Noise Cancellation: Viral Fine Tuning of the Cellular Environment for Its Own Genome Replication
Productive replication of DNA viruses elicits host cell DNA damage responses, which cause both beneficial and detrimental effects on viral replication. In response to the viral productive replication, host cells attempt to attenuate the S-phase cyclin-dependent kinase (CDK) activities to inhibit viral replication. However, accumulating evidence regarding interactions between viral factors and cellular signaling molecules indicate that viruses utilize them and selectively block the downstream signaling pathways that lead to attenuation of the high S-phase CDK activities required for viral replication. In this review, we describe the sophisticated strategy of Epstein-Barr virus to cancel such “noisy” host defense signals in order to hijack the cellular environment.
Vyšlo v časopise:
Noise Cancellation: Viral Fine Tuning of the Cellular Environment for Its Own Genome Replication. PLoS Pathog 6(12): e32767. doi:10.1371/journal.ppat.1001158
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001158
Souhrn
Productive replication of DNA viruses elicits host cell DNA damage responses, which cause both beneficial and detrimental effects on viral replication. In response to the viral productive replication, host cells attempt to attenuate the S-phase cyclin-dependent kinase (CDK) activities to inhibit viral replication. However, accumulating evidence regarding interactions between viral factors and cellular signaling molecules indicate that viruses utilize them and selectively block the downstream signaling pathways that lead to attenuation of the high S-phase CDK activities required for viral replication. In this review, we describe the sophisticated strategy of Epstein-Barr virus to cancel such “noisy” host defense signals in order to hijack the cellular environment.
Zdroje
1. SancarA
Lindsey-BoltzLA
Unsal-KacmazK
LinnS
2004 Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73 39 85
2. RouseJ
JacksonSP
2002 Interfaces between the detection, signaling, and repair of DNA damage. Science 297 547 551
3. HaffnerR
OrenM
1995 Biochemical properties and biological effects of p53. Curr Opin Genet Dev 5 84 90
4. KoLJ
PrivesC
1996 p53: puzzle and paradigm. Genes Dev 10 1054 1072
5. StrackerTH
CarsonCT
WeitzmanMD
2002 Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418 348 352
6. DahlJ
YouJ
BenjaminTL
2005 Induction and utilization of an ATM signaling pathway by polyomavirus. J Virol 79 13007 13017
7. ShirataN
KudohA
DaikokuT
TatsumiY
FujitaM
2005 Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J Biol Chem 280 30336 30341
8. GasparM
ShenkT
2006 Human cytomegalovirus inhibits a DNA damage response by mislocalizing checkpoint proteins. Proc Natl Acad Sci U S A 103 2821 2826
9. KudohA
FujitaM
ZhangL
ShirataN
DaikokuT
2005 Epstein-Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phase-like cellular environment. J Biol Chem 280 8156 8163
10. YoungLS
RickinsonAB
2004 Epstein-Barr virus: 40 years on. Nat Rev Cancer 4 757 768
11. AdamsA
1987 Replication of latent Epstein-Barr virus genomes in Raji cells. J Virol 61 1743 1746
12. DaikokuT
KudohA
FujitaM
SugayaY
IsomuraH
2005 Architecture of replication compartments formed during Epstein-Barr virus lytic replication. J Virol 79 3409 3418
13. JoabI
NicolasJC
SchwaabG
de-TheG
ClausseB
1991 Detection of anti-Epstein-Barr-virus transactivator (ZEBRA) antibodies in sera from patients with nasopharyngeal carcinoma. Int J Cancer 48 647 649
14. FengWH
CohenJI
FischerS
LiL
SnellerM
2004 Reactivation of latent Epstein-Barr virus by methotrexate: a potential contributor to methotrexate-associated lymphomas. J Natl Cancer Inst 96 1691 1702
15. HammerschmidtW
SugdenB
1988 Identification and characterization of oriLyt, a lytic origin of DNA replication of Epstein-Barr virus. Cell 55 427 433
16. FlemingtonEK
GoldfeldAE
SpeckSH
1991 Efficient transcription of the Epstein-Barr virus immediate-early BZLF1 and BRLF1 genes requires protein synthesis. J Virol 65 7073 7077
17. KudohA
FujitaM
KiyonoT
KuzushimaK
SugayaY
2003 Reactivation of lytic replication from B cells latently infected with Epstein-Barr virus occurs with high S-phase cyclin-dependent kinase activity while inhibiting cellular DNA replication. J Virol 77 851 861
18. TsurumiT
FujitaM
KudohA
2005 Latent and lytic Epstein-Barr virus replication strategies. Rev Med Virol 15 3 15
19. LiM
ChenD
ShilohA
LuoJ
NikolaevAY
2002 Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416 648 653
20. SaridakisV
ShengY
SarkariF
HolowatyMN
ShireK
2005 Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol Cell 18 25 36
21. SivachandranN
SarkariF
FrappierL
2008 Epstein-Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog 4 e1000170
22. CayrolC
FlemingtonE
1996 G0/G1 growth arrest mediated by a region encompassing the basic leucine zipper (bZIP) domain of the Epstein-Barr virus transactivator Zta. J Biol Chem 271 31799 31802
23. CayrolC
FlemingtonEK
1996 The Epstein-Barr virus bZIP transcription factor Zta causes G0/G1 cell cycle arrest through induction of cyclin-dependent kinase inhibitors. EMBO J 15 2748 2759
24. MauserA
Holley-GuthrieE
SimpsonD
KaufmannW
KenneyS
2002 The Epstein-Barr virus immediate-early protein BZLF1 induces both a G(2) and a mitotic block. J Virol 76 10030 10037
25. MauserA
SaitoS
AppellaE
AndersonCW
SeamanWT
2002 The Epstein-Barr virus immediate-early protein BZLF1 regulates p53 function through multiple mechanisms. J Virol 76 12503 12512
26. SatoY
ShirataN
MurataT
NakasuS
KudohA
2010 Transient increases in p53-responsible gene expression at early stages of Epstein-Barr virus productive replication. Cell Cycle 9 807 814
27. ChangSS
LoYC
ChuaHH
ChiuHY
TsaiSC
2008 Critical role of p53 in histone deacetylase inhibitor-induced Epstein-Barr virus Zta expression. J Virol 82 7745 7751
28. Chevallier-GrecoA
ManetE
ChavrierP
MosnierC
DaillieJ
1986 Both Epstein-Barr virus (EBV)-encoded trans-acting factors, EB1 and EB2, are required to activate transcription from an EBV early promoter. EMBO J 5 3243 3249
29. HardwickJM
LiebermanPM
HaywardSD
1988 A new Epstein-Barr virus transactivator, R, induces expression of a cytoplasmic early antigen. J Virol 62 2274 2284
30. CasavantNC
LuoMH
RosenkeK
WinegardnerT
ZurawskaA
2006 Potential role for p53 in the permissive life cycle of human cytomegalovirus. J Virol 80 8390 8401
31. JaultFM
JaultJM
RuchtiF
FortunatoEA
ClarkC
1995 Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J Virol 69 6697 6704
32. RosenkeK
SamuelMA
McDowellET
ToerneMA
FortunatoEA
2006 An intact sequence-specific DNA-binding domain is required for human cytomegalovirus-mediated sequestration of p53 and may promote in vivo binding to the viral genome during infection. Virology 348 19 34
33. KudohA
DaikokuT
SugayaY
IsomuraH
FujitaM
2004 Inhibition of S-phase cyclin-dependent kinase activity blocks expression of Epstein-Barr virus immediate-early and early genes, preventing viral lytic replication. J Virol 78 104 115
34. KudohA
DaikokuT
IshimiY
KawaguchiY
ShirataN
2006 Phosphorylation of MCM4 at sites inactivating DNA helicase activity of the MCM4-MCM6-MCM7 complex during Epstein-Barr virus productive replication. J Virol 80 10064 10072
35. TarakanovaVL
Leung-PinedaV
HwangS
YangCW
MatatallK
2007 Gamma-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe 1 275 286
36. SatoY
ShirataN
KudohA
IwahoriS
NakayamaS
2009 Expression of Epstein-Barr virus BZLF1 immediate-early protein induces p53 degradation independent of MDM2, leading to repression of p53-mediated transcription. Virology 388 204 211
37. SatoY
KamuraT
ShirataN
MurataT
KudohA
2009 Degradation of Phosphorylated p53 by Viral Protein-ECS E3 Ligase Complex. PLoS Pathog 5 e1000530
38. DengZ
ChenCJ
ZerbyD
DelecluseHJ
LiebermanPM
2001 Identification of acidic and aromatic residues in the Zta activation domain essential for Epstein-Barr virus reactivation. J Virol 75 10334 10347
39. OuYH
ChungPH
SunTP
ShiehSY
2005 p53 C-terminal phosphorylation by CHK1 and CHK2 participates in the regulation of DNA-damage-induced C-terminal acetylation. Mol Biol Cell 16 1684 1695
40. KudohA
IwahoriS
SatoY
NakayamaS
IsomuraH
2009 Homologous recombinational repair factors are recruited and loaded onto the viral DNA genome in Epstein-Barr virus replication compartments. J Virol 83 6641 6651
41. FortunatoEA
SpectorDH
1998 p53 and RPA are sequestered in viral replication centers in the nuclei of cells infected with human cytomegalovirus. J Virol 72 2033 2039
42. HsuCH
ChangMD
TaiKY
YangYT
WangPS
2004 HCMV IE2-mediated inhibition of HAT activity downregulates p53 function. EMBO J 23 2269 2280
43. WilcockD
LaneDP
1991 Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349 429 431
44. WenW
IwakiriD
YamamotoK
MaruoS
KandaT
2007 Epstein-Barr virus BZLF1 gene, a switch from latency to lytic infection, is expressed as an immediate-early gene after primary infection of B lymphocytes. J Virol 81 1037 1042
45. HalderS
MurakamiM
VermaSC
KumarP
YiF
2009 Early events associated with infection of Epstein-Barr virus infection of primary B-cells. PLoS One 4 e7214
46. KallaM
SchmeinckA
BergbauerM
PichD
HammerschmidtW
2010 AP-1 homolog BZLF1 of Epstein-Barr virus has two essential functions dependent on the epigenetic state of the viral genome. Proc Natl Acad Sci U S A 107 850 855
47. HongH
TakahashiK
IchisakaT
AoiT
KanagawaO
2009 Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460 1132 1135
48. LiH
ColladoM
VillasanteA
StratiK
OrtegaS
2009 The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460 1136 1139
49. KawamuraT
SuzukiJ
WangYV
MenendezS
MoreraLB
2009 Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460 1140 1144
50. UtikalJ
PoloJM
StadtfeldM
MaheraliN
KulalertW
2009 Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460 1145 1148
51. MarionRM
StratiK
LiH
MurgaM
BlancoR
2009 A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460 1149 1153
52. NakayamaKI
NakayamaK
2006 Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 6 369 381
53. PetroskiMD
DeshaiesRJ
2005 Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6 9 20
54. KraftC
VodermaierHC
Maurer-StrohS
EisenhaberF
PetersJM
2005 The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol Cell 18 543 553
55. SpruckC
StrohmaierH
WatsonM
SmithAP
RyanA
2001 A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol Cell 7 639 650
56. HaoB
ZhengN
SchulmanBA
WuG
MillerJJ
2005 Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase. Mol Cell 20 9 19
57. HarperJW
BurtonJL
SolomonMJ
2002 The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev 16 2179 2206
58. SkowyraD
CraigKL
TyersM
ElledgeSJ
HarperJW
1997 F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91 209 219
59. CarranoAC
EytanE
HershkoA
PaganoM
1999 SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1 193 199
60. SutterlutyH
ChatelainE
MartiA
WirbelauerC
SenftenM
1999 p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1 207 214
61. TsvetkovLM
YehKH
LeeSJ
SunH
ZhangH
1999 p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr Biol 9 661 664
62. MannDJ
ChildES
SwantonC
LamanH
JonesN
1999 Modulation of p27(Kip1) levels by the cyclin encoded by Kaposi's sarcoma-associated herpesvirus. EMBO J 18 654 663
63. EllisM
ChewYP
FallisL
FreddersdorfS
BoshoffC
1999 Degradation of p27(Kip) cdk inhibitor triggered by Kaposi's sarcoma virus cyclin-cdk6 complex. EMBO J 18 644 653
64. YarmishynA
ChildES
ElphickLM
MannDJ
2008 Differential regulation of the cyclin-dependent kinase inhibitors p21(Cip1) and p27(Kip1) by phosphorylation directed by the cyclin encoded by Murine Herpesvirus 68. Exp Cell Res 314 204 212
65. IwahoriS
MurataT
KudohA
SatoY
NakayamaS
2009 Phosphorylation of p27Kip1 by Epstein-Barr Virus Protein Kinase Induces Its Degradation through SCFSkp2 Ubiquitin Ligase Actions during Viral Lytic Replication. J Biol Chem 284 18923 18931
66. WhitehurstCB
NingS
BentzGL
DufourF
GershburgE
2009 The Epstein-Barr virus (EBV) deubiquitinating enzyme BPLF1 reduces EBV ribonucleotide reductase activity. J Virol 83 4345 4353
67. GastaldelloS
HildebrandS
FaridaniO
CallegariS
PalmkvistM
2010 A deneddylase encoded by Epstein-Barr virus promotes viral DNA replication by regulating the activity of cullin-RING ligases. Nat Cell Biol 12 351 361
68. RabutG
PeterM
2008 Function and regulation of protein neddylation. ‘Protein modifications: beyond the usual suspects’ review series. EMBO Rep 9 969 976
69. SompallaeR
GastaldelloS
HildebrandS
ZininN
HassinkG
2008 Epstein-barr virus encodes three bona fide ubiquitin-specific proteases. J Virol 82 10477 10486
70. BornsteinG
BloomJ
Sitry-ShevahD
NakayamaK
PaganoM
2003 Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J Biol Chem 278 25752 25757
71. GottweinE
CullenBR
2010 A human herpesvirus microRNA inhibits p21 expression and attenuates p21-mediated cell cycle arrest. J Virol 84 5229 5237
72. AdamsPD
KaelinWGJr
1995 Transcriptional control by E2F. Semin Cancer Biol 6 99 108
73. LiuC
SistaND
PaganoJS
1996 Activation of the Epstein-Barr virus DNA polymerase promoter by the BRLF1 immediate-early protein is mediated through USF and E2F. J Virol 70 2545 2555
74. MauserA
Holley-GuthrieE
ZanationA
YarboroughW
KaufmannW
2002 The Epstein-Barr virus immediate-early protein BZLF1 induces expression of E2F-1 and other proteins involved in cell cycle progression in primary keratinocytes and gastric carcinoma cells. J Virol 76 12543 12552
75. SwensonJJ
MauserAE
KaufmannWK
KenneySC
1999 The Epstein-Barr virus protein BRLF1 activates S phase entry through E2F1 induction. J Virol 73 6540 6550
76. LinWC
LinFT
NevinsJR
2001 Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev 15 1833 1844
77. StevensC
SmithL
La ThangueNB
2003 Chk2 activates E2F-1 in response to DNA damage. Nat Cell Biol 5 401 409
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 12
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- HIV-1 Envelope Subregion Length Variation during Disease Progression
- Coming of Age—Sexual Reproduction in Species
- Evidence That Intracellular Stages of Utilize Amino Sugars as a Major Carbon Source
- Compartmentation of Redox Metabolism in Malaria Parasites