Nucleolin interacts with US11 protein of herpes simplex virus 1 and is involved in its trafficking

Journal of Virology

Volumn 86, Issue 3, 2012, Pages 1449-1457

  Greco, Anna ^a,b   Arata, Loredana ^a,b   Soler, Eric ^a,b,g   Gaume, Xavier ^c   Couté, Yohann ^d,h   Hacot, Sabine ^a,b,e   Callé, Aleth ^a,b   Monier, Karine ^c   Epstein, Alberto L ^a,b   Sanchez, Jean Charles ^f   Bouvet, Philippe ^c   Diaz, Jean Jacques ^a,b,e  

^a UNIVERSITÉ LYON 1   (France)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^c Laboratoire Joliot Curie   (France)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e CENTRE LÉON BÉRARD   (France)

^f UNIVERSITY OF GENEVA   (Switzerland)

^g ERASMUS MEDICAL CENTER   (Netherlands)

^h CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOLIN; PROTEIN US11; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL INVASION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE SILENCING; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT;

BLOTTING, FAR-WESTERN; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; VIRAL PROTEINS;

HUMAN HERPESVIRUS 1;

EID: 84857099605     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06194-11     Document Type: Article

References (43)

1. Belin S, et al. 2010. Uncoupling ribosome biogenesis regulation from RNA polymerase I activity during herpes simplex virus type 1 infection. RNA 16:131-140.
2. Benboudjema L, Mulvey M, Gao Y, Pimplikar SW, Mohr I. 2003. Association of the herpes simplex virus type 1 Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides. J. Virol. 77:9192-9203.
3. Besse S, et al. 1996. In situ hybridization and immuno-electron microscope analyses of the Us11 gene of herpes simplex virus type 1 during transient expression. Chromosoma 104:434-444.
4. Bouvet P, Diaz JJ, Kindbeiter K, Madjar JJ, Amalric F. 1998. Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 273:19025-19029.
5. Brown SM, Harland J. 1987. Three mutants of herpes simplex virus type 2: one lacking the genes US10, US11 and US12 and two in which Rs has been extended by 6 kb to 0.91 map units with loss of Us sequences between 0.94 and the Us/TRs junction. J. Gen. Virol. 68:1-18.
6. Callé A, et al. 2008. Nucleolin is required for an efficient herpes simplex virus type 1 infection. J. Virol. 82:4762-4773.
7. Catez F, et al. 2002. Unique motif for nucleolar retention and nuclear export regulated by phosphorylation. Mol. Cell. Biol. 22:1126-1139.
8. Couté Y, et al. 2010. Early activation of the fatty acid metabolism pathway by chronic high glucose exposure in rat insulin secretory beta-cells. Proteomics 10:59-71.
9. Dalziel RG, Marsden HS. 1984. Identification of two herpes simplex virus type 1-induced proteins (21K and 22K) which interact specifically with the a sequence of herpes simplex virus DNA. J. Gen. Virol. 65:1467-1475.
10. Diaz JJ, et al. 1996. Post-transcriptional transactivation of human retroviral envelope glycoprotein expression by herpes simplex virus Us11 protein. Nature 379:273-277.
11. Diaz JJ, Giraud S, Greco A. 2002. Alteration of ribosomal protein maps in herpes simplex virus type 1 infection. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 771:237-249.
12. Diaz JJ, et al. 1993. The herpes simplex virus type 1 Us11 gene product is a phosphorylated protein found to be non-specifically associated with both ribosomal subunits. J. Gen. Virol. 74:397-406.
13. Diaz-Latoud C, et al. 1997. Herpes simplex virus Us11 protein enhances recovery of protein synthesis and survival in heat shock treated HeLa cells. Cell Stress Chaperones 2:119-131.
14. Diefenbach RJ, et al. 2002. Herpes simplex virus tegument protein US11 interacts with conventional kinesin heavy chain. J. Virol. 76:3282-3291.
15. Ghisolfi-Nieto L, Joseph G, Puvion-Dutilleul F, Amalric F, Bouvet P. 1996. Nucleolin is a sequence-specific RNA-binding protein: characterization of targets on pre-ribosomal RNA. J. Mol. Biol. 260:34-53.
16. Greco A, Laurent AM, Madjar JJ. 1997. Repression of ß-actin synthesis and persistence of ribosomal protein synthesis after infection of HeLa cells by herpes simplex virus type 1 are under translational control. Mol. Gen. Genet. 256:320-327.
17. Greco A, et al. 1994. The DNA sequence coding for the 5′ untranslated region of herpes simplex type 1 ICP22 mRNA mediates a high level of gene expression. J. Gen. Virol. 75:1693-1702.
18. Hill TJ, Yirrell DL, Blyth WA. 1986. Infection of the adrenal gland as a route to the central nervous system after viraemia with herpes simplex virus in the mouse. J. Gen. Virol. 67:309-320.
19. Javouhey E, Gibert B, Arrigo AP, Diaz JJ, Diaz-Latoud C. 2008. Protection against heat and staurosporine mediated apoptosis by the HSV-1 US11 protein. Virology 376:31-41.
20. Khoo D, Perez C, Mohr I. 2002. Characterization of RNA determinants recognized by the arginine- and proline-rich region of Us11, a herpes simplex virus type 1-encoded double-stranded RNA binding protein that prevents PKR activation. J. Virol. 76:11971-11981.
21. Longnecker R, Roizman B. 1987. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome. Science 236:573-576.
22. Longnecker R, Roizman B. 1986. Generation of an inverting herpes simplex virus 1 mutant lacking the L-S junction a sequences, an origin of DNA synthesis, and several genes including those specifying glycoprotein E and the alpha 47 gene. J. Virol. 58:583-591.
23. López-Iglesias C, Puvion-Dutilleul F, Cebrian J, Christensen ME. 1988. Herpes simplex virus type 1-induced modifications in the distribution of nucleolar B-36 protein. Eur. J. Cell Biol. 46:259-269.
24. Lymberopoulos MH, Pearson A. 2007. Involvement of UL24 in herpessimplex-virus-1-induced dispersal of nucleolin. Virology 363:397-409.
25. MacLean CA, Rixon FJ, Marsden HS. 1987. The products of gene Us11 of herpes simplex virus type 1 are DNA-binding and localize to the nucleoli of infected cells. J. Gen. Virol. 68:1921-1937.
26. Nishiyama Y, Kurachi R, Daikoku T, Umene K. 1993. The US 9, 10, 11, and 12 genes of herpes simplex virus type 1 are of no importance for its neurovirulence and latency in mice. Virology 194:419-423.
27. Peters GA, Khoo D, Mohr I, Sen GC. 2002. Inhibition of PACTmediated activation of PKR by the herpes simplex virus type 1 Us11 protein. J. Virol. 76:11054-11064.
28. Puvion-Dutilleul F. 1987. Localization of viral-specific 21 kDa protein in nucleoli of herpes simplex infected cells. Eur. J. Cell Biol. 43:487-498.
29. Roizman B, Sears AE. 1993. Herpes simplex viruses and their replication, p 11-68. In Roizman B, Whitley RJ, Lopez C (ed), The human herpes viruses, 3rd ed. Raven Press, New York, NY.
30. Roller RJ, Roizman B. 1991. Herpes simplex virus 1 RNA-binding protein US11 negatively regulates the accumulation of a truncated viral mRNA. J. Virol. 65:5873-5879.
31. Roller RJ, Roizman B. 1992. The herpes simplex virus 1 RNA binding protein Us11 is a virion component and associates with ribosomal 60S subunits. J. Virol. 66:3624-3632.
32. Sagou K, Uema M, Kawaguchi Y. 2010. Nucleolin is required for efficient nuclear egress of herpes simplex virus 1 nucleocapsids. J. Virol. 84:2110-2121.
33. Sànchez R, Mohr I. 2007. Inhibition of cellular 2′-5′ oligoadenylate synthetase by the herpes simplex virus type 1 Us11 protein. J. Virol. 81: 3455-3464.
34. Schaerer-Uthurralt N, Erard M, Kindbeiter K, Madjar JJ, Diaz JJ. 1998. Distinct domains in herpes simplex virus type 1 US11 protein mediate post-transcriptional transactivation of human T-lymphotropic virus type I envelope glycoprotein gene expression and specific binding to the Rex responsive element. J. Gen. Virol. 79:1593-1602.
35. Scherl A, et al. 2002. Functional proteomic analysis of the human nucleolus. Mol. Biol. Cell 13:4100-4109.
36. Serin G, et al. 1997. Two RNA-binding domains determine the RNA-binding specificity of nucleolin. J. Biol. Chem. 272:13109-13116.
37. Simonin D, Diaz JJ, Kindbeiter K, Pernas P, Madjar JJ. 1995. Phosphorylation of herpes simplex virus type 1 Us11 protein is independent of viral genome expression. Electrophoresis 16:1317-1322.
38. Simonin D, Diaz JJ, Masse T, Madjar JJ. 1997. Persistence of ribosomal protein synthesis after infection of HeLa cells by herpes simplex virus type 1. J. Gen. Virol. 78:435-443.
39. Storck S, Thiry M, Bouvet P. 2009. Conditional knockout of nucleolin in DT40 cells reveals the functional redundancy of its RNA-binding domains. Biol. Cell 101:153-167.
40. Ugrinova I, et al. 2007. Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication.BMCMol. Biol. 8:66.
41. Wagner EK, Roizman B. 1969. Ribonucleic acid synthesis in cells infected with herpes simplex virus. I. Patterns of ribonucleic acid synthesis in productively infected cells. J. Virol. 4:36-46.
42. Williamson MP. 1994. The structure and function of proline-rich regions in proteins. Biochem. J. 297:249-260.
43. Xing J, Wu F, Pan W, Zheng C. 2010. Molecular anatomy of subcellular localization of HSV-1 tegument protein US11 in living cells. Virus Res. 153:71-81.