Structures of Receptor Complexes of a North American H7N2 Influenza Hemagglutinin with a Loop Deletion in the Receptor Binding Site
Human infections with subtype H7 avian influenza viruses have been reported as early as 1979. In 1996, a genetically stable 24-nucleotide deletion emerged in North American H7 influenza virus hemagglutinins, resulting in an eight amino acid deletion in the receptor-binding site. The continuous circulation of these viruses in live bird markets, as well as its documented ability to infect humans, raises the question of how these viruses achieve structural stability and functionality. Here we report a detailed molecular analysis of the receptor binding site of the North American lineage subtype H7N2 virus A/New York/107/2003 (NY107), including complexes with an avian receptor analog (3′-sialyl-N-acetyllactosamine, 3′SLN) and two human receptor analogs (6′-sialyl-N-acetyllactosamine, 6′SLN; sialyllacto-N-tetraose b, LSTb). Structural results suggest a novel mechanism by which residues Arg220 and Arg229 (H3 numbering) are used to compensate for the deletion of the 220-loop and form interactions with the receptor analogs. Glycan microarray results reveal that NY107 maintains an avian-type (α2-3) receptor binding profile, with only moderate binding to human-type (α2-6) receptor. Thus despite its dramatically altered receptor binding site, this HA maintains functionality and confirms a need for continued influenza virus surveillance of avian and other animal reservoirs to define their zoonotic potential.
Vyšlo v časopise:
Structures of Receptor Complexes of a North American H7N2 Influenza Hemagglutinin with a Loop Deletion in the Receptor Binding Site. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001081
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001081
Souhrn
Human infections with subtype H7 avian influenza viruses have been reported as early as 1979. In 1996, a genetically stable 24-nucleotide deletion emerged in North American H7 influenza virus hemagglutinins, resulting in an eight amino acid deletion in the receptor-binding site. The continuous circulation of these viruses in live bird markets, as well as its documented ability to infect humans, raises the question of how these viruses achieve structural stability and functionality. Here we report a detailed molecular analysis of the receptor binding site of the North American lineage subtype H7N2 virus A/New York/107/2003 (NY107), including complexes with an avian receptor analog (3′-sialyl-N-acetyllactosamine, 3′SLN) and two human receptor analogs (6′-sialyl-N-acetyllactosamine, 6′SLN; sialyllacto-N-tetraose b, LSTb). Structural results suggest a novel mechanism by which residues Arg220 and Arg229 (H3 numbering) are used to compensate for the deletion of the 220-loop and form interactions with the receptor analogs. Glycan microarray results reveal that NY107 maintains an avian-type (α2-3) receptor binding profile, with only moderate binding to human-type (α2-6) receptor. Thus despite its dramatically altered receptor binding site, this HA maintains functionality and confirms a need for continued influenza virus surveillance of avian and other animal reservoirs to define their zoonotic potential.
Zdroje
1. ThompsonWW
ShayDK
WeintraubE
BrammerL
CoxN
2003 Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289 179 186
2. ThompsonWW
ShayDK
WeintraubE
BrammerL
BridgesCB
2004 Influenza-associated hospitalizations in the United States. JAMA 292 1333 1340
3. WHO 1980 A revision of the system of nomenclature for influenza viruses: a WHO memorandum. Bull, WHO 58 585 591
4. FouchierRA
MunsterV
WallenstenA
BestebroerTM
HerfstS
2005 Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79 2814 2822
5. ScholtissekC
RohdeW
Von HoyningenV
RottR
1978 On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87 13 20
6. KawaokaY
BeanWJ
WebsterRG
1989 Evolution of the hemagglutinin of equine H3 influenza viruses. Virology 169 283 292
7. GartenRJ
DavisCT
RussellCA
ShuB
LindstromS
2009 Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325 197 201
8. ShinyaK
EbinaM
YamadaS
OnoM
KasaiN
2006 Avian flu: influenza virus receptors in the human airway. Nature 440 435 436
9. MatrosovichMN
GambaryanAS
TenebergS
PiskarevVE
YamnikovaSS
1997 Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233 224 234
10. de JongJC
ClaasEC
OsterhausAD
WebsterRG
LimWL
1997 A pandemic warning? Nature 389 554
11. TaubenbergerJK
MorensDM
FauciAS
2007 The next influenza pandemic: can it be predicted? JAMA 297 2025 2027
12. WebsterRG
GeraciJ
PeturssonG
SkirnissonK
1981 Conjunctivitis in human beings caused by influenza A virus of seals. N Engl J Med 304 911
13. KurtzJ
ManvellRJ
BanksJ
1996 Avian influenza virus isolated from a woman with conjunctivitis. Lancet 348 901 902
14. KoopmansM
WilbrinkB
ConynM
NatropG
van der NatH
2004 Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363 587 593
15. FouchierRA
SchneebergerPM
RozendaalFW
BroekmanJM
KeminkSA
2004 Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101 1356 1361
16. CDC 2004 Update: influenza activity–United States and worldwide, 2003–04 season, and composition of the 2004–05 influenza vaccine. 547 552 MMWR Morb Mortal Wkly Rep: Centers for Disease Control
17. HirstM
AstellCR
GriffithM
CoughlinSM
MoksaM
2004 Novel avian influenza H7N3 strain outbreak, British Columbia. Emerg Infect Dis 10 2192 2195
18. TweedSA
SkowronskiDM
DavidST
LarderA
PetricM
2004 Human illness from avian influenza H7N3, British Columbia. Emerg Infect Dis 10 2196 2199
19. EditorialTeam 2007 Avian influenza A/H7N2 outbreak in the United Kingdom. Euro Surveill 12 2
20. SuarezDL
GarciaM
LatimerJ
SenneD
PerdueM
1999 Phylogenetic analysis of H7 avian influenza viruses isolated from the live bird markets of the Northeast United States. J Virol 73 3567 3573
21. BelserJA
LuX
MainesTR
SmithC
LiY
2007 Pathogenesis of avian influenza (H7) virus infection in mice and ferrets: enhanced virulence of Eurasian H7N7 viruses isolated from humans. J Virol 81 11139 11147
22. BelserJA
BlixtO
ChenLM
PappasC
MainesTR
2008 Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc Natl Acad Sci U S A 105 7558 7563
23. GambaryanAS
TuzikovAB
PazyninaGV
DeshevaJA
BovinNV
2008 6-sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol J 5 85
24. StevensJ
BlixtO
GlaserL
TaubenbergerJK
PaleseP
2006 Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355 1143 1155
25. StevensJ
CorperAL
BaslerCF
TaubenbergerJK
PaleseP
2004 Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303 1866 1870
26. RussellRJ
KerryPS
StevensDJ
SteinhauerDA
MartinSR
2008 Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci U S A 105 17736 17741
27. RussellRJ
GamblinSJ
HaireLF
StevensDJ
XiaoB
2004 H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology 325 287 296
28. MatrosovichM
TuzikovA
BovinN
GambaryanA
KlimovA
2000 Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74 8502 8512
29. NobusawaE
IshiharaH
MorishitaT
SatoK
NakajimaK
2000 Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Virology 278 587 596
30. StevensJ
BlixtO
ChenLM
DonisRO
PaulsonJC
2008 Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J Mol Biol 381 1382 1394
31. RussellRJ
StevensDJ
HaireLF
GamblinSJ
SkehelJJ
2006 Avian and human receptor binding by hemagglutinins of influenza A viruses. Glycoconj J 23 85 92
32. GamblinSJ
HaireLF
RussellRJ
StevensDJ
XiaoB
2004 The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303 1838 1842
33. SuarezDL
SpackmanE
SenneDA
2003 Update on molecular epidemiology of H1, H5, and H7 influenza virus infections in poultry in North America. Avian Dis 47 888 897
34. DanielsPS
JeffriesS
YatesP
SchildGC
RogersGN
1987 The receptor-binding and membrane-fusion properties of influenza virus variants selected using anti-haemagglutinin monoclonal antibodies. EMBO J 6 1459 1465
35. RosenthalPB
ZhangX
FormanowskiF
FitzW
WongCH
1998 Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 396 92 96
36. WeinsteinJ
de Souza-e-SilvaU
PaulsonJC
1982 Purification of a Gal beta 1 to 4GlcNAc alpha 2 to 6 sialyltransferase and a Gal beta 1 to 3(4)GlcNAc alpha 2 to 3 sialyltransferase to homogeneity from rat liver. J Biol Chem 257 13835 13844
37. GambaryanA
WebsterR
MatrosovichM
2002 Differences between influenza virus receptors on target cells of duck and chicken. Arch Virol 147 1197 1208
38. WanH
PerezDR
2006 Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 346 278 286
39. GuoCT
TakahashiN
YagiH
KatoK
TakahashiT
2007 The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 17 713 724
40. MainesTR
ChenLM
MatsuokaY
ChenH
RoweT
2006 Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103 12121 12126
41. WanH
SorrellEM
SongH
HossainMJ
Ramirez-NietoG
2008 Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 3 e2923
42. WeisWI
BrungerAT
SkehelJJ
WileyDC
1990 Refinement of the influenza virus hemagglutinin by simulated annealing. J Mol Biol 212 737 761
43. FrankS
KammererRA
MechlingD
SchulthessT
LandwehrR
2001 Stabilization of short collagen-like triple helices by protein engineering. J Mol Biol 308 1081 1089
44. StevensJ
BlixtO
TumpeyTM
TaubenbergerJK
PaulsonJC
2006 Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312 404 410
45. ChayenNE
Shaw-StewardPD
BlowDM
1992 Microbatch crystallization under oil – a new technique allowing many small volume crystallization experiments. J Cryst Growth 122 176 180
46. OtwinowskiA
MinorW
1997 Processing of X-ray diffraction data collected in oscillation mode. Meothds in Enzymology 276 307 326
47. McCoyAJ
Grosse-KunstleveRW
StoroniLC
ReadRJ
2005 Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61 458 464
48. EmsleyP
CowtanK
2004 Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 2126 2132
49. CCP4 1994 The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50 760 763
50. WinnMD
IsupovMN
MurshudovGN
2001 Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57 122 133
51. DavisIW
Leaver-FayA
ChenVB
BlockJN
KapralGJ
2007 MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35 W375 383
52. BrungerAT
2007 Version 1.2 of the Crystallography and NMR system. Nat Protoc 2 2728 2733
53. HoffmannE
WebsterRG
2000 Unidirectional RNA polymerase I-polymerase II transcription system for the generation of influenza A virus from eight plasmids. J Gen Virol 81 2843 2847
54. HiguchiR
KrummelB
SaikiRK
1988 A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16 7351 7367
55. BlixtO
HeadS
MondalaT
ScanlanC
HuflejtME
2004 Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci U S A 101 17033 17038
56. DeLanoWL
2002 The PyMol Molecular Graphics Systems. wwwpymolorg
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 9
- 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
- Structure of the Extracellular Portion of CD46 Provides Insights into Its Interactions with Complement Proteins and Pathogens
- The Length of Vesicular Stomatitis Virus Particles Dictates a Need for Actin Assembly during Clathrin-Dependent Endocytosis
- Inhibition of TIR Domain Signaling by TcpC: MyD88-Dependent and Independent Effects on Virulence
- Cellular Entry of Ebola Virus Involves Uptake by a Macropinocytosis-Like Mechanism and Subsequent Trafficking through Early and Late Endosomes