The Role of VP1 Amino Acid Residue 145 of Enterovirus 71 in Viral Fitness and Pathogenesis in a Cynomolgus Monkey Model

PLoS Pathogens

Volumn 11, Issue 7, 2015, Pages

  Kataoka, Chikako ^a   Suzuki, Tadaki ^b   Kotani, Osamu ^b   Iwata Yoshikawa, Naoko ^b   Nagata, Noriyo ^b   Ami, Yasushi ^a   Wakita, Takaji ^a   Nishimura, Yorihiro ^a,c   Shimizu, Hiroyuki ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b Department of Pathology ^*  (Japan)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; P SELECTIN GLYCOPROTEIN LIGAND 1; PROTEIN VP1; AMINO ACID;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; ENTEROVIRUS 71; FLOW CYTOMETRY; GENETIC STABILITY; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACACA FASCICULARIS; MALE; MOLECULAR CLONING; NEUROPATHOLOGY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; QUANTITATIVE ASSAY; VIRUS ISOLATION; VIRUS PATHOGENESIS; AMINO ACID SUBSTITUTION; ANIMAL; CENTRAL NERVOUS SYSTEM; DISEASE MODEL; ENTEROVIRUS A; ENTEROVIRUS INFECTION; GENETICS; HUMAN; METABOLISM; MONONUCLEAR CELL; VIROLOGY; VIRUS REPLICATION;

HUMAN ENTEROVIRUS 71; MACACA FASCICULARIS; MIRIDAE; PRIMATES;

AMINO ACID SUBSTITUTION; AMINO ACIDS; ANIMALS; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; HUMANS; LEUKOCYTES, MONONUCLEAR; MACACA FASCICULARIS; VIRUS REPLICATION;

EID: 84938792008     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005033     Document Type: Article

References (63)

1. Cifuente JO, Lee H, Yoder JD, Shingler KL, Carnegie MS, Yoder JL, et al. Structures of the procapsid and mature virion of enterovirus 71 strain 1095. J Virol. 2013;87(13):7637–45. doi: 10.1128/JVI.03519-12 23637404
2. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG, Crystal structure of human enterovirus 71. Science. 2012;336(6086):1274. doi: 10.1126/science.1218713 22383808
3. Brown BA, Oberste MS, Alexander JP, Kennett ML, Pallansch MA, Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol. 1999;73(12):9969–75. 10559310
4. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH, Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010;10(11):778–90. doi: 10.1016/S1473-3099(10)70194-8 20961813
5. Bessaud M, Razafindratsimandresy R, Nougairède A, Joffret ML, Deshpande JM, Dubot-Pérès A, et al. Molecular comparison and evolutionary analyses of VP1 nucleotide sequences of new African human enterovirus 71 isolates reveal a wide genetic diversity. PLoS One. 2014;9(3):e90624. doi: 10.1371/journal.pone.0090624 24598878
6. Feder HM, Jr.Bennett N, Modlin JF, Atypical hand, foot, and mouth disease: a vesiculobullous eruption caused by Coxsackie virus A6. Lancet Infect Dis. 2014;14(1):83–6. doi: 10.1016/S1473-3099(13)70264-0 24287184
7. Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T, Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol. 2010;9(11):1097–105. doi: 10.1016/S1474-4422(10)70209-X 20965438
8. Shimizu H, Utama A, Yoshii K, Yoshida H, Yoneyama T, Sinniah M, et al. 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. 1999;52(1):12–5. 10808253
9. Shimizu H, Utama A, Onnimala N, Li C, Li-Bi Z, Yu-Jie M, et al. Molecular epidemiology of enterovirus 71 infection in the Western Pacific Region. Pediatr Int. 2004;46(2):231–5. 15056257
10. McMinn PC, An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev. 2002;26(1):91–107. 12007645
11. Huang HI, Weng KF, Shih SR, Viral and host factors that contribute to pathogenicity of enterovirus 71. Future Microbiol. 2012;7(4):467–79. doi: 10.2217/fmb.12.22 22439724
12. Huang PN, Shih SR, Update on enterovirus 71 infection. Curr Opin Virol. 2014;5C:98–104. doi: 10.1016/j.coviro.2014.03.007
13. Lin JY, Shih SR, Cell and tissue tropism of enterovirus 71 and other enteroviruses infections. J Biomed Sci. 2014;21:18. doi: 10.1186/1423-0127-21-18 24602216
14. Su PY, Wang YF, Huang SW, Lo YC, Wang YH, Wu SR, et al. Cell Surface Nucleolin Facilitates Enterovirus 71 Binding and Infection. J Virol. 2015. doi: 10.1128/JVI.03498-14
15. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minowa T, Takemura T, et al. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med. 2009;15(7):798–801. doi: 10.1038/nm.1992 19543282
16. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, Shimizu H, Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med. 2009;15(7):794–7. doi: 10.1038/nm.1961 19543284
17. Tan CW, Poh CL, Sam IC, Chan YF, Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J Virol. 2013;87(1):611–20. doi: 10.1128/JVI.02226-12 23097443
18. Yang SL, Chou YT, Wu CN, Ho MS, Annexin II Binds to Capsid Protein VP1 of Enterovirus 71 and Enhances Viral Infectivity. J Virol. 2011;85(22):11809–20. doi: 10.1128/JVI.00297-11 21900167
19. Yang B, Chuang H, Yang KD, Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol J. 2009;6:141. doi: 10.1186/1743-422X-6-141 19751532
20. Lin YW, Wang SW, Tung YY, Chen SH, Enterovirus 71 Infection of Human Dendritic Cells. Exp Biol Med (Maywood). 2009. doi: 10.3181/0903-RM-116
21. Du N, Cong H, Tian H, Zhang H, Zhang W, Song L, et al. Cell surface vimentin is an attachment receptor for enterovirus 71. J Virol. 2014;88(10):5816–33. doi: 10.1128/JVI.03826-13 24623428
22. Kuronita T, Hatano T, Furuyama A, Hirota Y, Masuyama N, Saftig P, et al. The NH(2)-terminal transmembrane and lumenal domains of LGP85 are needed for the formation of enlarged endosomes/lysosomes. Traffic. 2005;6(10):895–906. doi: 10.1111/j.1600-0854.2005.00325.x 16138903
23. Kuronita T, Eskelinen EL, Fujita H, Saftig P, Himeno M, Tanaka Y, A role for the lysosomal membrane protein LGP85 in the biogenesis and maintenance of endosomal and lysosomal morphology. J Cell Sci. 2002;115(21):4117–31. doi: 10.1242/jcs.00075
24. Yamayoshi S, Iizuka S, Yamashita T, Minagawa H, Mizuta K, Okamoto M, et al. Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J Virol. 2012;86(10):5686–96. doi: 10.1128/JVI.00020-12 22438546
25. Fujii K, Nagata N, Sato Y, Ong KC, Wong KT, Yamayoshi S, et al. Transgenic mouse model for the study of enterovirus 71 neuropathogenesis. Proc Natl Acad Sci U S A. 2013;110(36):14753–8. doi: 10.1073/pnas.1217563110 23959904
26. Lin YW, Yu SL, Shao HY, Lin HY, Liu CC, Hsiao KN, et al. Human SCARB2 transgenic mice as an infectious animal model for enterovirus 71. PLoS One. 2013;8(2):e57591. doi: 10.1371/journal.pone.0057591 23451246
27. Laszik Z, Jansen PJ, Cummings RD, Tedder TF, McEver RP, Moore KL, P-selectin glycoprotein ligand-1 is broadly expressed in cells of myeloid, lymphoid, and dendritic lineage and in some nonhematopoietic cells. Blood. 1996;88(8):3010–21. 8874199
28. Somers WS, Tang J, Shaw GD, Camphausen RT, Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell. 2000;103(3):467–79. 11081633
29. Liu J, Dong W, Quan X, Ma C, Qin C, Zhang L, Transgenic expression of human P-selectin glycoprotein ligand-1 is not sufficient for enterovirus 71 infection in mice. Arch Virol. 2012;157(3):539–43. doi: 10.1007/s00705-011-1198-2 22187102
30. Nishimura Y, Lee H, Hafenstein S, Kataoka C, Wakita T, Bergelson JM, et al. Enterovirus 71 Binding to PSGL-1 on Leukocytes: VP1-145 Acts as a Molecular Switch to Control Receptor Interaction. PLoS Pathog. 2013;9(7):e1003511. doi: 10.1371/journal.ppat.1003511 23935488
31. Tee KK, Lam TT, Chan YF, Bible JM, Kamarulzaman A, Tong CY, et al. Evolutionary Genetics of Human Enterovirus 71: Origin, Population Dynamics, Natural Selection and Seasonal Periodicity of the VP1 Gene. J Virol. 2010. doi: 10.1128/JVI.01019-09
32. Chen X, Zhang Q, Li J, Cao W, Zhang JX, Zhang L, et al. Analysis of recombination and natural selection in human enterovirus 71. Virology. 2010;398(2):251–61. doi: 10.1016/j.virol.2009.12.007 20060995
33. Huang SW, Hsu YW, Smith DJ, Kiang D, Tsai HP, Lin KH, et al. Reemergence of Enterovirus 71 in 2008 in Taiwan: Dynamics of Genetic and Antigenic Evolution from 1998 to 2008. J Clin Microbiol. 2009;47(11):3653–62. doi: 10.1128/JCM.00630-09 19776232
34. Arita M, Ami Y, Wakita T, Shimizu H, 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. 2008;82(4):1787–97. doi: 10.1128/JVI.01798-07 18057246
35. Chua BH, Phuektes P, Sanders SA, Nicholls PK, McMinn PC, The molecular basis of mouse adaptation by human enterovirus 71. J Gen Virol. 2008;89(7):1622–32. doi: 10.1099/vir.0.83676-0
36. Huang SW, Wang YF, Yu CK, Su IJ, Wang JR, Mutations in VP2 and VP1 capsid proteins increase infectivity and mouse lethality of enterovirus 71 by virus binding and RNA accumulation enhancement. Virology. 2012;422(1):132–43. doi: 10.1016/j.virol.2011.10.015 22078110
37. Zaini Z, McMinn P, A single mutation in capsid protein VP1 (Q145E) of a genogroup C4 strain of human enterovirus 71 generates a mouse-virulent phenotype. J Gen Virol. 2012;93(Pt 9):1935–40. doi: 10.1099/vir.0.043893-0 22647370
38. Chang SC, Li WC, Chen GW, Tsao KC, Huang CG, Huang YC, et al. Genetic characterization of enterovirus 71 isolated from patients with severe disease by comparative analysis of complete genomes. J Med Virol. 2012;84(6):931–9. doi: 10.1002/jmv.23287 22499017
39. Zhang B, Wu X, Huang K, Li L, Zheng L, Wan C, et al. The variations of VP1 protein might be associated with nervous system symptoms caused by enterovirus 71 infection. BMC Infect Dis. 2014;14:243. doi: 10.1186/1471-2334-14-243 24886383
40. Liu Y, Fu C, Wu S, Chen X, Shi Y, Zhou B, et al. A novel finding for enterovirus virulence from the capsid protein VP1 of EV71 circulating in mainland China. Virus Genes. 2014;48(2):260–72. doi: 10.1007/s11262-014-1035-2 24442718
41. Li R, Zou Q, Chen L, Zhang H, Wang Y, Molecular analysis of virulent determinants of enterovirus 71. PLoS One. 2011;6(10):e26237. doi: 10.1371/journal.pone.0026237 22039449
42. Arita M, Nagata N, Iwata N, Ami Y, Suzaki Y, Mizuta K, et al. An attenuated strain of enterovirus 71 belonging to genotype a showed a broad spectrum of antigenicity with attenuated neurovirulence in cynomolgus monkeys. J Virol. 2007;81(17):9386–95. doi: 10.1128/JVI.02856-06 17567701
43. Arita M, Shimizu H, Nagata N, Ami Y, Suzaki Y, Sata T, et al. Temperature-sensitive mutants of enterovirus 71 show attenuation in cynomolgus monkeys. J Gen Virol. 2005;86(5):1391–401. doi: 10.1099/vir.0.80784-0
44. Nagata N, Iwasaki T, Ami Y, Tano Y, Harashima A, Suzaki Y, et al. Differential localization of neurons susceptible to enterovirus 71 and poliovirus type 1 in the central nervous system of cynomolgus monkeys after intravenous inoculation. J Gen Virol. 2004;85(10):2981–9. doi: 10.1099/vir.0.79883-0
45. Zhang Y, Liu H, Wang L, Yang F, Hu Y, Ren X, et al. Comparative study of the cytokine/chemokine response in children with differing disease severity in enterovirus 71-induced hand, foot, and mouth disease. PLoS One. 2013;8(6):e67430. doi: 10.1371/journal.pone.0067430 23840697
46. Griffiths MJ, Ooi MH, Wong SC, Mohan A, Podin Y, Perera D, et al. In enterovirus 71 encephalitis with cardio-respiratory compromise, elevated interleukin 1β, interleukin 1 receptor antagonist, and granulocyte colony-stimulating factor levels are markers of poor prognosis. J Infect Dis. 2012;206(6):881–92. doi: 10.1093/infdis/jis446 22829643
47. Wang SM, Lei HY, Huang KJ, Wu JM, Wang JR, Yu CK, et al. Pathogenesis of enterovirus 71 brainstem encephalitis in pediatric patients: roles of cytokines and cellular immune activation in patients with pulmonary edema. J Infect Dis. 2003;188(4):564–70. doi: 10.1086/376998 12898444
48. Lin TY, Chang LY, Huang YC, Hsu KH, Chiu CH, Yang KD, Different proinflammatory reactions in fatal and non-fatal enterovirus 71 infections: implications for early recognition and therapy. Acta Paediatr. 2002;91(6):632–5. doi: 10.1128/JCM.00542-06 12162592
49. Nix WA, Oberste MS, Pallansch MA, Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol. 2006;44(8):2698–704. doi: 10.1128/JCM.00542-06 16891480
50. He Y, Ong KC, Gao Z, Zhao X, Anderson VM, McNutt MA, et al. Tonsillar crypt epithelium is an important extra-central nervous system site for viral replication in EV71 encephalomyelitis. Am J Pathol. 2014;184(3):714–20. doi: 10.1016/j.ajpath.2013.11.009 24378407
51. Yamayoshi S, Fujii K, Koike S, Receptors for enterovirus 71. Emerging Microbes & Infections. 2014;3(e53). doi: 10.1038/emi.2014.49
52. Chen H, Zhang Y, Yang E, Liu L, Che Y, Wang J, et al. The effect of enterovirus 71 immunization on neuropathogenesis and protein expression profiles in the thalamus of infected rhesus neonates. Virology. 2012;432(2):417–26. doi: 10.1016/j.virol.2012.06.026 22819834
53. Wang J, Pu J, Huang H, Zhang Y, Liu L, Yang E, et al. EV71-infected CD14+ cells modulate the immune activity of T lymphocytes in rhesus monkeys. Emerg Microbes Infect. 2013;2.e44. doi: 10.1038/emi.2013.44
54. Miyamura K, Nishimura Y, Abo M, Wakita T, Shimizu H, Adaptive mutations in the genomes of enterovirus 71 strains following infection of mouse cells expressing human P-selectin glycoprotein ligand-1. J Gen Virol. 2011;92(2):287–91. doi: 10.1099/vir.0.022418-0
55. Lee H, Cifuente JO, Ashley RE, Conway JF, Makhov AM, Tano Y, et al. A Strain-Specific Epitope of Enterovirus 71 Identified by Cryo-Electron Microscopy of the Complex with Fab from Neutralizing Antibody. J Virol. 2013;87(21):11363–70. doi: 10.1128/JVI.01926-13 23946455
56. Hashimoto I, Hagiwara A, Pathogenicity of a poliomyelitis-like disease in monkeys infected orally with enterovirus 71: a model for human infection. Neuropathol Appl Neurobiol. 1982;8(2):149–56. doi: 10.1111/j.1365-2990.1982.tb00269.x 7048123
57. Salmi M, Jalkanen S, Human leukocyte subpopulations from inflamed gut bind to joint vasculature using distinct sets of adhesion molecules. J Immunol. 2001;166(7):4650–7. doi: 10.4049/jimmunol.166.7.4650 11254724
58. Cordey S, Petty TJ, Schibler M, Martinez Y, Gerlach D, van Belle S, et al. Identification of Site-Specific Adaptations Conferring Increased Neural Cell Tropism during Human Enterovirus 71 Infection. PLoS Pathog. 2012;8(7):e1002826. doi: 10.1371/journal.ppat.1002826 22910880
59. Wang X, Peng W, Ren J, Hu Z, Xu J, Lou Z, et al. A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat Struct Mol Biol. 2012;19(4):424–9. doi: 10.1038/nsmb.2255 22388738
60. Qing J, Wang Y, Sun Y, Huang J, Yan W, Wang J, et al. Cyclophilin a associates with enterovirus-71 virus capsid and plays an essential role in viral infection as an uncoating regulator. PLoS Pathog. 2014;10(10):e1004422. doi: 10.1371/journal.ppat.1004422 25275585
61. Zaini Z, Phuektes P, McMinn P, Mouse adaptation of a sub-genogroup B5 strain of human enterovirus 71 is associated with a novel lysine to glutamic acid substitution at position 244 in protein VP1. Virus Res. 2012;167(1):86–96. doi: 10.1016/j.virusres.2012.04.009 22575826
62. Nagata N, Shimizu H, Ami Y, Tano Y, Harashima A, Suzaki Y, et al. Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol. 2002;67(2):207–16. doi: 10.1002/jmv.2209 11992581
63. Jonsson N, Gullberg M, Lindberg AM, 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. 2009;53(3):149–54. doi: 10.1111/j.1348-0421.2009.00107.x 19302525