Herpes simplex virus ICP27 protein directly interacts with the nuclear pore complex through Nup62, inhibiting host nucleocytoplasmic transport pathways

Journal of Biological Chemistry

Volumn 287, Issue 15, 2012, Pages 12277-12292

  Malik, Poonam ^a,b   Tabarraei, Alijan ^b   Kehlenbach, Ralph H ^c   Korfali, Nadia ^a   Iwasawa, Ryota ^a   Graham, Sheila V ^b   Schirmer, Eric C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CO-IMMUNOPRECIPITATIONS; HERPES SIMPLEX VIRUS; HOST CELLS; IN-VITRO; NUCLEAR EXPORT; NUCLEAR IMPORT; NUCLEAR PORE COMPLEXES; NUCLEAR TRANSPORT; NUCLEOCYTOPLASMIC TRANSPORT; TRANSPORT PATHWAYS; WILD TYPES;

MACHINERY; RNA; VIRUSES;

PROTEINS;

CORE PROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; MUTANT PROTEIN; NUCLEOPORIN; PROTEIN ICP27; PROTEIN NUP62; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING ASSAY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE DELETION; GENE MAPPING; HERPES SIMPLEX VIRUS; HOST CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; NUCLEAR IMPORT; NUCLEOCYTOPLASMIC TRANSPORT; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; BINDING SITES; CELL NUCLEUS; HELA CELLS; HERPESVIRUS 1, HUMAN; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNOPRECIPITATION; MEMBRANE GLYCOPROTEINS; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PEPTIDE MAPPING; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; RNA, MESSENGER; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

SIMPLEXVIRUS;

EID: 84859501317     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.331777     Document Type: Article

References (84)

1. Pasdeloup, D., Blondel, D., Isidro, A. L., and Rixon, F. J. (2009) Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J. Virol. 83, 6610-6623
2. Copeland, A. M., Newcomb, W. W., and Brown, J. C. (2009) Herpes simplex virus replication. Roles of viral proteins and nucleoporins in capsidnucleus attachment. J. Virol. 83, 1660-1668
3. Pellet, P. E., and Roizman, B. (2007) The Herpesviridae family. A brief introduction. in Fields' Virology (Knipe, D. M., and Howley, P. M., eds) 5th Ed., pp. 2501-2601, Wolters Kluwer Health/Lippincott Williams &Wilkins, Philadelphia
4. Wente, S. R. (2000) Gatekeepers of the nucleus. Science 288, 1374-1377
5. Strambio-De-Castillia, C., Niepel, M., and Rout, M. P. (2010) The nuclear pore complex. Bridging nuclear transport and gene regulation. Nat. Rev. Mol. Cell Biol. 11, 490-501
6. Wagstaff, K. M., and Jans, D. A. (2009) Importins and beyond. Non-conventional nuclear transport mechanisms. Traffic 10, 1188-1198
7. Arnold, M., Nath, A., Hauber, J., and Kehlenbach, R. H. (2006) Multiple importins function as nuclear transport receptors for the Rev protein of human immunodeficiency virus type 1. J. Biol. Chem. 281, 20883-20890 (Pubitemid 44115429)
8. Bonifaci, N., Moroianu, J., Radu, A., and Blobel, G. (1997) Karyopherin β2 mediates nuclear import of an mRNA binding protein. Proc. Natl. Acad. Sci. U.S.A. 94, 5055-5060 (Pubitemid 27214735)
9. Fridell, R. A., Truant, R., Thorne, L., Benson, R. E., and Cullen, B. R. (1997) Nuclear import of hnRNP A1 is mediated by a novel cellular cofactor related to karyopherin-β. J. Cell Sci. 110, 1325-1331 (Pubitemid 27273703)
10. Fornerod, M., Ohno, M., Yoshida, M., and Mattaj, I. W. (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060 (Pubitemid 27408519)
11. Fischer, U., Huber, J., Boelens, W. C., Mattaj, I. W., and Lührmann, R. (1995) The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82, 475-483
12. Pasquinelli, A. E., Ernst, R. K., Lund, E., Grimm, C., Zapp, M. L., Rekosh, D., Hammarskjöld, M. L., and Dahlberg, J. E. (1997) The constitutive transport element (CTE) of Mason-Pfizer monkey virus (MPMV) accesses a cellular mRNA export pathway. EMBO J. 16, 7500-7510 (Pubitemid 28010509)
13. Saavedra, C., Felber, B., and Izaurralde, E. (1997) The simian retrovirus-1 constitutive transport element, unlike the HIV-1 RRE, uses factors required for cellular mRNA export. Curr. Biol. 7, 619-628 (Pubitemid 27408859)
14. Strässer, K., and Hurt, E. (2000) Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J. 19, 410-420 (Pubitemid 30072611)
15. Grüter, P., Tabernero, C., von Kobbe, C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B. K., and Izaurralde, E. (1998) TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1, 649-659 (Pubitemid 128379243)
16. Petersen, J. M., Her, L. S., and Dahlberg, J. E. (2001) Multiple vesiculoviral matrix proteins inhibit both nuclear export and import. Proc. Natl. Acad. Sci. U.S.A. 98, 8590-8595 (Pubitemid 32678072)
17. Gustin, K. E., and Sarnow, P. (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J. 20, 240-249 (Pubitemid 32099120)
18. Gustin, K. E., and Sarnow, P. (2002) Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J. Virol. 76, 8787-8796 (Pubitemid 34864074)
19. Nelson, L. M., Rose, R. C., and Moroianu, J. (2003) The L1 major capsid protein of human papillomavirus type 11 interacts with Kap β2 and Kap β3 nuclear import receptors. Virology 306, 162-169 (Pubitemid 36293406)
20. Darshan, M. S., Lucchi, J., Harding, E., and Moroianu, J. (2004) The l2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors. J. Virol. 78, 12179-12188 (Pubitemid 39458737)
21. Park, N., Skern, T., and Gustin, K. E. (2010) Specific cleavage of the nuclear pore complex protein Nup62 by a viral protease. J. Biol. Chem. 285, 28796-28805
22. Faria, P. A., Chakraborty, P., Levay, A., Barber, G. N., Ezelle, H. J., Enninga, J., Arana, C., van Deursen, J., and Fontoura, B. M. (2005) VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol. Cell 17, 93-102 (Pubitemid 40075368)
23. Satterly, N., Tsai, P. L., van Deursen, J., Nussenzveig, D. R., Wang, Y., Faria, P. A., Levay, A., Levy, D. E., and Fontoura, B. M. (2007) Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc. Natl. Acad. Sci. U.S.A. 104, 1853-1858 (Pubitemid 46239868)
24. Macaulay, C., Meier, E., and Forbes, D. J. (1995) Differential mitotic phosphorylation of proteins of the nuclear pore complex. J. Biol. Chem. 270, 254-262
25. Fontoura, B. M., Faria, P. A., and Nussenzveig, D. R. (2005) Viral interactions with the nuclear transport machinery. Discovering and disrupting pathways. IUBMB Life 57, 65-72 (Pubitemid 40632296)
26. Gustin, K. E. (2003) Inhibition of nucleo-cytoplasmic trafficking by RNA viruses. Targeting the nuclear pore complex. Virus Res. 95, 35-44
27. Tsuji, T., Sheehy, N., Gautier, V. W., Hayakawa, H., Sawa, H., and Hall, W. W. (2007) The nuclear import of the human T lymphotropic virus type I (HTLV-1) Tax protein is carrier- and energy-independent. J. Biol. Chem. 282, 13875-13883 (Pubitemid 47100539)
28. Sandri-Goldin, R. M. (2008) The many roles of the regulatory protein ICP27 during herpes simplex virus infection. Front. Biosci. 13, 5241-5256
29. Smith, R. W., Malik, P., and Clements, J. B. (2005) The herpes simplex virus ICP27 protein. A multifunctional post-transcriptional regulator of gene expression. Biochem. Soc. Trans. 33, 499-501 (Pubitemid 40873875)
30. Malik, P., Blackbourn, D. J., and Clements, J. B. (2004) The evolutionarily conserved Kaposi's sarcoma-associated herpesvirus ORF57 protein interacts with REF protein and acts as an RNA export factor. J. Biol. Chem. 279, 33001-33011 (Pubitemid 39014760)
31. Hiriart, E., Farjot, G., Gruffat, H., Nguyen, M. V., Sergeant, A., and Manet, E. (2003) A novel nuclear export signal and a REF interaction domain both promote mRNA export by the Epstein-Barr virus EB2 protein. J. Biol. Chem. 278, 335-342 (Pubitemid 36043581)
32. Han, Z., and Swaminathan, S. (2006) Kaposi's sarcoma-associated herpes-virus lytic gene ORF57 is essential for infectious virion production. J. Virol. 80, 5251-5260
33. Gruffat, H., Batisse, J., Pich, D., Neuhierl, B., Manet, E., Hammerschmidt, W., and Sergeant, A. (2002) Epstein-Barr virus mRNA export factor EB2 is essential for production of infectious virus. J. Virol. 76, 9635-9644 (Pubitemid 35006504)
34. Rice, S. A., and Knipe, D. M. (1988) Gene-specific transactivation by herpes simplex virus type 1 α protein ICP27. J. Virol. 62, 3814-3823
35. Sekulovich, R. E., Leary, K., and Sandri-Goldin, R. M. (1988) The herpes simplex virus type 1 α protein ICP27 can act as a trans-repressor or a trans-activator in combination with ICP4 and ICP0. J. Virol. 62, 4510-4522 (Pubitemid 19006112)
36. McCarthy, A. M., McMahan, L., and Schaffer, P. A. (1989) Herpes simplex virus type 1 ICP27 deletion mutants exhibit altered patterns of transcription and are DNA-deficient. J. Virol. 63, 18-27 (Pubitemid 19028077)
37. Rice, S. A., and Knipe, D. M. (1990) Genetic evidence for two distinct transactivation functions of the herpes simplex virus α protein ICP27. J. Virol. 64, 1704-1715 (Pubitemid 20104909)
38. Hardwicke, M. A., and Sandri-Goldin, R. M. (1994) The herpes simplex virus regulatory protein ICP27 contributes to the decrease in cellular mRNA levels during infection. J. Virol. 68, 4797-4810 (Pubitemid 24226544)
39. Fontaine-Rodriguez, E. C., and Knipe, D. M. (2008) Herpes simplex virus ICP27 increases translation of a subset of viral late mRNAs. J. Virol. 82, 3538-3545 (Pubitemid 351429929)
40. Larralde, O., Smith, R. W., Wilkie, G. S., Malik, P., Gray, N. K., and Clements, J. B. (2006) Direct stimulation of translation by the multifunctional herpesvirus ICP27 protein. J. Virol. 80, 1588-1591 (Pubitemid 43134114)
41. Ellison, K. S., Maranchuk, R. A., Mottet, K. L., and Smiley, J. R. (2005) Control of VP16 translation by the herpes simplex virus type 1 immediate-early protein ICP27. J. Virol. 79, 4120-4131 (Pubitemid 40388350)
42. Escudero-Paunetto, L., Li, L., Hernandez, F. P., and Sandri-Goldin, R. M. (2010) SR proteins SRp20 and 9G8 contribute to efficient export of herpes simplex virus 1 mRNAs. Virology 401, 155-164
43. Long, J. C., and Caceres, J. F. (2009) The SR protein family of splicing factors. Master regulators of gene expression. Biochem. J. 417, 15-27
44. Pearson, A., Knipe, D. M., and Coen, D. M. (2004) ICP27 selectively regulates the cytoplasmic localization of a subset of viral transcripts in herpes simplex virus type 1-infected cells. J. Virol. 78, 23-32 (Pubitemid 37549716)
45. Hernandez, F. P., and Sandri-Goldin, R. M. (2010) Herpes simplex virus 1 regulatory protein ICP27 undergoes a head-to-tail intramolecular interaction. J. Virol. 84, 4124-4135
46. Zhi, Y., Sciabica, K. S., and Sandri-Goldin, R. M. (1999) Self-interaction of the herpes simplex virus type 1 regulatory protein ICP27. Virology 257, 341-351 (Pubitemid 29393402)
47. Koffa, M. D., Clements, J. B., Izaurralde, E., Wadd, S., Wilson, S. A., Mattaj, I. W., and Kuersten, S. (2001) Herpes simplex virus ICP27 protein provides viral mRNAs with access to the cellular mRNA export pathway. EMBO J. 20, 5769-5778 (Pubitemid 33010052)
48. Chen, I. H., Li, L., Silva, L., and Sandri-Goldin, R. M. (2005) ICP27 recruits Aly/REF but not TAP/NXF1 to herpes simplex virus type 1 transcription sites although TAP/NXF1 is required for ICP27 export. J. Virol. 79, 3949-3961 (Pubitemid 40388335)
49. Chen, I. H., Sciabica, K. S., and Sandri-Goldin, R. M. (2002) ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J. Virol. 76, 12877-12889 (Pubitemid 35386971)
50. Soliman, T. M., and Silverstein, S. J. (2000) Herpesvirus mRNAs are sorted for export via Crm1-dependent and -independent pathways. J. Virol. 74, 2814-2825 (Pubitemid 30117593)
51. Lilley, C. E., Groutsi, F., Han, Z., Palmer, J. A., Anderson, P. N., Latchman, D. S., and 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 (Pubitemid 32410146)
52. Soliman, T. M., and Silverstein, S. J. (2000) Identification of an export control sequence and a requirement for the KH domains in ICP27 from herpes simplex virus type 1. J. Virol. 74, 7600-7609 (Pubitemid 30613106)
53. Lengyel, J., Guy, C., Leong, V., Borge, S., and Rice, S. A. (2002) Mapping of functional regions in the amino-terminal portion of the herpes simplex virus ICP27 regulatory protein. Importance of the leucine-rich nuclear export signal and RGG box RNA-binding domain. J. Virol. 76, 11866-11879 (Pubitemid 35304287)
54. Rice, S. A., Lam, V., and Knipe, D. M. (1993) The acidic amino-terminal region of herpes simplex virus type 1 α protein ICP27 is required for an essential lytic function. J. Virol. 67, 1778-1787 (Pubitemid 23088348)
55. Aubert, M., Rice, S. A., and Blaho, J. A. (2001) Accumulation of herpes simplex virus type 1 early and leaky-late proteins correlates with apoptosis prevention in infected human HEp-2 cells. J. Virol. 75, 1013-1030 (Pubitemid 32037304)
56. Mears, W. E., Lam, V., and Rice, S. A. (1995) Identification of nuclear and nucleolar localization signals in the herpes simplex virus regulatory protein ICP27. J. Virol. 69, 935-947
57. Rice, S. A., and Lam, V. (1994) Amino acid substitution mutations in the herpes simplex virus ICP27 protein define an essential gene regulation function. J. Virol. 68, 823-833 (Pubitemid 24022185)
58. Mears, W. E., and Rice, S. A. (1996) The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J. Virol. 70, 7445-7453 (Pubitemid 26339048)
59. Braun, I. C., Rohrbach, E., Schmitt, C., and Izaurralde, E. (1999) TAP binds to the constitutive transport element (CTE) through a novel RNA-binding motif that is sufficient to promote CTE-dependent RNA export from the nucleus. EMBO J. 18, 1953-1965 (Pubitemid 29158538)
60. Bryant, H. E., Matthews, D. A., Wadd, S., Scott, J. E., Kean, J., Graham, S., Russell, W. C., and Clements, J. B. (2000) Interaction between herpes simplex virus type 1 IE63 protein and cellular protein p32. J. Virol. 74, 11322-11328 (Pubitemid 32224002)
61. Hutten, S., Flotho, A., Melchior, F., and Kehlenbach, R. H. (2008) The Nup358-RanGAP complex is required for efficient importin α/β- dependent nuclear import. Mol. Biol. Cell 19, 2300-2310
62. Siomi, H., and Dreyfuss, G. (1995) A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129, 551-560
63. Phelan, A., Carmo-Fonseca, M., McLaughlan, J., Lamond, A. I., and Clements, J. B. (1993) A herpes simplex virus type 1 immediate-early gene product, IE63, regulates small nuclear ribonucleoprotein distribution. Proc. Natl. Acad. Sci. U.S.A. 90, 9056-9060 (Pubitemid 23306450)
64. Gerace, L., Ottaviano, Y., and Kondor-Koch, C. (1982) Identification of a major polypeptide of the nuclear pore complex. J. Cell Biol. 95, 826-837 (Pubitemid 13186105)
65. Malik, P., Korfali, N., Srsen, V., Lazou, V., Batrakou, D. G., Zuleger, N., Kavanagh, D. M., Wilkie, G. S., Goldberg, M. W., and Schirmer, E. C. (2010) Cell-specific and lamin-dependent targeting of novel transmembrane proteins in the nuclear envelope. Cell Mol. Life Sci. 67, 1353-1369
66. Hofemeister, H., and O'Hare, P. (2008) Nuclear pore composition and gating in herpes simplex virus-infected cells. J. Virol. 82, 8392-8399
67. Pritchard, C. E., Fornerod, M., Kasper, L. H., and van Deursen, J. M. (1999) RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J. Cell Biol. 145, 237-254
68. Bachi, A., Braun, I. C., Rodrigues, J. P., Panté, N., Ribbeck, K., von Kobbe, C., Kutay, U., Wilm, M., Görlich, D., Carmo-Fonseca, M., and Izaurralde, E. (2000) The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6, 136-158 (Pubitemid 30069044)
69. Michael, W. M., Choi, M., and Dreyfuss, G. (1995) A nuclear export signal in hnRNP A1.Asignal-mediated, temperature-dependent nuclear protein export pathway. Cell 83, 415-422
70. Pollard, V. W., Michael, W. M., Nakielny, S., Siomi, M. C., Wang, F., and Dreyfuss, G. (1996) A novel receptor-mediated nuclear protein import pathway. Cell 86, 985-994 (Pubitemid 26336802)
71. Schmitt, I., and Gerace, L. (2001) In vitro analysis of nuclear transport mediated by the C-terminal shuttle domain of Tap. J. Biol. Chem. 276, 42355-42363
72. Flach, J., Bossie, M., Vogel, J., Corbett, A., Jinks, T., Willins, D. A., and Silver, P. A. (1994) A yeast RNA-binding protein shuttles between the nucleus and the cytoplasm. Mol. Cell Biol. 14, 8399-8407 (Pubitemid 24373589)
73. Piñol-Roma, S., and Dreyfuss, G. (1992) Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355, 730-732
74. Kambach, C., and Mattaj, I. W. (1992) Intracellular distribution of the U1A protein depends on active transport and nuclear binding to U1 snRNA. J. Cell Biol. 118, 11-21
75. Li, Y., Yamakita, Y., and Krug, R. M. (1998) Regulation of a nuclear export signal by an adjacent inhibitory sequence. The effector domain of the influenza virus NS1 protein. Proc. Natl. Acad. Sci. U.S.A. 95, 4864-4869 (Pubitemid 28208516)
76. Meyer, B. E., and Malim, M. H. (1994) The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev. 8, 1538-1547 (Pubitemid 24218288)
77. Lengyel, J., Strain, A. K., Perkins, K. D., and Rice, S. A. (2006) ICP27-dependent resistance of herpes simplex virus type 1 to leptomycin B is associated with enhanced nuclear localization of ICP4 and ICP0. Virology 352, 368-379 (Pubitemid 44216000)
78. Johnson, L. A., Li, L., and Sandri-Goldin, R. M. (2009) The cellular RNA export receptor TAP/NXF1 is required for ICP27-mediated export of herpes simplex virus 1 RNA, but the TREX complex adaptor protein Aly/REF appears to be dispensable. J. Virol. 83, 6335-6346
79. Cullen, B. R. (1994) RNA sequence-mediated gene regulation in HIV-1. Infect. Agents Dis. 3, 68-76
80. Mears, W. E., and Rice, S. A. (1998) The herpes simplex virus immediate-early protein ICP27 shuttles between nucleus and cytoplasm. Virology 242, 128-137 (Pubitemid 28396366)
81. Ellison, K. S., Rice, S. A., Verity, R., and Smiley, J. R. (2000) Processing of α-globin and ICP0 mRNA in cells infected with herpes simplex virus type 1 ICP27 mutants. J. Virol. 74, 7307-7319 (Pubitemid 30613076)
82. Zhi, Y., and Sandri-Goldin, R. M. (1999) Analysis of the phosphorylation sites of herpes simplex virus type 1 regulatory protein ICP27. J. Virol. 73, 3246-3257 (Pubitemid 29135717)
83. Rojas, S., Corbin-Lickfett, K. A., Escudero-Paunetto, L., and Sandri-Goldin, R. M. (2010) ICP27 phosphorylation site mutants are defective in herpes simplex virus 1 replication and gene expression. J. Virol. 84, 2200-2211
84. Souki, S. K., Gershon, P. D., and Sandri-Goldin, R. M. (2009) Arginine methylation of the ICP27 RGG box regulates ICP27 export and is required for efficient herpes simplex virus 1 replication. J. Virol. 83, 5309-5320