ICAM-5/Telencephalin Is a Functional Entry Receptor for Enterovirus D68

Cell Host and Microbe

Volumn 20, Issue 5, 2016, Pages 631-641

  Wei, Wei ^a   Guo, Haoran ^a   Chang, Junliang ^a   Yu, Yingzi ^b   Liu, Guanchen ^a   Zhang, Nannan ^a   Willard, Stephen H ^c,d   Zheng, Shu ^b   Yu, Xiao Fang ^a,b,c  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d Cellphire Inc   (United States)

Author keywords

acute flaccid myelitis; enterovirus; entry receptor; EV D68; ICAM 5 telencephalin; picornaviridae; respiratory illness

Indexed keywords

COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; DECAY ACCELERATING FACTOR; GLYCAN; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 3; INTERCELLULAR ADHESION MOLECULE 5; RECEPTOR; SIALIC ACID; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; ICAM5 PROTEIN, HUMAN; NERVE PROTEIN; PROTEIN BINDING; SIALIC ACID DERIVATIVE; VIRUS RECEPTOR;

ARTICLE; CONTROLLED STUDY; ENTEROVIRUS D; HEK293 CELL LINE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS ENTRY; VIRUS REPLICATION; METABOLISM; PHYSIOLOGY; VIRUS ATTACHMENT;

CELL ADHESION MOLECULES; ENTEROVIRUS D, HUMAN; HUMANS; NERVE TISSUE PROTEINS; PROTEIN BINDING; RECEPTORS, VIRUS; SIALIC ACIDS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 84994708597     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.09.013     Document Type: Article

References (40)

1. Baggen, J., Thibaut, H.J., Staring, J., Jae, L.T., Liu, Y., Guo, H., Slager, J.J., de Bruin, J.W., van Vliet, A.L., Blomen, V.A., et al. Enterovirus D68 receptor requirements unveiled by haploid genetics. Proc. Natl. Acad. Sci. USA 113 (2016), 1399–1404.
2. Blomqvist, S., Savolainen, C., Råman, L., Roivainen, M., Hovi, T., Human rhinovirus 87 and enterovirus 68 represent a unique serotype with rhinovirus and enterovirus features. J. Clin. Microbiol. 40 (2002), 4218–4223.
3. Brinton, M.A., Heinz, F.X., New Aspects of Positive-Strand RNA Viruses. 1990, American Society for Microbiology.
4. Bubeck, D., Filman, D.J., Cheng, N., Steven, A.C., Hogle, J.M., Belnap, D.M., The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79 (2005), 7745–7755.
5. Centers for Disease Control and Prevention (CDC). Enterovirus surveillance–United States, 2002-2004. MMWR Morb. Mortal. Wkly. Rep. 55 (2006), 153–156.
6. Centers for Disease Control and Prevention (CDC). Clusters of acute respiratory illness associated with human enterovirus 68–Asia, Europe, and United States, 2008-2010. MMWR Morb. Mortal. Wkly. Rep. 60 (2011), 1301–1304.
7. Chang, J., Li, J., Wei, W., Liu, X., Liu, G., Yang, J., Zhang, W., Yu, X.F., Determinants of EV71 immunogenicity and protection against lethal challenge in a mouse model. Immunol. Res. 62 (2015), 306–315.
8. Chen, P., Song, Z., Qi, Y., Feng, X., Xu, N., Sun, Y., Wu, X., Yao, X., Mao, Q., Li, X., et al. 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 (2012), 6406–6420.
9. Davis, P.M., Phillpotts, R.J., Susceptibility of the VERO line of African green monkey kidney cells to human enteroviruses. J. Hyg. (Lond.) 72 (1974), 23–30.
10. Fricks, C.E., Hogle, J.M., Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64 (1990), 1934–1945.
11. Gahmberg, C.G., Tian, L., Ning, L., Nyman-Huttunen, H., ICAM-5–a novel two-facetted adhesion molecule in the mammalian brain. Immunol. Lett. 117 (2008), 131–135.
12. Gahmberg, C.G., Ning, L., Paetau, S., ICAM-5: a neuronal dendritic adhesion molecule involved in immune and neuronal functions. Adv. Neurobiol. 8 (2014), 117–132.
13. Greninger, A.L., Naccache, S.N., Messacar, K., Clayton, A., Yu, G., Somasekar, S., Federman, S., Stryke, D., Anderson, C., Yagi, S., et al. A novel outbreak enterovirus D68 strain associated with acute flaccid myelitis cases in the USA (2012-14): a retrospective cohort study. Lancet Infect. Dis. 15 (2015), 671–682.
14. Greve, J.M., Davis, G., Meyer, A.M., Forte, C.P., Yost, S.C., Marlor, C.W., Kamarck, M.E., McClelland, A., The major human rhinovirus receptor is ICAM-1. Cell 56 (1989), 839–847.
15. Krautkrämer, E., Zeier, M., Hantavirus causing hemorrhagic fever with renal syndrome enters from the apical surface and requires decay-accelerating factor (DAF/CD55). J. Virol. 82 (2008), 4257–4264.
16. Kreuter, J.D., Barnes, A., McCarthy, J.E., Schwartzman, J.D., Oberste, M.S., Rhodes, C.H., Modlin, J.F., Wright, P.F., A fatal central nervous system enterovirus 68 infection. Arch. Pathol. Lab. Med. 135 (2011), 793–796.
17. Liu, Y., Rossmann, M.G., The cellular receptor for enterovirus 71. Protein Cell 5 (2014), 655–657.
18. Liu, Y., Sheng, J., Baggen, J., Meng, G., Xiao, C., Thibaut, H.J., van Kuppeveld, F.J., Rossmann, M.G., Sialic acid-dependent cell entry of human enterovirus D68. Nat. Commun., 6, 2015, 8865.
19. Liu, Y., Sheng, J., Fokine, A., Meng, G., Shin, W.H., Long, F., Kuhn, R.J., Kihara, D., Rossmann, M.G., Structure and inhibition of EV-D68, a virus that causes respiratory illness in children. Science 347 (2015), 71–74.
20. Messacar, K., Schreiner, T.L., Maloney, J.A., Wallace, A., Ludke, J., Oberste, M.S., Nix, W.A., Robinson, C.C., Glodé, M.P., Abzug, M.J., Dominguez, S.R., A cluster of acute flaccid paralysis and cranial nerve dysfunction temporally associated with an outbreak of enterovirus D68 in children in Colorado, USA. Lancet 385 (2015), 1662–1671.
21. Midgley, C.M., Watson, J.T., Nix, W.A., Curns, A.T., Rogers, S.L., Brown, B.A., Conover, C., Dominguez, S.R., Feikin, D.R., Gray, S., et al., EV-D68 Working Group. Severe respiratory illness associated with a nationwide outbreak of enterovirus D68 in the USA (2014): a descriptive epidemiological investigation. Lancet Respir. Med. 3 (2015), 879–887.
22. Nelson, R., Outbreaks of enterovirus D68 continue across the USA. Lancet Respir. Med., 2, 2014, 791.
23. Numazaki, Y., Oshima, T., Ohmi, A., Tanaka, A., Oizumi, Y., Komatsu, S., Takagi, T., Karahashi, M., Ishida, N., A microplate method for isolation of viruses from infants and children with acute respiratory infections. Microbiol. Immunol. 31 (1987), 1085–1095.
24. Oberste, M.S., Maher, K., Schnurr, D., Flemister, M.R., Lovchik, J.C., Peters, H., Sessions, W., Kirk, C., Chatterjee, N., Fuller, S., et al. Enterovirus 68 is associated with respiratory illness and shares biological features with both the enteroviruses and the rhinoviruses. J. Gen. Virol. 85 (2004), 2577–2584.
25. Qing, J., Wang, Y., Sun, Y., Huang, J., Yan, W., Wang, J., Su, D., Ni, C., Li, J., Rao, Z., et al. Cyclophilin A associates with enterovirus-71 virus capsid and plays an essential role in viral infection as an uncoating regulator. PLoS Pathog., 10, 2014, e1004422.
26. Recacha, R., Jiménez, D., Tian, L., Barredo, R., Gahmberg, C.G., Casasnovas, J.M., Crystal structures of an ICAM-5 ectodomain fragment show electrostatic-based homophilic adhesions. Acta Crystallogr. D Biol. Crystallogr. 70 (2014), 1934–1943.
27. Reed, L.J., Muench, H., A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 27 (1938), 493–497.
28. Rhoden, E., Zhang, M., Nix, W.A., Oberste, M.S., In Vitro Efficacy of Antiviral Compounds against Enterovirus D68. Antimicrob. Agents Chemother. 59 (2015), 7779–7781.
29. Schieble, J.H., Fox, V.L., Lennette, E.H., A probable new human picornavirus associated with respiratory diseases. Am. J. Epidemiol. 85 (1967), 297–310.
30. Staunton, D.E., Dustin, M.L., Erickson, H.P., Springer, T.A., The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. Cell 61 (1990), 243–254.
31. Su, P.Y., Liu, Y.T., Chang, H.Y., Huang, S.W., Wang, Y.F., Yu, C.K., Wang, J.R., Chang, C.F., Cell surface sialylation affects binding of enterovirus 71 to rhabdomyosarcoma and neuroblastoma cells. BMC Microbiol., 12, 2012, 162.
32. Tse, M.C., Lane, C., Mott, K., Onlamoon, N., Hsiao, H.M., Perng, G.C., ICAM-5 modulates cytokine/chemokine production in the CNS during the course of herpes simplex virus type 1 infection. J. Neuroimmunol. 213 (2009), 12–19.
33. Tyler, K.L., Rationale for the evaluation of fluoxetine in the treatment of enterovirus D68-associated acute flaccid myelitis. JAMA Neurol. 72 (2015), 493–494.
34. Uncapher, C.R., DeWitt, C.M., Colonno, R.J., The major and minor group receptor families contain all but one human rhinovirus serotype. Virology 180 (1991), 814–817.
35. van Ooij, M.J., Polacek, C., Glaudemans, D.H., Kuijpers, J., van Kuppeveld, F.J., Andino, R., Agol, V.I., Melchers, W.J., Polyadenylation of genomic RNA and initiation of antigenomic RNA in a positive-strand RNA virus are controlled by the same cis-element. Nucleic Acids Res. 34 (2006), 2953–2965.
36. Yamayoshi, S., Yamashita, Y., Li, J., Hanagata, N., Minowa, T., Takemura, T., Koike, S., Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat. Med. 15 (2009), 798–801.
37. Yang, H., Structure, Expression, and Function of ICAM-5. Comp. Funct. Genomics, 2012, 2012, 368938.
38. Yang, B., Chuang, H., Yang, K.D., Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol. J., 6, 2009, 141.
39. Zhang, H., Casasnovas, J.M., Jin, M., Liu, J.H., Gahmberg, C.G., Springer, T.A., Wang, J.H., An unusual allosteric mobility of the C-terminal helix of a high-affinity alphaL integrin I domain variant bound to ICAM-5. Mol. Cell 31 (2008), 432–437.
40. Zhang, W., Du, J., Evans, S.L., Yu, Y., Yu, X.F., T-cell differentiation factor CBF-β regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481 (2011), 376–379.