Interplay between polyadenylate-binding protein 1 and Kaposi's sarcoma-associated herpesvirus ORF57 in accumulation of polyadenylated nuclear RNA, a viral long noncoding RNA

Journal of Virology

Volumn 87, Issue 1, 2013, Pages 243-256

  Massimelli, Maria J ^a   Majerciak, Vladimir ^a   Kruhlak, Michael ^a   Zheng, Zhi Ming ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; E1B PROTEIN; NUCLEAR RNA; POLYADENYLIC ACID BINDING PROTEIN CYTOPLASMIC 1; PROTEIN ORF5; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; HUMAN HERPESVIRUS 8; INHIBITION KINETICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STEADY STATE; UPREGULATION; VIRUS INFECTIVITY;

CELL LINE; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; POLY(A)-BINDING PROTEIN I; PROTEIN BINDING; RNA, LONG UNTRANSLATED; RNA, NUCLEAR; VIRAL PROTEINS;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8;

EID: 84871992043     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01693-12     Document Type: Article

References (72)

1. Grange T, de Sa CM, Oddos J, Pictet R. 1987. Human mRNA polyadenylate binding protein: evolutionary conservation of a nucleic acid binding motif. Nucleic Acids Res. 15:4771-4787.
2. Huntzinger E, Braun JE, Heimstadt S, Zekri L, Izaurralde E. 2010. Two PABPC1-binding sites in GW182 proteins promote miRNA-mediated gene silencing. EMBO J. 29:4146-4160.
3. Lemay JF, Lemieux C, St. Andre O, Bachand F. 2010. Crossing the borders: poly(A)-binding proteins working on both sides of the fence. RNA Biol. 7:291-295.
4. Smith RW, Gray NK. 2010. Poly(A)-binding protein (PABP): a common viral target. Biochem. J. 426:1-12.
5. Walters RW, Bradrick SS, Gromeier M. 2010. Poly(A)-binding protein modulates mRNA susceptibility to cap-dependent miRNA-mediated repression. RNA 16:239-250.
6. Bag J, Bhattacharjee RB. 2010. Multiple levels of post-transcriptional control of expression of the poly (A)-binding protein. RNA Biol. 7:5-12.
7. Derry MC, Yanagiya A, Martineau Y, Sonenberg N. 2006. Regulation of poly(A)-binding protein through PABP-interacting proteins. Cold Spring Harbor Symp. Quant. Biol. 71:537-543.
8. Hinnebusch AG. 2011. Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 75:434-467.
9. Kahvejian A, Roy G, Sonenberg N. 2001. The mRNA closed-loop model: the function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harbor Symp. Quant. Biol. 66:293-300.
10. Kuhn U, Wahle E. 2004. Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta 1678:67-84.
11. Behm-Ansmant I, Gatfield D, Rehwinkel J, Hilgers V, Izaurralde E. 2007. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J. 26:1591-1601.
12. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27:736-747.
13. Singh G, Rebbapragada I, Lykke-Andersen J. 2008. A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 6:e111. doi:10.1371/ journal.pbio.0060111.
14. Zekri L, Huntzinger E, Heimstadt S, Izaurralde E. 2009. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol. Cell. Biol. 29:6220-6231.
15. Ding L, Han M. 2007. GW182 family proteins are crucial for microRNAmediated gene silencing. Trends Cell Biol. 17:411-416.
16. Afonina E, Stauber R, Pavlakis GN. 1998. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J. Biol. Chem. 273:13015-13021.
17. Hosoda N, Lejeune F, Maquat LE. 2006. Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell. Biol. 26: 3085-3097.
18. Burgess HM, Richardson WA, Anderson RC, Salaun C, Graham SV, Gray NK. 2011. Nuclear relocalisation of cytoplasmic poly(A)-binding proteins PABP1 and PABP4 in response to UV irradiation reveals mRNAdependent export of metazoan PABPs. J. Cell Sci. 124:3344-3355.
19. Uchida N, Hoshino S, Katada T. 2004. Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J. Biol. Chem. 279:1383-1391.
20. Ezzeddine N, Chang TC, Zhu W, Yamashita A, Chen CY, Zhong Z, Yamashita Y, Zheng D, Shyu AB. 2007. Human TOB, an antiproliferative transcription factor, is a poly(A)-binding protein-dependent positive regulator of cytoplasmic mRNA deadenylation. Mol. Cell. Biol. 27:7791-7801.
21. Okochi K, Suzuki T, Inoue J, Matsuda S, Yamamoto T. 2005. Interaction of anti-proliferative protein Tob with poly(A)-binding protein and inducible poly(A)-binding protein: implication of Tob in translational control. Genes Cells 10:151-163.
22. Funakoshi Y, Doi Y, Hosoda N, Uchida N, Osawa M, Shimada I, Tsujimoto M, Suzuki T, Katada T, Hoshino S. 2007. Mechanism of mRNA deadenylation: evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev. 21: 3135-3148.
23. Blakqori G, Kvan I, Elliott RM. 2009. Bunyamwera orthobunyavirus S-segment untranslated regions mediate poly(A) tail-independent translation. J. Virol. 83:3637-3646.
24. Covarrubias S, Richner JM, Clyde K, Lee YJ, Glaunsinger BA. 2009. Host shutoff is a conserved phenotype of gammaherpesvirus infection and is orchestrated exclusively from the cytoplasm. J. Virol. 83:9554-9566.
25. Dobrikova E, Shveygert M, Walters R, Gromeier M. 2010. Herpes simplex virus proteins ICP27 and UL47 associate with polyadenylatebinding protein and control its subcellular distribution. J. Virol. 84:270-279.
26. Harb M, Becker MM, Vitour D, Baron CH, Vende P, Brown SC, Bolte S, Arold ST, Poncet D. 2008. Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J. Virol. 82:11283-11293.
27. Kumar GR, Glaunsinger BA. 2010. Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Mol. Cell. Biol. 30:4996-5008.
28. Lee YJ, Glaunsinger BA. 2009. Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol. 7:e1000107. doi:10.1371/journal.pbio.1000107.
29. Salaun C, MacDonald AI, Larralde O, Howard L, Lochtie K, Burgess HM, Brook M, Malik P, Gray NK, Graham SV. 2010. Poly(A)-binding protein 1 partially relocalizes to the nucleus during herpes simplex virus type 1 infection in an ICP27-independent manner and does not inhibit virus replication. J. Virol. 84:8539-8548.
30. Alvarez E, Castello A, Menendez-Arias L, Carrasco L. 2006. HIV protease cleaves poly(A)-binding protein. Biochem. J. 396:219-226.
31. Bushell M, Sarnow P. 2002. Hijacking the translation apparatus by RNA viruses. J. Cell Biol. 158:395-399.
32. Gorgoni B, Gray NK. 2004. The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective. Brief. Funct. Genomic. Proteomic. 3:125-141.
33. Joachims M, Van Breugel PC, Lloyd RE. 1999. Cleavage of poly(A)- binding protein by enterovirus proteases concurrent with inhibition of translation in vitro. J. Virol. 73:718-727.
34. Kerekatte V, Keiper BD, Badorff C, Cai A, Knowlton KU, Rhoads RE. 1999. Cleavage of poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff? J. Virol. 73:709-717.
35. Kuyumcu-Martinez M, Belliot G, Sosnovtsev SV, Chang KO, Green KY, Lloyd RE. 2004. Calicivirus 3C-like proteinase inhibits cellular translation by cleavage of poly(A)-binding protein. J. Virol. 78:8172-8182.
36. Kuyumcu-Martinez NM, Joachims M, Lloyd RE. 2002. Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease. J. Virol. 76:2062-2074.
37. Kuyumcu-Martinez NM, Van Eden ME, Younan P, Lloyd RE. 2004. Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol. Cell. Biol. 24:1779-1790.
38. Rivera CI, Lloyd RE. 2008. Modulation of enteroviral proteinase cleavage of poly(A)-binding protein (PABP) by conformation and PABPassociated factors. Virology 375:59-72.
39. Arias C, Walsh D, Harbell J, Wilson AC, Mohr I. 2009. Activation of host translational control pathways by a viral developmental switch. PLoS Pathog. 5:e1000334. doi:10.1371/journal.ppat.1000334.
40. Kanno T, Sato Y, Sata T, Katano H. 2006. Expression of Kaposi's sarcoma-associated herpesvirus-encoded K10/10.1 protein in tissues and its interaction with poly(A)-binding protein. Virology 352:100-109.
41. Glaunsinger B, Ganem D. 2004. Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol. Cell 13:713-723.
42. Bagneris C, Briggs LC, Savva R, Ebrahimi B, Barrett TE. 2011. Crystal structure of a KSHV-SOX-DNA complex: insights into the molecular mechanisms underlying DNase activity and host shutoff. Nucleic Acids Res. 39:5744-5756.
43. Glaunsinger B, Chavez L, Ganem D. 2005. The exonuclease and host shutoff functions of the SOX protein of Kaposi's sarcoma-associated herpesvirus are genetically separable. J. Virol. 79:7396-7401.
44. Bello LJ, Davison AJ, Glenn MA, Whitehouse A, Rethmeier N, Schulz TF, Barklie CJ. 1999. The human herpesvirus-8 ORF 57 gene and its properties. J. Gen. Virol. 80:3207-3215.
45. Gupta AK, Ruvolo V, Patterson C, Swaminathan S. 2000. 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.
46. Kirshner JR, Lukac DM, Chang J, Ganem D. 2000. Kaposi's sarcomaassociated herpesvirus open reading frame 57 encodes a posttranscriptional regulator with multiple distinct activities. J. Virol. 74:3586-3597.
47. Majerciak V, Yamanegi K, Nie SH, Zheng ZM. 2006. Structural and functional analyses of Kaposi sarcoma-associated herpesvirus ORF57 nuclear localization signals in living cells. J. Biol. Chem. 281:28365-28378.
48. Nekorchuk M, Han Z, Hsieh TT, Swaminathan S. 2007. Kaposi's sarcoma- associated herpesvirus ORF57 protein enhances mRNA accumulation independently of effects on nuclear RNA export. J. Virol. 81:9990-9998.
49. Majerciak V, Kruhlak M, Dagur PK, McCoy JP, Jr, Zheng ZM. 2010. Caspase-7 cleavage of Kaposi sarcoma-associated herpesvirus ORF57 confers a cellular function against viral lytic gene expression. J. Biol. Chem. 285:11297-11307.
50. Majerciak V, Yamanegi K, Allemand E, Kruhlak M, Krainer AR, Zheng ZM. 2008. 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.
51. Massimelli MJ, Kang JG, Majerciak V, Le SY, Liewehr DJ, Steinberg SM, Zheng ZM. 2011. Stability of a long noncoding viral RNA depends on a 9-nt core element at the RNA 5= end to interact with viral ORF57 and cellular PABPC1. Int. J. Biol. Sci. 7:1145-1160.
52. Sei E, Conrad NK. 2011. Delineation of a core RNA element required for Kaposi's sarcoma-associated herpesvirus ORF57 binding and activity. Virology 419:107-116.
53. Borah S, Darricarrere N, Darnell A, Myoung J, Steitz JA. 2011. A viral nuclear noncoding RNA binds re-localized poly(A) binding protein and is required for late KSHV gene expression. PLoS Pathog. 7:e1002300. doi: 10.1371/journal.ppat.1002300.
54. Rossetto CC, Pari G. 2012. KSHV PAN RNA associates with demethylases UTX and JMJD3 to activate lytic replication through a physical interaction with the virus genome. PLoS Pathog. 8:e1002680. doi:10.1371/ journal.ppat.1002680.
55. Rossetto CC, Pari GS. 2011. KSHV noncoding PAN RNA interacts with virus and cellular-encoded proteins and suppresses expression of genes involved in immune modulation. J. Virol. 85:13290-13297.
56. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, Jung JU. 2003. Global changes in Kaposi's sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J. Virol. 77:4205-4220.
57. Majerciak V, Pripuzova N, McCoy JP, Gao SJ, Zheng ZM. 2007. Targeted disruption of Kaposi's sarcoma-associated 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.
58. Majerciak V, Yamanegi K, Zheng ZM. 2006. Gene structure and expression of Kaposi's sarcoma-associated herpesvirus ORF56, ORF57, ORF58, and ORF59. J. Virol. 80:11968-11981.
59. Jia R, Liu X, Tao M, Kruhlak M, Guo M, Meyers C, Baker CC, Zheng ZM. 2009. Control of the papillomavirus early-to-late switch by differentially expressed SRp20. J. Virol. 83:167-180.
60. Kang JG, Pripuzova N, Majerciak V, Kruhlak M, Le SY, Zheng ZM. 2011. Kaposi's sarcoma-associated herpesvirus ORF57 promotes escape of viral and human interleukin-6 from microRNA-mediated suppression. J. Virol. 85:2620-2630.
61. Yong J, Golembe TJ, Battle DJ, Pellizzoni L, Dreyfuss G. 2004. snRNAs contain specific SMN-binding domains that are essential for snRNP assembly. Mol. Cell. Biol. 24:2747-2756.
62. Majerciak V, Uranishi H, Kruhlak M, Pilkington GR, Massimelli MJ, Bear J, Pavlakis GN, Felber BK, Zheng ZM. 2011. Kaposi's sarcomaassociated herpesvirus ORF57 interacts with cellular RNA export cofactors RBM15 and OTT3 to promote expression of viral ORF59. J. Virol. 85:1528-1540.
63. Majerciak V, Zheng ZM. 2009. Kaposi's sarcoma-associated herpesvirus ORF57 in viral RNA processing. Front. Biosci. 14:1516-1528.
64. Bachi A, Braun IC, Rodrigues JP, Pante N, Ribbeck K, von Kobbe C, Kutay U, Wilm M, Gorlich D, Carmo-Fonseca M, 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.
65. Barral PM, Rusch A, Turnell AS, Gallimore PH, Byrd PJ, Dobner T, Grand RJ. 2005. The interaction of the hnRNP family member E1B-AP5 with p53. FEBS Lett. 579:2752-2758.
66. Blackford AN, Bruton RK, Dirlik O, Stewart GS, Taylor AM, Dobner T, Grand RJ, Turnell AS. 2008. A role for E1B-AP5 in ATR signaling pathways during adenovirus infection. J. Virol. 82:7640-7652.
67. Gabler S, Schutt H, Groitl P, Wolf H, Shenk T, Dobner T. 1998. E1B 55-kilodalton-associated protein: a cellular protein with RNA-binding activity implicated in nucleocytoplasmic transport of adenovirus and cellular mRNAs. J. Virol. 72:7960-7971.
68. Kzhyshkowska J, Rusch A, Wolf H, Dobner T. 2003. Regulation of transcription by the heterogeneous nuclear ribonucleoprotein E1B-AP5 is mediated by complex formation with the novel bromodomain-containing protein BRD7. Biochem. J. 371:385-393.
69. Kozlov G, Gehring K. 2010. Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein. PLoS One 5:e10169. doi: 10.1371/journal.pone.0010169.
70. Zhouravleva G, Frolova L, Le GX, Le GR, Inge-Vechtomov S, Kisselev L, Philippe M. 1995. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 14:4065-4072.
71. Bag J. 2001. Feedback inhibition of poly(A)-binding protein mRNA translation. A possible mechanism of translation arrest by stalled 40 S ribosomal subunits. J. Biol. Chem. 276:47352-47360.
72. Boyne JR, Colgan KJ, Whitehouse A. 2008. Recruitment of the complete hTREX complex is required for Kaposi's sarcoma-associated herpesvirus intronless mRNA nuclear export and virus replication. PLoS Pathog. 4:e1000194. doi:10.1371/journal.ppat.1000194.