Enterovirus 71 Binding to PSGL-1 on Leukocytes: VP1-145 Acts as a Molecular Switch to Control Receptor Interaction
Some strains of enterovirus 71 (EV71), but not others, infect leukocytes by binding to a specific receptor molecule: the P-selectin glycoprotein ligand-1 (PSGL-1). We find that a single amino acid residue within the capsid protein VP1 determines whether EV71 binds to PSGL-1. Examination of capsid sequences of representative EV71 strains revealed that the PSGL-1-binding viruses had either a G or a Q at residue 145 within the capsid protein VP1 (VP1-145G or Q), whereas PSGL-1-nonbinding viruses had VP1-145E. Using site-directed mutagenesis we found that PSGL-1-binding strains lost their capacity to bind when VP1-145G/Q was replaced by E; conversely, nonbinding strains gained the capacity to bind PSGL-1 when VP1-145E was replaced with either G or Q. Viruses with G/Q at VP1-145 productively infected a leukocyte cell line, Jurkat T-cells, whereas viruses with E at this position did not. We previously reported that EV71 binds to the N-terminal region of PSGL-1, and that binding depends on sulfated tyrosine residues within this region. We speculated that binding depends on interaction between negatively charged sulfate groups and positively charged basic residues in the virus capsid. VP1-145 on the virus surface is in close proximity to conserved lysine residues at VP1-242 and VP1-244. Comparison of recently published crystal structures of EV71 isolates with either Q or E at VP1-145 revealed that VP1-145 controls the orientation of the lysine side-chain of VP1-244: with VP1-145Q the lysine side chain faces outward, but with VP1-145E, the lysine side chain is turned toward the virus surface. Mutation of VP1-244 abolished virus binding to PSGL-1, and mutation of VP1-242 greatly reduced binding. We propose that conserved lysine residues on the virus surface are responsible for interaction with sulfated tyrosine residues at the PSGL-1 N-terminus, and that VP1-145 acts as a switch, controlling PSGL-1 binding by modulating the exposure of VP1-244K.
Vyšlo v časopise:
Enterovirus 71 Binding to PSGL-1 on Leukocytes: VP1-145 Acts as a Molecular Switch to Control Receptor Interaction. PLoS Pathog 9(7): e32767. doi:10.1371/journal.ppat.1003511
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003511
Souhrn
Some strains of enterovirus 71 (EV71), but not others, infect leukocytes by binding to a specific receptor molecule: the P-selectin glycoprotein ligand-1 (PSGL-1). We find that a single amino acid residue within the capsid protein VP1 determines whether EV71 binds to PSGL-1. Examination of capsid sequences of representative EV71 strains revealed that the PSGL-1-binding viruses had either a G or a Q at residue 145 within the capsid protein VP1 (VP1-145G or Q), whereas PSGL-1-nonbinding viruses had VP1-145E. Using site-directed mutagenesis we found that PSGL-1-binding strains lost their capacity to bind when VP1-145G/Q was replaced by E; conversely, nonbinding strains gained the capacity to bind PSGL-1 when VP1-145E was replaced with either G or Q. Viruses with G/Q at VP1-145 productively infected a leukocyte cell line, Jurkat T-cells, whereas viruses with E at this position did not. We previously reported that EV71 binds to the N-terminal region of PSGL-1, and that binding depends on sulfated tyrosine residues within this region. We speculated that binding depends on interaction between negatively charged sulfate groups and positively charged basic residues in the virus capsid. VP1-145 on the virus surface is in close proximity to conserved lysine residues at VP1-242 and VP1-244. Comparison of recently published crystal structures of EV71 isolates with either Q or E at VP1-145 revealed that VP1-145 controls the orientation of the lysine side-chain of VP1-244: with VP1-145Q the lysine side chain faces outward, but with VP1-145E, the lysine side chain is turned toward the virus surface. Mutation of VP1-244 abolished virus binding to PSGL-1, and mutation of VP1-242 greatly reduced binding. We propose that conserved lysine residues on the virus surface are responsible for interaction with sulfated tyrosine residues at the PSGL-1 N-terminus, and that VP1-145 acts as a switch, controlling PSGL-1 binding by modulating the exposure of VP1-244K.
Zdroje
1. Pallansch M, Roos R (2007) Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 5th edition. Philadelphia: Lippincott Williams & Wilkins. pp. 839–893.
2. PlevkaP, PereraR, CardosaJ, KuhnRJ, RossmannMG (2012) Crystal structure of human enterovirus 71. Science 336: 1274.
3. PlevkaP, PereraR, CardosaJ, KuhnRJ, RossmannMG (2012) Structure determination of enterovirus 71. Acta Crystallogr D Biol Crystallogr 68: 1217–1222.
4. WangX, PengW, RenJ, HuZ, XuJ, et al. (2012) A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat Struct Mol Biol 19: 424–429.
5. AlexanderJPJr, BadenL, PallanschMA, AndersonLJ (1994) Enterovirus 71 infections and neurologic disease–United States, 1977–1991. J Infect Dis 169: 905–908.
6. McMinnPC (2002) An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 26: 91–107.
7. OoiMH, WongSC, LewthwaiteP, CardosaMJ, SolomonT (2010) Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 9: 1097–1105.
8. SolomonT, LewthwaiteP, PereraD, CardosaMJ, McMinnP, et al. (2010) Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 10: 778–790.
9. BibleJM, PantelidisP, ChanPKS, TongCYW (2007) Genetic evolution of enterovirus 71: epidemiological and pathological implications. Rev Med Virol 17: 371–379.
10. YangF, RenL, XiongZ, LiJ, XiaoY, et al. (2009) Enterovirus 71 outbreak in the People's Republic of China in 2008. J Clin Microbiol 47: 2351–2352.
11. LinYW, WangSW, TungYY, ChenSH (2009) Enterovirus 71 infection of human dendritic cells. Exp Biol Med (Maywood) 234: 1166–1173.
12. NishimuraY, ShimojimaM, TanoY, MiyamuraT, WakitaT, et al. (2009) Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15: 794–797.
13. TanCW, PohCL, SamIC, ChanYF (2013) Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J Virol 87: 611–620.
14. YamayoshiS, YamashitaY, LiJ, HanagataN, MinowaT, et al. (2009) Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 15: 798–801.
15. YangB, ChuangH, YangKD (2009) Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol J 6: 141.
16. YangSL, ChouYT, WuCN, HoMS (2011) Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J Virol 85: 11809–11820.
17. NishimuraY, ShimizuH (2012) Cellular receptors for human enterovirus species A. Front Microbiol 3: 105.
18. PatelKP, BergelsonJM (2009) Receptors identified for hand, foot and mouth virus. Nat Med 15: 728–729.
19. LaszikZ, JansenPJ, CummingsRD, TedderTF, McEverRP, et al. (1996) P-selectin glycoprotein ligand-1 is broadly expressed in cells of myeloid, lymphoid, and dendritic lineage and in some nonhematopoietic cells. Blood 88: 3010–3021.
20. SakoD, ChangXJ, BaroneKM, VachinoG, WhiteHM, et al. (1993) Expression cloning of a functional glycoprotein ligand for P-selectin. Cell 75: 1179–1186.
21. YamayoshiS, IizukaS, YamashitaT, MinagawaH, MizutaK, et al. (2012) Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J Virol 86: 5686–5696.
22. LiuWJ, RamachandranV, KangJ, KishimotoTK, CummingsRD, et al. (1998) Identification of N-terminal residues on P-selectin glycoprotein ligand-1 required for binding to P-selectin. J Biol Chem 273: 7078–7087.
23. PouyaniT, SeedB (1995) PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell 83: 333–343.
24. SakoD, ComessKM, BaroneKM, CamphausenRT, CummingDA, et al. (1995) A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell 83: 323–331.
25. WilkinsPP, MooreKL, McEverRP, CummingsRD (1995) Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J Biol Chem 270: 22677–22680.
26. NishimuraY, WakitaT, ShimizuH (2010) Tyrosine sulfation of the amino terminus of PSGL-1 is critical for enterovirus 71 infection. PLoS Pathog 6: e1001174.
27. MiyamuraK, NishimuraY, AboM, WakitaT, ShimizuH (2011) Adaptive mutations in the genomes of enterovirus 71 strains following infection of mouse cells expressing human P-selectin glycoprotein ligand-1. J Gen Virol 92: 287–291.
28. BrownBA, ObersteMS, AlexanderJPJr, KennettML, PallanschMA (1999) Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73: 9969–9975.
29. TeeKK, LamTT, ChanYF, BibleJM, KamarulzamanA, et al. (2010) Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection and seasonal periodicity of the VP1 gene. J Virol 84: 3339–3350.
30. ChenP, SongZ, QiY, FengX, XuN, et al. (2012) Molecular determinants of enterovirus 71 viral entry: cleft around GLN-172 on VP1 protein interacts with variable region on scavenge receptor B 2. J Biol Chem 287: 6406–6420.
31. ArnoldK, BordoliL, KoppJ, SchwedeT (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195–201.
32. KieferF, ArnoldK, KunzliM, BordoliL, SchwedeT (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res 37: D387–392.
33. PeitschMC (1995) Protein modeling by E-mail. Nat Biotechnol 13: 658–660.
34. YamayoshiS, OhkaS, FujiiK, KoikeS (2013) Functional comparison of SCARB2 and PSGL1 as receptors for EV71. J Virol 87: 3335–3347.
35. KilpatrickDR, NottayB, YangCF, YangSJ, Da SilvaE, et al. (1998) Serotype-specific identification of polioviruses by PCR using primers containing mixed-base or deoxyinosine residues at positions of codon degeneracy. J Clin Microbiol 36: 352–357.
36. JonssonN, GullbergM, LindbergAM (2009) Real-time polymerase chain reaction as a rapid and efficient alternative to estimation of picornavirus titers by tissue culture infectious dose 50% or plaque forming units. Microbiol Immunol 53: 149–154.
37. SomersWS, TangJ, ShawGD, CamphausenRT (2000) Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLeX and PSGL-1. Cell 103: 467–479.
38. SchnurE, NoahE, AyzenshtatI, SargsyanH, InuiT, et al. (2011) The conformation and orientation of a 27-residue CCR5 peptide in a ternary complex with HIV-1 gp120 and a CD4-mimic peptide. J Mol Biol 410: 778–797.
39. McLeishNJ, WilliamsÇH, KaloudasD, RoivainenM, StanwayG (2012) Symmetry-related clustering of positive charges is a common mechanism for heparan sulfate binding in enteroviruses. J Virol 86: 11163–11170.
40. ChenX, ZhangQ, LiJ, CaoW, ZhangJX, et al. (2010) Analysis of recombination and natural selection in human enterovirus 71. Virology 398: 251–261.
41. ShiWF, ZhangZ, DunAS, ZhangYZ, YuGF, et al. (2009) Positive selection analysis of VP1 Genes of worldwide human enterovirus 71 viruses. Virol Sin 24: 59–64.
42. ChangSC, LiWC, ChenGW, TsaoKC, HuangCG, et al. (2012) Genetic characterization of enterovirus 71 isolated from patients with severe disease by comparative analysis of complete genomes. J Med Virol 84: 931–939.
43. LiR, ZouQ, ChenL, ZhangH, WangY (2011) Molecular analysis of virulent determinants of enterovirus 71. PLoS One 6: e26237.
44. AritaM, AmiY, WakitaT, ShimizuH (2008) Cooperative effect of the attenuation determinants derived from poliovirus Sabin 1 strain is essential for attenuation of enterovirus 71 in the NOD/SCID mouse infection model. J Virol 82: 1787–1797.
45. ChuaBH, PhuektesP, SandersSA, NichollsPK, McMinnPC (2008) The molecular basis of mouse adaptation by human enterovirus 71. J Gen Virol 89: 1622–1632.
46. HuangSW, WangYF, YuCK, SuIJ, WangJR (2012) Mutations in VP2 and VP1 capsid proteins increase infectivity and mouse lethality of enterovirus 71 by virus binding and RNA accumulation enhancement. Virology 422: 132–143.
47. HogleJM (2002) Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu Rev Microbiol 56: 677–702.
48. CarlowDA, GossensK, NausS, VeermanKM, SeoW, et al. (2009) PSGL-1 function in immunity and steady state homeostasis. Immunol Rev 230: 75–96.
49. UrzainquiA, Martínez del HoyoG, LamanaA, de la FuenteH, BarreiroO, et al. (2007) Functional role of P-selectin glycoprotein ligand 1/P-selectin interaction in the generation of tolerogenic dendritic cells. J Immunol 179: 7457–7465.
50. WeyrichAS, McIntyreTM, McEverRP, PrescottSM, ZimmermanGA (1995) Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-alpha secretion. Signal integration and NF-kappa B translocation. J Clin Invest 95: 2297–2303.
51. WeyrichAS, ElstadMR, McEverRP, McIntyreTM, MooreKL, et al. (1996) Activated platelets signal chemokine synthesis by human monocytes. J Clin Invest 97: 1525–1534.
52. ZarbockA, MüllerH, KuwanoY, LeyK (2009) PSGL-1-dependent myeloid leukocyte activation. J Leukoc Biol 86: 1119–1124.
53. SchmidtNJ, LennetteEH, HoHH (1974) An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis 129: 304–309.
54. ShimizuH, UtamaA, YoshiiK, YoshidaH, YoneyamaT, et al. (1999) Enterovirus 71 from fatal and nonfatal cases of hand, foot and mouth disease epidemics in Malaysia, Japan and Taiwan in 1997–1998. Jpn J Infect Dis 52: 12–15.
55. MizutaK, AbikoC, MurataT, MatsuzakiY, ItagakiT, et al. (2005) Frequent importation of enterovirus 71 from surrounding countries into the local community of Yamagata, Japan, between 1998 and 2003. J Clin Microbiol 43: 6171–6175.
56. NagataN, ShimizuH, AmiY, TanoY, HarashimaA, et al. (2002) Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol 67: 207–216.
57. ShimizuH, UtamaA, OnnimalaN, LiC, Li-BiZ, et al. (2004) Molecular epidemiology of enterovirus 71 infection in the Western Pacific Region. Pediatr Int 46: 231–235.
58. TagayaI, TachibanaK (1975) Epidemic of hand, foot and mouth disease in Japan, 1972–1973: difference in epidemiologic and virologic features from the previous one. Jpn J Med Sci Biol 28: 231–234.
59. DurocherY, PerretS, KamenA (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res 30: E9.
60. PettersenEF, GoddardTD, HuangCC, CouchGS, GreenblattDM, et al. (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 25: 1605–1612.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2013 Číslo 7
- 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
- Pertussis: Challenges Today and for the Future
- It's No Fluke: The Planarian as a Model for Understanding Schistosomes
- Emerging Infectious Diseases: Threats to Human Health and Global Stability
- A Multi-targeted Drug Candidate with Dual Anti-HIV and Anti-HSV Activity