Kaposi's sarcoma-associated herpesvirus ORF57 in viral RNA processing

Frontiers in Bioscience

Volumn 14, Issue 4, 2009, Pages 1516-1528

  Majerciak, Vladimir ^a   Zheng, Zhi Ming ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Gene expression; Kaposi's sarcoma associated herpesvirus; ORF57; Posttranscriptional regulation; Protein RNA interaction; Review; RNA export; RNA splicing

Indexed keywords

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 8;

VIRUS RNA;

GENETICS; HUMAN; HUMAN HERPESVIRUS 8; KAPOSI SARCOMA; METABOLISM; OPEN READING FRAME; REVIEW; RNA PROCESSING; RNA SPLICING; VIROLOGY; VIRUS GENE;

GENES, VIRAL; HERPESVIRUS 8, HUMAN; HUMANS; OPEN READING FRAMES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICING; RNA, VIRAL; SARCOMA, KAPOSI;

EID: 63849102197     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3322     Document Type: Article

References (84)

1. Y. Chang, E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles & P. S. Moore, Identification of rus-like DNA sequences in AIDS-associated Kaposi's sarcoma, Science 266, 1865-1869 (1994).
2. T. F. Schulz, Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8), J.Gen.Virol. 79, 1573-1591 (1998). (Pubitemid 28330660)
3. E. Cesarman, Y. Chang, P. S. Moore, J. W. Said & D. M. Knowles, Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas, N.Engl.J.Med. 332, 1186-1191 (1995).
4. J. Soulier, L. Grollet, E. Oksenhendler, P. Cacoub, D. Cazals-Hatem, P. Babinet, M. F. d'Agay, J. P. Clauvel, M. Raphael, L. Degos & F. Sigaux, Kaposi's sarcomaassociated herpesvirus-like DNA sequences in multicentric Castleman's disease, Blood 86, 1276-1280 (1995).
5. J. J. Russo, R. A. Bohenzky, M. C. Chien, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang & P. S. Moore, Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8), Proc.Natl.Acad.Sci.U.S.A 93, 14862-14867 (1996). (Pubitemid 26419060)
6. W. Zhong, H. Wang, B. Herndier & D. Ganem, Restricted expression of Kaposi sarcoma-associated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma, Proc.Natl.Acad.Sci.U.S.A 93, 6641-6646 (1996). (Pubitemid 26230362)
7. F. D. Fakhari & D. P. Dittmer, Charting latency transcripts in Kaposi's sarcoma-associated herpesvirus by whole-genome real-time quantitative PCR, J.Virol. 76, 6213-6223 (2002). (Pubitemid 34556317)
8. D. A. Davis, A. S. Rinderknecht, J. P. Zoeteweij, Y. Aoki, E. L. Read-Connole, G. Tosato, A. Blauvelt & R. Yarchoan, Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus, Blood 97, 3244-3250 (2001).
9. C. M. Klass, L. T. Krug, V. P. Pozharskaya & M. K. Offermann, The targeting of primary effusion lymphoma cells for apoptosis by inducing lytic replication of human herpesvirus 8 while blocking virus production, Blood 105, 4028-4034 (2005). (Pubitemid 40656152)
10. G. Miller, M. O. Rigsby, L. Heston, E. Grogan, R. Sun, C. Metroka, J. A. Levy, S. J. Gao, Y. Chang & P. Moore, Antibodies to butyrate-inducible antigens of Kaposi's sarcoma-associated herpesvirus in patients with HIV-1 infection, N.Engl.J.Med. 334, 1292-1297 (1996). (Pubitemid 26139952)
11. R. Renne, W. Zhong, B. Herndier, M. McGrath, N. Abbey, D. Kedes & D. Ganem, Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture, Nat.Med. 2, 342-346 (1996). (Pubitemid 26080656)
12. V. Majerciak, K. Yamanegi, E. Allemand, M. Kruhlak, A. R. Krainer & Z. M. Zheng, Kaposi sarcoma-associated herpesvirus ORF57 functions as a viral splicing factor and promotes the expression of intron-containing viral lytic genes in spliceosome-mediated RNA splicing, J.Virol. 82, 2792-2801 (2008). (Pubitemid 351329170)
13. V. Majerciak, N. Pripuzova, J. P. McCoy, S. J. Gao & Z. M. Zheng, Targeted disruption of Kaposi's sarcomaassociated herpesvirus ORF57 in the viral genome is detrimental for the expression of ORF59, K8alpha, and K8.1 and the production of infectious virus, J.Virol. 81, 1062-1071 (2007). (Pubitemid 46167830)
14. L. J. Bello, A. J. Davison, M. A. Glenn, A. Whitehouse, N. Rethmeier, T. F. Schulz & J. B. Clements, The human herpesvirus-8 ORF 57 gene and its properties, J.Gen.Virol. 80, 3207-3215 (1999).
15. J. R. Kirshner, D. M. Lukac, J. Chang & D. Ganem, Kaposi's sarcoma-associated herpesvirus open reading frame 57 encodes a posttranscriptional regulator with multiple distinct activities, J.Virol. 74, 3586-3597 (2000). (Pubitemid 30180302)
16. A. K. Gupta, V. Ruvolo, C. Patterson & S. Swaminathan, The human herpesvirus 8 homolog of Epstein-Barr virus SM protein (KS-SM) is a posttranscriptional activator of gene expression, J.Virol. 74, 1038-1044 (2000). (Pubitemid 30036245)
17. V. Majerciak, K. Yamanegi, S. H. Nie & Z. M. Zheng, Structural and functional analyses of Kaposi sarcomaassociated herpesvirus ORF57 nuclear localization signals in living cells, J.Biol.Chem. 281, 28365-28378 (2006). (Pubitemid 44414550)
18. M. Nekorchuk, Z. Han, T. T. Hsieh & S. Swaminathan, Kaposi's Sarcoma-Associated Herpesvirus ORF57 Protein Enhances mRNA Accumulation Independently of Effects on Nuclear RNA Export, J.Virol. 81, 9990-9998 (2007). (Pubitemid 350067702)
19. P. Malik, D. J. Blackbourn, M. F. Cheng, G. S. Hayward & J. B. Clements, Functional co-operation between the Kaposi's sarcoma-associated herpesvirus ORF57 and ORF50 regulatory proteins, J.Gen.Virol. 85, 2155-2166 (2004). (Pubitemid 39162586)
20. D. Palmeri, S. Spadavecchia, K. D. Carroll & D. M. Lukac, Promoter- and cell-specific transcriptional transactivation by the Kaposi's sarcoma-associated herpesvirus ORF57/Mta protein, J.Virol. 81, 13299-13314 (2007). (Pubitemid 350247827)
21. R. M. Sandri-Goldin, M. K. Hibbard & M. A. Hardwicke, The C-terminal repressor region of herpes simplex virus type 1 ICP27 is required for the redistribution of small nuclear ribonucleoprotein particles and splicing factor SC35; however, these alterations are not sufficient to inhibit host cell splicing, J.Virol. 69, 6063-6076 (1995).
22. R. M. Sandri-Goldin & M. K. Hibbard, The herpes simplex virus type 1 regulatory protein ICP27 coimmunoprecipitates with anti-Sm antiserum, and the C terminus appears to be required for this interaction, J.Virol. 70, 108-118 (1996). (Pubitemid 126508775)
23. M. Winkler, S. A. Rice & T. Stamminger, UL69 of human cytomegalovirus, an open reading frame with homology to ICP27 of herpes simplex virus, encodes a transactivator of gene expression, J.Virol. 68, 3943-3954 (1994). (Pubitemid 24177420)
24. P. Defechereux, L. Melen, L. Baudoux, M.-P. Merville-Louis, B. Rentier & J. Piette, Characterization of the regulatory functions of varicella-zoster virus open reading frame 4 gene product, J. Virol. 67, 4379-4385 (1993). (Pubitemid 23180767)
25. I. D. Cook, F. Shanahan & P. J. Farrell, Epstein-Barr virus SM protein, Virology 205, 217-227 (1994). (Pubitemid 24360608)
26. V. Ruvolo, E. Wang, S. Boyle & S. Swaminathan, The Epstein-Barr virus nuclear protein SM is both a posttranscriptional inhibitor and activator of gene expression, Proc.Natl.Acad.Sci.U.S.A 95, 8852-8857 (1998). (Pubitemid 28350578)
27. A. Whitehouse, M. Cooper & D. M. Meredith, The immediate-early gene product encoded by open reading frame 57 of herpesvirus saimiri modulates gene expression at a posttranscriptional level, J.Virol. 72, 857-861 (1998). (Pubitemid 28048913)
28. M. Cooper, D. J. Goodwin, K. T. Hall, A. J. Stevenson, D. M. Meredith, A. F. Markham & A. Whitehouse, The gene product encoded by ORF 57 of herpesvirus saimiri regulates the redistribution of the splicing factor SC-35, J.Gen.Virol. 80, 1311-1316 (1999). (Pubitemid 29213819)
29. D. J. Goodwin, K. T. Hall, A. J. Stevenson, A. F. Markham & A. Whitehouse, The open reading frame 57 gene product of herpesvirus saimiri shuttles between the nucleus and cytoplasm and is involved in viral RNA nuclear export, J.Virol. 73, 10519-10524 (1999).
30. V. Majerciak, K. Yamanegi & Z. M. Zheng, Gene structure and expression of Kaposi's sarcoma-associated herpesvirus ORF56, ORF57, ORF58, and ORF59, J.Virol. 80, 11968-11981 (2006). (Pubitemid 44904346)
31. M. Mackett, J. P. Stewart, V. P. de, M. Chee, S. Efstathiou, A. A. Nash & J. R. Arrand, Genetic content and preliminary transcriptional analysis of a representative region of murine gammaherpesvirus 68, J.Gen.Virol. 78, 1425-1433 (1997). (Pubitemid 27281345)
32. D. M. Lukac, J. R. Kirshner & D. Ganem, Transcriptional activation by the product of open reading frame 50 of Kaposi's sarcoma-associated herpesvirus is required for lytic viral reactivation in B cells, J.Virol. 73, 9348-9361 (1999). (Pubitemid 29487090)
33. K. Nishimura, K. Ueda, E. Guwanan, S. Sakakibara, E. Do, E. Osaki, K. Yada, T. Okuno & K. Yamanishi, A posttranscriptional regulator of Kaposi's sarcomaassociated herpesvirus interacts with RNA-binding protein PCBP1 and controls gene expression through the IRES, Virology. 325, 364-378 (2004). (Pubitemid 38906713)
34. D. M. Lukac, R. Renne, J. R. Kirshner & D. Ganem, Reactivation of Kaposi's sarcoma-associated herpesvirus infection from latency by expression of the ORF 50 transactivator, a homolog of the EBV R protein, Virology 252, 304-312 (1998). (Pubitemid 29013411)
35. P. J. Chang, D. Shedd & G. Miller, Two subclasses of Kaposi's sarcoma-associated herpesvirus lytic cycle promoters distinguished by open reading frame 50 mutant proteins that are deficient in binding to DNA, J.Virol. 79, 8750-8763 (2005). (Pubitemid 40934786)
36. H. Deng, M. J. Song, J. T. Chu & R. Sun, Transcriptional regulation of the interleukin-6 gene of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus), J.Virol. 76, 8252-8264 (2002). (Pubitemid 34809080)
37. M. J. Song, H. J. Brown, T. T. Wu & R. Sun, Transcription activation of polyadenylated nuclear rna by rta in human herpesvirus 8/Kaposi's sarcoma-associated herpesvirus, J.Virol. 75, 3129-3140 (2001). (Pubitemid 32225877)
38. D. M. Lukac, L. Garibyan, J. R. Kirshner, D. Palmeri & D. Ganem, DNA binding by Kaposi's sarcoma-associated herpesvirus lytic switch protein is necessary for transcriptional activation of two viral delayed early promoters, J.Virol. 75, 6786-6799 (2001). (Pubitemid 32641564)
39. M. J. Song, H. Deng & R. Sun, Comparative study of regulation of RTA-responsive genes in Kaposi's sarcoma associated herpesvirus/human herpesvirus 8, J.Virol. 77, 9451-9462 (2003). (Pubitemid 37011041)
40. D. J. Goodwin & A. Whitehouse, A gamma-2 herpesvirus nucleocytoplasmic shuttle protein interacts with importin alpha 1 and alpha 5, J.Biol.Chem. 276, 19905-19912 (2001).
41. E. Hiriart, L. Bardouillet, E. Manet, H. Gruffat, F. Penin, R. Montserret, G. Farjot & A. Sergeant, A region of the Epstein-Barr virus (EBV) mRNA export factor EB2 containing an arginine-rich motif mediates direct binding to RNA, J.Biol.Chem. 278, 37790-37798 (2003). (Pubitemid 37175306)
42. W. E. Mears, V. Lam & S. A. Rice, Identification of nuclear and nucleolar localization signals in the herpes simplex virus regulatory protein ICP27, J.Virol. 69, 935- 947 (1995).
43. M. K. Hibbard & R. M. Sandri-Goldin, Arginine-rich regions succeeding the nuclear localization region of the herpes simplex virus type 1 regulatory protein ICP27 are required for efficient nuclear localization and late gene expression, J.Virol. 69, 4656-4667 (1995).
44. S. M. Boyle, V. Ruvolo, A. K. Gupta & S. Swaminathan, Association with the cellular export receptor CRM 1 mediates function and intracellular localization of Epstein-Barr virus SM protein, a regulator of gene expression, J.Virol. 73, 6872-6881 (1999). (Pubitemid 29327870)
45. R. M. Sandri-Goldin, ICP27 mediates HSV RNA export by shuttling through a leucine-rich nuclear export signal and binding viral intronless RNAs through an RGG motif, Genes Dev. 12, 868-879 (1998). (Pubitemid 28150887)
46. J. R. Boyne & A. Whitehouse, Nucleolar trafficking is essential for nuclear export of intronless herpesvirus mRNA, Proc.Natl.Acad.Sci.U.S.A 103, 15190-15195 (2006). (Pubitemid 44583186)
47. V. Ruvolo, A. K. Gupta & S. Swaminathan, Epstein-Barr virus SM protein interacts with mRNA in vivo and mediates a gene-specific increase in cytoplasmic mRNA, J.Virol. 75, 6033-6041 (2001). (Pubitemid 32553134)
48. L. Aravind & D. Landsman, AT-hook motifs identified in a wide variety of DNA-binding proteins, Nucleic Acids Res. 26, 4413-4421 (1998). (Pubitemid 28442133)
49. P. J. Vaughan, K. J. Thibault, M. A. Hardwicke & R. M. Sandri-Goldin, The herpes simplex virus immediate early protein ICP27 encodes a potential metal binding domain and binds zinc in vitro, Virology 189, 377-384 (1992).
50. M. A. Hardwicke, P. J. Vaughan, R. E. Sekulovich, R. O'Conner & R. M. Sandri-Goldin, The regions important for the activator and repressor functions of herpes simplex virus type 1 alpha protein ICP27 map to the C-terminal half of the molecule, J.Virol. 63, 4590-4602 (1989). (Pubitemid 19257833)
51. S. A. Rice & D. M. Knipe, Gene-specific transactivation by herpes simplex virus type 1 alpha protein ICP27, J.Virol. 62, 3814-3823 (1988).
52. V. Ruvolo, L. Sun, K. Howard, S. Sung, H. J. Delecluse, W. Hammerschmidt & S. Swaminathan, Functional analysis of Epstein-Barr virus SM protein: identification of amino acids essential for structure, transactivation, splicing inhibition, and virion production, J.Virol. 78, 340-352 (2004). (Pubitemid 37549747)
53. P. Malik & J. B. Clements, Protein kinase CK2 phosphorylation regulates the interaction of Kaposi's sarcoma-associated herpesvirus regulatory protein ORF57 with its multifunctional partner hnRNP K, Nucleic Acids Res. 32, 5553-5569 (2004). (Pubitemid 39545673)
54. S. Wadd, H. Bryant, O. Filhol, J. E. Scott, T. Y. Hsieh, R. D. Everett & J. B. Clements, The multifunctional herpes simplex virus IE63 protein interacts with heterogeneous ribonucleoprotein K and with casein kinase 2, J.Biol.Chem. 274, 28991-28998 (1999).
55. C. Medina-Palazon, H. Gruffat, F. Mure, O. Filhol, V. Vingtdeux-Didier, H. Drobecq, C. Cochet, N. Sergeant, A. Sergeant & E. Manet, Protein kinase CK2 phosphorylation of EB2 regulates its function in the production of Epstein- Barr virus infectious viral particles, J.Virol. 81, 11850-11860 (2007). (Pubitemid 47623817)
56. Y. Zhi & R. M. Sandri-Goldin, Analysis of the phosphorylation sites of herpes simplex virus type 1 regulatory protein ICP27, J.Virol. 73, 3246-3257 (1999). (Pubitemid 29135717)
57. H. J. Dyson & P. E. Wright, Intrinsically unstructured proteins and their functions, Nat.Rev.Mol.Cell Biol. 6, 197- 208 (2005). (Pubitemid 40314921)
58. Z. Han & S. Swaminathan, Kaposi's sarcoma-associated herpesvirus lytic gene ORF57 is essential for infectious virion production, J.Virol. 80, 5251-5260 (2006).
59. P. Malik, D. J. Blackbourn & J. B. Clements, 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 (2004). (Pubitemid 39014760)
60. D. Longman, I. L. Johnstone & J. F. Caceres, The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans, RNA 9, 881-891 (2003). (Pubitemid 36734785)
61. M. MacMorris, C. Brocker & T. Blumenthal, UAP56 levels affect viability and mRNA export in Caenorhabditis elegans, RNA 9, 847-857 (2003). (Pubitemid 36734782)
62. D. Gatfield & E. Izaurralde, REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export, J.Cell Biol. 159, 579-588 (2002).
63. R. Sun, S. F. Lin, L. Gradoville & G. Miller, Polyadenylylated nuclear RNA encoded by Kaposi sarcoma-associated herpesvirus, Proc.Natl.Acad.Sci.U.S.A 93, 11883-11888 (1996). (Pubitemid 26347218)
64. M. L. Fenwick & J. Clark, Early and delayed shut-off of host protein synthesis in cells infected with herpes simplex virus, J.Gen.Virol. 61, 121-125 (1982). (Pubitemid 12003884)
65. B. Glaunsinger, L. Chavez & D. Ganem, The exonuclease and host shutoff functions of the SOX protein of Kaposi's sarcoma-associated herpesvirus are genetically separable, J.Virol. 79, 7396-7401 (2005). (Pubitemid 40756776)
66. H. E. Bryant, S. E. Wadd, A. I. Lamond, S. J. Silverstein & J. B. Clements, Herpes simplex virus IE63 (ICP27) protein interacts with spliceosome-associated protein 145 and inhibits splicing prior to the first catalytic step, J.Virol. 75, 4376-4385 (2001). (Pubitemid 32410149)
67. K. S. Sciabica, Q. J. Dai & R. M. Sandri-Goldin, ICP27 interacts with SRPK1 to mediate HSV splicing inhibition by altering SR protein phosphorylation, EMBO J. 22, 1608-1619 (2003). (Pubitemid 36417409)
68. M. A. Hardwicke & R. M. Sandri-Goldin, The herpes simplex virus regulatory protein ICP27 contributes to the decrease in cellular mRNA levels during infection, J.Virol. 68, 4797-4810 (1994). (Pubitemid 24226544)
69. A. Phelan, J. Dunlop & J. B. Clements, Herpes simplex virus type 1 protein IE63 affects the nuclear export of virus intron-containing transcripts, J.Virol. 70, 5255-5265 (1996). (Pubitemid 26240698)
70. Z. M. Zheng, Split genes and their expression in Kaposi's sarcoma-associated herpesvirus, Rev.Med.Virol. 13, 173-184 (2003).
71. P. Uetz, Y. A. Dong, C. Zeretzke, C. Atzler, A. Baiker, B. Berger, S. V. Rajagopala, M. Roupelieva, D. Rose, E. Fossum & J. Haas, Herpesviral protein networks and their interaction with the human proteome, Science 311, 239-242 (2006). (Pubitemid 43108191)
72. M. Kiledjian, X. Wang & S. A. Liebhaber, Identification of two KH domain proteins in the alphaglobin mRNP stability complex, EMBO J. 14, 4357-4364 (1995).
73. A. Ostareck-Lederer, D. H. Ostareck & M. W. Hentze, Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2, Trends Biochem.Sci. 23, 409-411 (1998). (Pubitemid 28540737)
74. A. V. Makeyev & S. A. Liebhaber, The poly (C)- binding proteins: a multiplicity of functions and a search for mechanisms, RNA 8, 265-278 (2002). (Pubitemid 34311177)
75. O. Larralde, R. W. Smith, G. S. Wilkie, P. Malik, N. K. Gray & J. B. Clements, Direct stimulation of translation by the multifunctional herpesvirus ICP27 protein, J.Virol. 80, 1588-1591 (2006). (Pubitemid 43134114)
76. Z. Toth, P. Lischka & T. Stamminger, RNA-binding of the human cytomegalovirus transactivator protein UL69, mediated by arginine-rich motifs, is not required for nuclear export of unspliced RNA, Nucleic Acids Res. 34, 1237-1249 (2006).
77. M. H. Malim, L. S. Tiley, D. F. McCarn, J. R. Rusche, J. Hauber & B. R. Cullen, HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence, Cell 60, 675-683 (1990).
78. B. J. Calnan, S. Biancalana, D. Hudson & A. D. Frankel, Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features of RNA-protein recognition, Genes Dev. 5, 201-210 (1991). (Pubitemid 21905945)
79. D. Lazinski, E. Grzadzielska & A. Das, Sequencespecific recognition of RNA hairpins by bacteriophage antiterminators requires a conserved arginine-rich motif, Cell 59, 207-218 (1989). (Pubitemid 19248570)
80. K. Bomsztyk, O. Denisenko & J. Ostrowski, hnRNP K: one protein multiple processes, Bioessays 26, 629-638 (2004). (Pubitemid 38758340)
81. B. Glaunsinger & D. Ganem, Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover, Mol.Cell. 13, 713-723 (2004). (Pubitemid 38368128)
82. M. Rowe, B. Glaunsinger, L. D. van, J. Zuo, D. Sweetman, D. Ganem, J. Middeldorp, E. J. Wiertz & M. E. Ressing, Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion, Proc.Natl.Acad.Sci.U.S.A 104, 3366-3371 (2007). (Pubitemid 46364165)
83. K. Bryson, L. J. McGuffin, R. L. Marsden, J. J. Ward, J. S. Sodhi & D. T. Jones, Protein structure prediction servers at University College London, Nucleic Acids Res. 33, W36-W38 (2005). (Pubitemid 44529876)
84. C. Zimmer, A. von Gabain & T. Henics, Analysis of sequence-specific binding of RNA to Hsp70 and its various homologs indicates the involvement of N- and C-terminal interactions, RNA 7, 1628-1637 (2001). (Pubitemid 33078937)