein of herpes simplex virus 1. Mol Biol Rep 41:5997–6002CrossRefPubMed Li ML, Cui W, Mo CC, Wang JL, Zhao ZY, Cai MS (2014) Cloning, expression, purification, antiserum preparation and its characteristics of the truncated UL6 protein of herpes simplex virus 1. Mol Biol Rep 41:5997–6002CrossRefPubMed
13.
go back to reference Li ML, Jiang S, Mo CC, Zeng ZC, Li XW, Chen CK, Yang YJ, Wang JL, Huang JL, Chen DX, Peng T, Cai MS (2015) Identification of molecular determinants for the nuclear import of pseudorabies virus UL31. Arch Biochem Biophys 587:12–17CrossRefPubMed Li ML, Jiang S, Mo CC, Zeng ZC, Li XW, Chen CK, Yang YJ, Wang JL, Huang JL, Chen DX, Peng T, Cai MS (2015) Identification of molecular determinants for the nuclear import of pseudorabies virus UL31. Arch Biochem Biophys 587:12–17CrossRefPubMed
14.
go back to reference Li ML, Jiang S, Wang JL, Mo CC, Zeng ZC, Yang YJ, Chen CK, Li XW, Cui W, Huang JL, Peng T, Cai MS (2015) Characterization of the nuclear import and export signals of pseudorabies virus UL31. Arch Virol 160:2591–2594CrossRefPubMed Li ML, Jiang S, Wang JL, Mo CC, Zeng ZC, Yang YJ, Chen CK, Li XW, Cui W, Huang JL, Peng T, Cai MS (2015) Characterization of the nuclear import and export signals of pseudorabies virus UL31. Arch Virol 160:2591–2594CrossRefPubMed
15.
go back to reference Mou F, Wills E, Baines JD (2009) Phosphorylation of the U(L)31 protein of herpes simplex virus 1 by the U(S)3-encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J Virol 83:5181–5191CrossRefPubMedPubMedCentral Mou F, Wills E, Baines JD (2009) Phosphorylation of the U(L)31 protein of herpes simplex virus 1 by the U(S)3-encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J Virol 83:5181–5191CrossRefPubMedPubMedCentral
16.
go back to reference Nakielny S, Dreyfuss G (1999) Transport of proteins and RNAs in and out of the nucleus. Cell 99:677–690CrossRefPubMed Nakielny S, Dreyfuss G (1999) Transport of proteins and RNAs in and out of the nucleus. Cell 99:677–690CrossRefPubMed
17.
go back to reference Park R, Baines JD (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 80:494–504CrossRefPubMedPubMedCentral Park R, Baines JD (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 80:494–504CrossRefPubMedPubMedCentral
18.
go back to reference Passvogel L, Klupp BG, Granzow H, Fuchs W, Mettenleiter TC (2015) Functional characterization of nuclear trafficking signals in pseudorabies virus pUL31. J Virol 89:2002–2012CrossRefPubMed Passvogel L, Klupp BG, Granzow H, Fuchs W, Mettenleiter TC (2015) Functional characterization of nuclear trafficking signals in pseudorabies virus pUL31. J Virol 89:2002–2012CrossRefPubMed
19.
go back to reference Reynolds AE, Wills EG, Roller RJ, Ryckman BJ, Baines JD (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 76:8939–8952CrossRefPubMedPubMedCentral Reynolds AE, Wills EG, Roller RJ, Ryckman BJ, Baines JD (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 76:8939–8952CrossRefPubMedPubMedCentral
20.
go back to reference Reynolds AE, Liang L, Baines JD (2004) Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes U(L)31 and U(L)34. J Virol 78:5564–5575CrossRefPubMedPubMedCentral Reynolds AE, Liang L, Baines JD (2004) Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes U(L)31 and U(L)34. J Virol 78:5564–5575CrossRefPubMedPubMedCentral
21.
go back to reference Roberts KL, Baines JD (2011) UL31 of herpes simplex virus 1 is necessary for optimal NF-kappaB activation and expression of viral gene products. J Virol 85:4947–4953CrossRefPubMedPubMedCentral Roberts KL, Baines JD (2011) UL31 of herpes simplex virus 1 is necessary for optimal NF-kappaB activation and expression of viral gene products. J Virol 85:4947–4953CrossRefPubMedPubMedCentral
22.
go back to reference Roller RJ, Bjerke SL, Haugo AC, Hanson S (2010) Analysis of a charge cluster mutation of herpes simplex virus type 1 UL34 and its extragenic suppressor suggests a novel interaction between pUL34 and pUL31 that is necessary for membrane curvature around capsids. J Virol 84:3921–3934CrossRefPubMedPubMedCentral Roller RJ, Bjerke SL, Haugo AC, Hanson S (2010) Analysis of a charge cluster mutation of herpes simplex virus type 1 UL34 and its extragenic suppressor suggests a novel interaction between pUL34 and pUL31 that is necessary for membrane curvature around capsids. J Virol 84:3921–3934CrossRefPubMedPubMedCentral
23.
go back to reference Simpson-Holley M, Baines J, Roller R, Knipe DM (2004) Herpes simplex virus 1 U(L)31 and U(L)34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. J Virol 78:5591–5600CrossRefPubMedPubMedCentral Simpson-Holley M, Baines J, Roller R, Knipe DM (2004) Herpes simplex virus 1 U(L)31 and U(L)34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. J Virol 78:5591–5600CrossRefPubMedPubMedCentral
24.
go back to reference Tanaka M, Kagawa H, Yamanashi Y, Sata T, Kawaguchi Y (2003) Construction of an excisable bacterial artificial chromosome containing a full-length infectious clone of herpes simplex virus type 1: viruses reconstituted from the clone exhibit wild-type properties in vitro and in vivo. J Virol 77:1382–1391CrossRefPubMed Tanaka M, Kagawa H, Yamanashi Y, Sata T, Kawaguchi Y (2003) Construction of an excisable bacterial artificial chromosome containing a full-length infectious clone of herpes simplex virus type 1: viruses reconstituted from the clone exhibit wild-type properties in vitro and in vivo. J Virol 77:1382–1391CrossRefPubMed
25.
go back to reference Wang KZ, Ni LW, Wang S, Zheng CF (2014) Herpes simplex virus 1 protein kinase US3 hyperphosphorylates p65/RelA and dampens NF-kappaB activation. J Virol 88:7941–7951CrossRefPubMedPubMedCentral Wang KZ, Ni LW, Wang S, Zheng CF (2014) Herpes simplex virus 1 protein kinase US3 hyperphosphorylates p65/RelA and dampens NF-kappaB activation. J Virol 88:7941–7951CrossRefPubMedPubMedCentral
26.
go back to reference Ye GJ, 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 97:11002–11007CrossRefPubMedPubMedCentral Ye GJ, 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 97:11002–11007CrossRefPubMedPubMedCentral
Metadata
Title
Characterization of the nuclear import signal of herpes simplex virus 1 UL31
Authors
Mingsheng Cai
Daixiong Chen
Zhancheng Zeng
Hang Yang
Si Jiang
Xiaowei Li
Jingying Mai
Tao Peng
Meili Li
Publication date
01-09-2016
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 9/2016
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-016-2910-z

Other articles of this Issue 9/2016

Archives of Virology 9/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.