The N-Terminal Domain of the Arenavirus L Protein Is an RNA Endonuclease Essential in mRNA Transcription
Arenaviridae synthesize viral mRNAs using short capped primers presumably acquired from cellular transcripts by a ‘cap-snatching’ mechanism. Here, we report the crystal structure and functional characterization of the N-terminal 196 residues (NL1) of the L protein from the prototypic arenavirus: lymphocytic choriomeningitis virus. The NL1 domain is able to bind and cleave RNA. The 2.13 Å resolution crystal structure of NL1 reveals a type II endonuclease α/β architecture similar to the N-terminal end of the influenza virus PA protein. Superimposition of both structures, mutagenesis and reverse genetics studies reveal a unique spatial arrangement of key active site residues related to the PD…(D/E)XK type II endonuclease signature sequence. We show that this endonuclease domain is conserved and active across the virus families Arenaviridae, Bunyaviridae and Orthomyxoviridae and propose that the arenavirus NL1 domain is the Arenaviridae cap-snatching endonuclease.
Vyšlo v časopise:
The N-Terminal Domain of the Arenavirus L Protein Is an RNA Endonuclease Essential in mRNA Transcription. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001038
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001038
Souhrn
Arenaviridae synthesize viral mRNAs using short capped primers presumably acquired from cellular transcripts by a ‘cap-snatching’ mechanism. Here, we report the crystal structure and functional characterization of the N-terminal 196 residues (NL1) of the L protein from the prototypic arenavirus: lymphocytic choriomeningitis virus. The NL1 domain is able to bind and cleave RNA. The 2.13 Å resolution crystal structure of NL1 reveals a type II endonuclease α/β architecture similar to the N-terminal end of the influenza virus PA protein. Superimposition of both structures, mutagenesis and reverse genetics studies reveal a unique spatial arrangement of key active site residues related to the PD…(D/E)XK type II endonuclease signature sequence. We show that this endonuclease domain is conserved and active across the virus families Arenaviridae, Bunyaviridae and Orthomyxoviridae and propose that the arenavirus NL1 domain is the Arenaviridae cap-snatching endonuclease.
Zdroje
1. BrieseT
PaweskaJT
McMullanLK
HutchisonSK
StreetC
2009 Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog 5 e1000455
2. CharrelRN
de LamballerieX
EmonetS
2008 Phylogeny of the genus Arenavirus. Curr Opin Microbiol 11 362 368
3. BartonLL
BuddSC
MorfittWS
PetersCJ
KsiazekTG
1993 Congenital lymphocytic choriomeningitis virus infection in twins. Pediatr Infect Dis J 12 942 946
4. BartonLL
HyndmanNJ
2000 Lymphocytic choriomeningitis virus: reemerging central nervous system pathogen. Pediatrics 105 E35
5. FischerSA
GrahamMB
KuehnertMJ
KottonCN
SrinivasanA
2006 Transmission of lymphocytic choriomeningitis virus by organ transplantation. N Engl J Med 354 2235 2249
6. PalaciosG
DruceJ
DuL
TranT
BirchC
2008 A new arenavirus in a cluster of fatal transplant-associated diseases. N Engl J Med 358 991 998
7. MeyerBJ
de la TorreJC
SouthernPJ
2002 Arenaviruses: genomic RNAs, transcription, and replication. Curr Top Microbiol Immunol 262 139 157
8. SalvatoMS
ShimomayeEM
1989 The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173 1 10
9. MeyerBJ
SouthernPJ
1993 Concurrent sequence analysis of 5′ and 3′ RNA termini by intramolecular circularization reveals 5′ nontemplated bases and 3′ terminal heterogeneity for lymphocytic choriomeningitis virus mRNAs. J Virol 67 2621 2627
10. RajuR
RajuL
HackerD
GarcinD
CompansR
1990 Nontemplated bases at the 5′ ends of Tacaribe virus mRNAs. Virology 174 53 59
11. PolyakSJ
ZhengS
HarnishDG
1995 5′ termini of Pichinde arenavirus S RNAs and mRNAs contain nontemplated nucleotides. J Virol 69 3211 3215
12. PlotchSJ
BouloyM
KrugRM
1979 Transfer of 5′-terminal cap of globin mRNA to influenza viral complementary RNA during transcription in vitro. Proc Natl Acad Sci U S A 76 1618 1622
13. PlotchSJ
BouloyM
UlmanenI
KrugRM
1981 A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell 23 847 858
14. BishopDH
GayME
MatsuokoY
1983 Nonviral heterogeneous sequences are present at the 5′ ends of one species of snowshoe hare bunyavirus S complementary RNA. Nucleic Acids Res 11 6409 6418
15. DiasA
BouvierD
CrepinT
McCarthyAA
HartDJ
2009 The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458 914 918
16. YuanP
BartlamM
LouZ
ChenS
ZhouJ
2009 Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458 909 913
17. LopezN
JacamoR
Franze-FernandezMT
2001 Transcription and RNA replication of tacaribe virus genome and antigenome analogs require N and L proteins: Z protein is an inhibitor of these processes. J Virol 75 12241 12251
18. MullerR
PochO
DelarueM
BishopDH
BouloyM
1994 Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J Gen Virol 75 Pt 6 1345 1352
19. ViethS
TordaAE
AsperM
SchmitzH
GuntherS
2004 Sequence analysis of L RNA of Lassa virus. Virology 318 153 168
20. LukashevichIS
DjavaniM
ShapiroK
SanchezA
RavkovE
1997 The Lassa fever virus L gene: nucleotide sequence, comparison, and precipitation of a predicted 250 kDa protein with monospecific antiserum. J Gen Virol 78 Pt 3 547 551
21. WildaM
LopezN
CasabonaJC
Franze-FernandezMT
2008 Mapping of the tacaribe arenavirus Z-protein binding sites on the L protein identified both amino acids within the putative polymerase domain and a region at the N terminus of L that are critically involved in binding. J Virol 82 11454 11460
22. HolmL
KaariainenS
RosenstromP
SchenkelA
2008 Searching protein structure databases with DaliLite v.3. Bioinformatics 24 2780 2781
23. NicholSTBBJ
ElliottRM
2005 Virus Taxonomy, VIIIth Report of the ICTV. Fauquet CM, Mayo AM, Maniloff J et al eds London: Elsevier Academic Press 695 716
24. GroMC
Di BonitoP
AccardiL
GiorgiC
1992 Analysis of 3′ and 5′ ends of N and NSs messenger RNAs of Toscana Phlebovirus. Virology 191 435 438
25. Frias-StaheliN
GiannakopoulosNV
KikkertM
TaylorSL
BridgenA
2007 Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2 404 416
26. ZhaoC
LouZ
GuoY
MaM
ChenY
2009 Nucleoside monophosphate complex structures of the endonuclease domain from the influenza virus polymerase PA subunit reveal the substrate binding site inside the catalytic center. J Virol 83 9024 9030
27. GarcinD
KolakofskyD
1990 A novel mechanism for the initiation of Tacaribe arenavirus genome replication. J Virol 64 6196 6203
28. NewmanM
StrzeleckaT
DornerLF
SchildkrautI
AggarwalAK
1994 Structure of restriction endonuclease BamHI and its relationship to EcoRI. Nature 368 660 664
29. PingoudA
FuxreiterM
PingoudV
WendeW
2005 Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62 685 707
30. LelkeM
BrunotteL
BuschC
GuntherS
2010 An N-terminal region of Lassa virus L protein plays a critical role in transcription but not replication of the virus genome. J Virol 84 1934 1944
31. GuilligayD
TarendeauF
Resa-InfanteP
ColomaR
CrepinT
2008 The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15 500 506
32. AbrahamJ
CorbettKD
FarzanM
ChoeH
HarrisonSC
Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat Struct Mol Biol
33. De ClercqE
NeytsJ
2007 Avian influenza A (H5N1) infection: targets and strategies for chemotherapeutic intervention. Trends Pharmacol Sci 28 280 285
34. HsiehHP
HsuJT
2007 Strategies of development of antiviral agents directed against influenza virus replication. Curr Pharm Des 13 3531 3542
35. ParkesKE
ErmertP
FasslerJ
IvesJ
MartinJA
2003 Use of a pharmacophore model to discover a new class of influenza endonuclease inhibitors. J Med Chem 46 1153 1164
36. PowellHR
1999 The Rossmann Fourier autoindexing algorithm in MOSFLM. Acta Crystallogr D Biol Crystallogr 55 1690 1695
37. 1994 The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50 760 763
38. EmsleyP
CowtanK
2004 Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 2126 2132
39. AltschulSF
MaddenTL
SchafferAA
ZhangJ
ZhangZ
1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402
40. FinnRD
MistryJ
TateJ
CoggillP
HegerA
The Pfam protein families database. Nucleic Acids Res 38 D211 222
41. MaletH
CoutardB
JamalS
DutartreH
PapageorgiouN
2009 The crystal structures of Chikungunya and Venezuelan equine encephalitis virus nsP3 macro domains define a conserved adenosine binding pocket. J Virol 83 6534 6545
42. HassM
GölnitzU
MüllerS
Becker-ZiajaB
GüntherS
2004 Replicon system for Lassa virus. J Virol 78 13793 13803
43. BuchholzUJ
FinkeS
ConzelmannKK
1999 Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73 251 259
44. HassM
LelkeM
BuschC
Becker-ZiajaB
GüntherS
2008 Mutational evidence for a structural model of the Lassa virus RNA polymerase domain and identification of two residues, Gly1394 and Asp1395, that are critical for transcription but not replication of the genome. J Virol 82 10207 10217
45. SutterG
OhlmannM
ErfleV
1995 Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett 371 9 12
46. Kabsch W Xds. Acta Crystallogr D Biol Crystallogr 66 125 132
47. EvansP
2006 Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62 72 82
48. VonrheinC
BlancE
RoversiP
BricogneG
2007 Automated structure solution with autoSHARP. Methods Mol Biol 364 215 230
49. SchneiderTR
SheldrickGM
2002 Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58 1772 1779
50. BricogneG
VonrheinC
FlensburgC
SchiltzM
PaciorekW
2003 Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 59 2023 2030
51. CowtanK
1994 An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31 34 38
52. CowtanK
2006 The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62 1002 1011
53. AbrahamsJP
LeslieAG
1996 Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr D Biol Crystallogr 52 30 42
54. EmsleyP
LohkampB
ScottWG
CowtanK
Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66 486 501
55. BricogneG
BlancE
BrandlM
FlensburgC
KellerP
2010 BUSTER version 2.X. Global Phasing Ltd Cambridge, United Kingdom
56. LeslieAG
1992 MOSFLM - Recent changes and future developments. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 35 18 19
57. MurshudovGN
VaginAA
DodsonEJ
1997 Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53 240 255
58. SmartO
BrandlM
FlensburgC
KellerP
PaciorekW
2008 Refinement with Local Structure Similarity Restraints (LSSR) Enables Exploitation of Information from Related Structures and Facilitates use of NCS. Annual Meeting of the American Crystallographic Association
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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