Coordinated Destruction of Cellular Messages in Translation Complexes by the Gammaherpesvirus Host Shutoff Factor and the Mammalian Exonuclease Xrn1

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Several viruses encode factors that promote host mRNA degradation to silence gene expression. It is unclear, however, whether cellular mRNA turnover pathways are engaged to assist in this process. In Kaposi's sarcoma-associated herpesvirus this phenotype is enacted by the host shutoff factor SOX. Here we show that SOX-induced mRNA turnover is a two-step process, in which mRNAs are first cleaved internally by SOX itself then degraded by the cellular exonuclease Xrn1. SOX therefore bypasses the regulatory steps of deadenylation and decapping normally required for Xrn1 activation. SOX is likely recruited to translating mRNAs, as it cosediments with translation initiation complexes and depletes polysomes. Cleaved mRNA intermediates accumulate in the 40S fraction, indicating that recognition occurs at an early stage of translation. This is the first example of a viral protein commandeering cellular mRNA turnover pathways to destroy host mRNAs, and suggests that Xrn1 is poised to deplete messages undergoing translation in mammalian cells.

Vyšlo v časopise: Coordinated Destruction of Cellular Messages in Translation Complexes by the Gammaherpesvirus Host Shutoff Factor and the Mammalian Exonuclease Xrn1. PLoS Pathog 7(10): e32767. doi:10.1371/journal.ppat.1002339
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002339

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1. GrahamJRHendershottMCTerragniJCooperGM 2010 mRNA degradation plays a significant role in the program of gene expression regulated by phosphatidylinositol 3-kinase signaling. Mol Cell Biol 30 5295 5305

2. FanJYangXWangWWoodWH3rdBeckerKG 2002 Global analysis of stress-regulated mRNA turnover by using cDNA arrays. Proc Natl Acad Sci U S A 99 10611 10616

3. CheadleCFanJCho-ChungYSWernerTRayJ 2005 Control of gene expression during T cell activation: alternate regulation of mRNA transcription and mRNA stability. BMC Genomics 6 75

4. BelascoJG 2010 All things must pass: contrasts and commonalities in eukaryotic and bacterial mRNA decay. Nat Rev Mol Cell Biol 11 467 478

5. GarneauNLWiluszJWiluszCJ 2007 The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8 113 126

6. DeckerCJParkerR 1993 A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev 7 1632 1643

7. MuhlradDDeckerCJParkerR 1994 Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′–>3′ digestion of the transcript. Genes Dev 8 855 866

8. DunckleyTParkerR 1999 The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 18 5411 5422

9. WangZJiaoXCarr-SchmidAKiledjianM 2002 The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc Natl Acad Sci U S A 99 12663 12668

10. TomeckiRDziembowskiA 2010 Novel endoribonucleases as central players in various pathways of eukaryotic RNA metabolism. RNA 16 1692 1724

11. GagliaMMGlaunsingerB 2010 Viruses and the cellular RNA decay machinery. Wiley Interdisciplinary Reviews: RNA 1 47 59

12. SokoloskiKJDicksonAMChaskeyELGarneauNLWiluszCJ 2010 Sindbis virus usurps the cellular HuR protein to stabilize its transcripts and promote productive infections in mammalian and mosquito cells. Cell Host Microbe 8 196 207

13. UmbachJLCullenBR 2009 The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev 23 1151 1164

14. PijlmanGPFunkAKondratievaNLeungJTorresS 2008 A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4 579 591

15. RoweMGlaunsingerBvan LeeuwenDZuoJSweetmanD 2007 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

16. KwongADKruperJAFrenkelN 1988 Herpes simplex virus virion host shutoff function. J Virol 62 912 921

17. KamitaniWNarayananKHuangCLokugamageKIkegamiT 2006 Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci U S A 103 12885 12890

18. GlaunsingerBGanemD 2004 Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol Cell 13 713 723

19. ChangYCesarmanEPessinMSLeeFCulpepperJ 1994 Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266 1865 1869

20. SoulierJGrolletLOksenhendlerECacoubPCazals-HatemD 1995 Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86 1276 1280

21. CesarmanEChangYMoorePSSaidJWKnowlesDM 1995 Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332 1186 1191

22. GlaunsingerBGanemD 2004 Highly selective escape from KSHV-mediated host mRNA shutoff and its implications for viral pathogenesis. J Exp Med 200 391 398

23. CovarrubiasSRichnerJMClydeKLeeYJGlaunsingerBA 2009 Host shutoff is a conserved phenotype of gammaherpesvirus infection and is orchestrated exclusively from the cytoplasm. J Virol 83 9554 9566

24. ClydeKGlaunsingerB 2011 Deep sequencing reveals direct targets of gammaherpesvirus-induced mRNA decay and suggests that multiple mechanisms govern cellular transcript escape. PLoS One 6 e19655

25. LeeYJGlaunsingerBA 2009 Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol 7 e1000107

26. KumarGRShumLGlaunsingerBA 2011 Importin {alpha}-Mediated Nuclear Import of Cytoplasmic Poly(A) Binding Protein Occurs as a Direct Consequence of Cytoplasmic mRNA Depletion. Mol Cell Biol 31 3113 3125

27. KumarGRGlaunsingerBA 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. BagnerisCBriggsLCSavvaREbrahimiBBarrettTE 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

29. KnopfCWWeisshartK 1990 Comparison of exonucleolytic activities of herpes simplex virus type-1 DNA polymerase and DNase. Eur J Biochem 191 263 273

30. BuissonMGeouiTFlotDTarbouriechNRessingME 2009 A bridge crosses the active-site canyon of the Epstein-Barr virus nuclease with DNase and RNase activities. J Mol Biol 391 717 728

31. HoffmannPJChengYC 1978 The deoxyribonuclease induced after infection of KB cells by herpes simplex virus type 1 or type 2. I. Purification and characterization of the enzyme. J Biol Chem 253 3557 3562

32. BaylisSAPurifoyDJLittlerE 1989 The characterization of the EBV alkaline deoxyribonuclease cloned and expressed in E. coli. Nucleic Acids Res 17 7609 7622

33. GlaunsingerBChavezLGanemD 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

34. OzgurSChekulaevaMStoecklinG 2010 Human Pat1b connects deadenylation with mRNA decapping and controls the assembly of processing bodies. Mol Cell Biol 30 4308 4323

35. SongMGLiYKiledjianM 2010 Multiple mRNA decapping enzymes in mammalian cells. Mol Cell 40 423 432

36. EberleABLykke-AndersenSMuhlemannOJensenTH 2009 SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16 49 55

37. HuntzingerEKashimaIFauserMSauliereJIzaurraldeE 2008 SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14 2609 2617

38. HoffmannPJChengYC 1979 DNase induced after infection of KB cells by herpes simplex virus type 1 or type 2. II. Characterization of an associated endonuclease activity. J Virol 32 449 457

39. StolzenbergMCOokaT 1990 Purification and properties of Epstein-Barr virus DNase expressed in Escherichia coli. J Virol 64 96 104

40. SheafferAKWeinheimerSPTenneyDJ 1997 The human cytomegalovirus UL98 gene encodes the conserved herpesvirus alkaline nuclease. J Gen Virol 78 Pt 11 2953 2961

41. DahlrothSLGurmuDHaasJErlandsenHNordlundP 2009 Crystal structure of the shutoff and exonuclease protein from the oncogenic Kaposi's sarcoma-associated herpesvirus. FEBS J 276 6636 6645

42. GatfieldDIzaurraldeE 2004 Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429 575 578

43. IshigakiYLiXSerinGMaquatLE 2001 Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106 607 617

44. HendricksonDGHoganDJMcCulloughHLMyersJWHerschlagD 2009 Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol 7 e1000238

45. NakamuraHLuMGwackYSouvlisJZeichnerSL 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

46. RiveraCILloydRE 2008 Modulation of enteroviral proteinase cleavage of poly(A)-binding protein (PABP) by conformation and PABP-associated factors. Virology 375 59 72

47. ChenCYSarnowP 1995 Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 268 415 417

48. de Melo NetoOPStandartNMartins de SaC 1995 Autoregulation of poly(A)-binding protein synthesis in vitro. Nucleic Acids Res 23 2198 2205

49. DomaMKParkerR 2006 Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440 561 564

50. MeisterGLandthalerMPatkaniowskaADorsettYTengG 2004 Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15 185 197

51. HollienJWeissmanJS 2006 Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 104 107

52. HanDLernerAGVande WalleLUptonJPXuW 2009 IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138 562 575

53. LebretonATomeckiRDziembowskiASeraphinB 2008 Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456 993 996

54. SchneiderCLeungEBrownJTollerveyD 2009 The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37 1127 1140

55. SchaefferDTsanovaBBarbasAReisFPDastidarEG 2009 The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16 56 62

56. ChenCYXuNShyuAB 1995 mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol Cell Biol 15 5777 5788

57. MorinBCoutardBLelkeMFerronFKerberR 2010 The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog 6 e1001038 doi:1001010.1001371/journal.ppat.1001038

58. YuanPBartlamMLouZChenSZhouJ 2009 Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458 909 913

59. YangXCSullivanKDMarzluffWFDominskiZ 2009 Studies of the 5′ exonuclease and endonuclease activities of CPSF-73 in histone pre-mRNA processing. Mol Cell Biol 29 31 42

60. MathyNBenardLPellegriniODaouRWenT 2007 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129 681 692

61. CarpousisAJLuisiBFMcDowallKJ 2009 Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog Mol Biol Transl Sci 85 91 135

62. KamitaniWHuangCNarayananKLokugamageKGMakinoS 2009 A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat Struct Mol Biol 16 1134 1140

63. TaddeoBRoizmanB 2006 The virion host shutoff protein (UL41) of herpes simplex virus 1 is an endoribonuclease with a substrate specificity similar to that of RNase A. J Virol 80 9341 9345

64. TaddeoBZhangWRoizmanB 2006 The U(L)41 protein of herpes simplex virus 1 degrades RNA by endonucleolytic cleavage in absence of other cellular or viral proteins. Proc Natl Acad Sci U S A 103 2827 2832

65. ElgadiMMHayesCESmileyJR 1999 The herpes simplex virus vhs protein induces endoribonucleolytic cleavage of target RNAs in cell extracts. J Virol 73 7153 7164

66. ZelusBDStewartRSRossJ 1996 The virion host shutoff protein of herpes simplex virus type 1: messenger ribonucleolytic activity in vitro. J Virol 70 2411 2419

67. FengPEverlyDNJrReadGS 2005 mRNA decay during herpes simplex virus (HSV) infections: protein-protein interactions involving the HSV virion host shutoff protein and translation factors eIF4H and eIF4A. J Virol 79 9651 9664

68. FengPEverlyDNJrReadGS 2001 mRNA decay during herpesvirus infections: interaction between a putative viral nuclease and a cellular translation factor. J Virol 75 10272 10280

69. TaddeoBZhangWRoizmanB 2009 The virion-packaged endoribonuclease of herpes simplex virus 1 cleaves mRNA in polyribosomes. Proc Natl Acad Sci U S A 106 12139 12144

70. KhaleghpourKSvitkinYVCraigAWDeMariaCTDeoRC 2001 Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol Cell 7 205 216

71. JacksonAOLarkinsBA 1976 Influence of Ionic Strength, pH, and Chelation of Divalent Metals on Isolation of Polyribosomes from Tobacco Leaves. Plant Physiol 57 5 10