Functional comparison of SCARB2 and PSGL1 as receptors for enterovirus 71

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3335-3347

  Yamayoshi, Seiya ^a   Ohka, Seii ^a   Fujii, Ken ^a   Koike, Satoshi ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; GENOMIC RNA; MEMBRANE RECEPTOR; P SELECTIN GLYCOPROTEIN LIGAND 1; PROTEIN VP4; SCAVENGER RECEPTOR B2; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOSOME; ENTEROVIRUS 71; ENTEROVIRUS INFECTION; IMMUNOFLUORESCENCE MICROSCOPY; INTERNALIZATION; L CELL; NONHUMAN; PATHOPHYSIOLOGY; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RECEPTOR AFFINITY; SUCROSE DENSITY GRADIENT CENTRIFUGATION; VIRION; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS ENTRY; VIRUS UNCOATING;

ANIMALS; CELL LINE; ENTEROVIRUS A, HUMAN; HUMANS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICROSCOPY, FLUORESCENCE; RECEPTORS, SCAVENGER; RECEPTORS, VIRUS; VIRUS INTERNALIZATION; VIRUS UNCOATING;

EID: 84874742838     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02070-12     Document Type: Article

References (67)

1. Racaniello V. 2007. Picornaviridae: the viruses and their replication, p 795-838. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Rossmann MG, Johnson JE. 1989. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58:533-573.
3. Wang X, Peng W, Ren J, Hu Z, Xu J, Lou Z, Li X, Yin W, Shen X, Porta C, Walter TS, Evans G, Axford D, Owen R, Rowlands DJ, Wang J, Stuart DI, Fry EE, Rao Z. 2012. A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat. Struct. Mol. Biol. 19:424-429.
4. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG. 2012. Crystal structure of human enterovirus 71. Science 336:1274.
5. Rossmann MG, He Y, Kuhn RJ. 2002. Picornavirus-receptor interactions. Trends Microbiol. 10:324-331.
6. Schmidt NJ, Lennette EH, Ho HH. 1974. An apparently new enterovirus isolated from patients with disease of the central nervous system. J. Infect. Dis. 129:304-309.
7. Blomberg J, Lycke E, Ahlfors K, Johnsson T, Wolontis S, von Zeipel G. 1974. New enterovirus type associated with epidemic of aseptic meningitis and-or hand, foot, and mouth disease. Lancet ii:112.
8. Hagiwara A, Tagaya I, Yoneyama T. 1978. Epidemic of hand, foot and mouth disease associated with enterovirus 71 infection. Intervirology 9:60-63.
9. McMinn PC. 2002. An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol. Rev. 26:91-107.
10. Fujimoto T, Chikahira M, Yoshida S, Ebira H, Hasegawa A, Totsuka A, Nishio O. 2002. Outbreak of central nervous system disease associated with hand, foot, and mouth disease in Japan during the summer of 2000: detection and molecular epidemiology of enterovirus 71. Microbiol. Immunol. 46:621-627.
11. Chan LG, Parashar UD, Lye MS, Ong FG, Zaki SR, Alexander JP, Ho KK, Han LL, Pallansch MA, Suleiman AB, Jegathesan M, Anderson LJ. 2000. Deaths of children during an outbreak of hand, foot, and mouth disease in Sarawak, Malaysia: clinical and pathological characteristics of the disease. For the Outbreak Study Group. Clin. Infect. Dis. 31:678-683.
12. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shih SR. 1999. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med. 341:929-935.
13. Ahmad K. 2000. Hand, foot, and mouth disease outbreak reported in Singapore. Lancet 356:1338.
14. Qiu J. 2008. Enterovirus 71 infection: a new threat to global public health? Lancet Neurol. 7:868-869.
15. Yan JJ, Wang JR, Liu CC, Yang HB, Su IJ. 2000. An outbreak of enterovirus 71 infection in Taiwan 1998: a comprehensive pathological, virological, and molecular study on a case of fulminant encephalitis. J. Clin. Virol. 17:13-22.
16. Yang F, Ren L, Xiong Z, Li J, Xiao Y, Zhao R, He Y, Bu G, Zhou S, Wang J, Qi J. 2009. Enterovirus 71 outbreak in the People's Republic of China in 2008. J. Clin. Microbiol. 47:2351-2352.
17. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minowa T, Takemura T, Koike S. 2009. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat. Med. 15:798-801.
18. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, Shimizu H. 2009. Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat. Med. 15:794-797.
19. Eskelinen EL, Tanaka Y, Saftig P. 2003. At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13:137-145.
20. Reczek D, Schwake M, Schroder J, Hughes H, Blanz J, Jin X, Brondyk W, Van Patten S, Edmunds T, Saftig P. 2007. LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of betaglucocerebrosidase. Cell 131:770-783.
21. Blanz J, Groth J, Zachos C, Wehling C, Saftig P, Schwake M. 2010. Disease-causing mutations within the lysosomal integral membrane protein type 2 (LIMP-2) reveal the nature of binding to its ligand betaglucocerebrosidase. Hum. Mol. Genet. 19:563-572.
22. Yamayoshi S, Iizuka S, Yamashita T, Minagawa H, Mizuta K, Okamoto M, Nishimura H, Sanjoh K, Katsushima N, Itagaki T, Nagai Y, Fujii K, Koike S. 2012. Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J. Virol. 86:5686-5696.
23. Yamayoshi S, Koike S. 2011. Identification of a human SCARB2 region that is important for enterovirus 71 binding and infection. J. Virol. 85: 4937-4946.
24. Chen P, Song Z, Qi Y, Feng X, Xu N, Sun Y, Wu X, Yao X, Mao Q, Li X, Dong W, Wan X, Huang N, Shen X, Liang Z, Li W. 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.
25. Hussain KM, Leong KL, Ng MM, Chu JJ. 2011. The essential role of clathrin-mediated endocytosis in the infectious entry of human enterovirus 71. J. Biol. Chem. 286:309-321.
26. Lin YW, Lin HY, Tsou YL, Chitra E, Hsiao KN, Shao HY, Liu CC, Sia C, Chong P, Chow YH. 2012. Human SCARB2-mediated entry and endocytosis of EV71. PLoS One 7:e30507. doi:10.1371/journal.pone .0030507.
27. Sako D, Chang XJ, Barone KM, Vachino G, White HM, Shaw G, Veldman GM, Bean KM, Ahern TJ, Furie B, Cumming DA, Larsen GR. 1993. Expression cloning of a functional glycoprotein ligand for Pselectin. Cell 75:1179-1186.
28. Laszik Z, Jansen PJ, Cummings RD, Tedder TF, McEver RP, Moore KL. 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.
29. Somers WS, Tang J, Shaw GD, Camphausen RT. 2000. 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 103:467-479.
30. Ley K, Kansas GS. 2004. Selectins in T-cell recruitment to non-lymphoid tissues and sites of inflammation. Nat. Rev. Immunol. 4:325-335.
31. Nishimura Y, Wakita T, Shimizu H. 2010. Tyrosine sulfation of the amino terminus of PSGL-1 is critical for enterovirus 71 infection. PLoS Pathog. 6:e1001174. doi:10.1371/journal.ppat.1001174.
32. Liu J, Dong W, Quan X, Ma C, Qin C, Zhang L. 2012. Transgenic expression of human P-selectin glycoprotein ligand-1 is not sufficient for enterovirus 71 infection in mice. Arch. Virol. 157:539-543.
33. Bergelson JM. 2010. Receptors, p 73-86. In Ehrenfeld E, Domingo E, Roos RP (ed), The picornaviruses. ASM Press, Washington, DC.
34. Tuthill TJ, Groppelli E, Hogle JM, Rowlands DJ. 2010. Picornaviruses. Curr. Top. Microbiol. Immunol. 343:43-89
35. Mendelsohn CL, Wimmer E, Racaniello VR. 1989. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855-865.
36. Koike S, Horie H, Ise I, Okitsu A, Yoshida M, Iizuka N, Takeuchi K, Takegami T, Nomoto A. 1990. The poliovirus receptor protein is produced both as membrane-bound and secreted forms. EMBO J. 9:3217-3224.
37. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA. 1989. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56:849-853.
38. Tomassini JE, Graham D, DeWitt CM, Lineberger DW, Rodkey JA, Colonno RJ. 1989. cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. U. S. A. 86:4907-4911.
39. Greve JM, Davis G, Meyer AM, Forte CP, Yost SC, Marlor CW, Kamarck ME, McClelland A. 1989. The major human rhinovirus receptor is ICAM-1. Cell 56:839-847.
40. Duque H, Baxt B. 2003. Foot-and-mouth disease virus receptors: comparison of bovine alpha(V) integrin utilization by type A and O viruses. J. Virol. 77:2500-2511.
41. Hofer F, Gruenberger M, Kowalski H, Machat H, Huettinger M, Kuechler E, Blaas D. 1994. Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc. Natl. Acad. Sci. U. S. A. 91:1839-1842.
42. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
43. Tomko RP, Xu R, Philipson L. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. U. S. A. 94:3352-3356.
44. Shafren DR, Bates RC, Agrez MV, Herd RL, Burns GF, Barry RD. 1995. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J. Virol. 69:3873-3877.
45. Shafren DR, Williams DT, Barry RD. 1997. A decay-accelerating factorbinding strain of coxsackievirus B3 requires the coxsackievirusadenovirus receptor protein to mediate lytic infection of rhabdomyosarcoma cells. J. Virol. 71:9844-9848.
46. Milstone AM, Petrella J, Sanchez MD, Mahmud M, Whitbeck JC, Bergelson JM. 2005. Interaction with coxsackievirus and adenovirus receptor, but not with decay-accelerating factor (DAF), induces A-particle formation in a DAF-binding coxsackievirus B3 isolate. J. Virol. 79:655-660.
47. Coyne CB, Bergelson JM. 2006. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124: 119-131.
48. Arita M, Koike S, Aoki J, Horie H, Nomoto A. 1998. Interaction of poliovirus with its purified receptor and conformational alteration in the virion. J. Virol. 72:3578-3586.
49. Fricks CE, Hogle JM. 1990. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64:1934-1945.
50. Prchla E, Kuechler E, Blaas D, Fuchs R. 1994. Uncoating of human rhinovirus serotype 2 from late endosomes. J. Virol. 68:3713-3723.
51. Curry S, Abrams CC, Fry E, Crowther JC, Belsham GJ, Stuart DI, King AM. 1995. Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J. Virol. 69:430-438.
52. Tuthill TJ, Harlos K, Walter TS, Knowles NJ, Groppelli E, Rowlands DJ, Stuart DI, Fry EE. 2009. Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism? PLoS Pathog. 5:e1000620. doi:10.1371/journal.ppat.1000620.
53. Nurani G, Lindqvist B, Casasnovas JM. 2003. Receptor priming of major group human rhinoviruses for uncoating and entry at mild low-pH environments. J. Virol. 77:11985-11991.
54. Nagata N, Shimizu H, Ami Y, Tano Y, Harashima A, Suzaki Y, Sato Y, Miyamura T, Sata T, Iwasaki T. 2002. Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J. Med. Virol. 67:207-216.
55. Shiroki K, Kato H, Koike S, Odaka T, Nomoto A. 1993. Temperaturesensitive mouse cell factors for strand-specific initiation of poliovirus RNA synthesis. J. Virol. 67:3989-3996.
56. Hatakeyama S, Sakai-Tagawa Y, Kiso M, Goto H, Kawakami C, Mitamura K, Sugaya N, Suzuki Y, Kawaoka Y. 2005. Enhanced expression of an alpha2,6-linked sialic acid onMDCKcells improves isolation of human influenza viruses and evaluation of their sensitivity to a neuraminidase inhibitor. J. Clin. Microbiol. 43:4139-4146.
57. Yamayoshi S, Noda T, Ebihara H, Goto H, Morikawa Y, Lukashevich IS, Neumann G, Feldmann H, Kawaoka Y. 2008. Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. Cell Host Microbe 3:168-177.
58. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 27:493-499.
59. Arita M, Takebe Y, Wakita T, Shimizu H. 2010. A bifunctional antienterovirus compound that inhibits replication and the early stage of enterovirus 71 infection. J. Gen. Virol. 91:2734-2744.
60. Dierssen U, Rehren F, Henke-Gendo C, Harste G, Heim A. 2008. Rapid routine detection of enterovirus RNA in cerebrospinal fluid by a one-step real-time RT-PCR assay. J. Clin. Virol. 42:58-64.
61. Kaplan G, Freistadt MS, Racaniello VR. 1990. Neutralization of poliovirus by cell receptors expressed in insect cells. J. Virol. 64:4697-4702.
62. Liu CC, Guo MS, Lin FH, Hsiao KN, Chang KH, Chou AH, Wang YC, Chen YC, Yang CS, Chong PC. 2011. Purification and characterization of enterovirus 71 viral particles produced from Vero cells grown in a serumfree microcarrier bioreactor system. PLoS One 6:e20005. doi:10.1371 /journal.pone.0020005.
63. Miyamura K, Nishimura Y, Abo M, Wakita T, Shimizu H. 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.
64. Garriga D, Pickl-Herk A, Luque D, Wruss J, Caston JR, Blaas D, Verdaguer N. 2012. Insights into minor group rhinovirus uncoating: the X-ray structure of the HRV2 empty capsid. PLoS Pathog. 8:e1002473. doi: 10.1371/journal.ppat.1002473.
65. Bostina M, Levy H, Filman DJ, Hogle JM. 2011. Poliovirus RNA is released from the capsid near a twofold symmetry axis. J. Virol. 85:776-783.
66. Lin TY, Hsia SH, Huang YC, Wu CT, Chang LY. 2003. Proinflammatory cytokine reactions in enterovirus 71 infections of the central nervous system. Clin. Infect. Dis. 36:269-274.
67. Wang SM, Lei HY, Huang KJ, Wu JM, Wang JR, Yu CK, Su IJ, Liu CC. 2003. Pathogenesis of enterovirus 71 brainstem encephalitis in pediatric patients: roles of cytokines and cellular immune activation in patients with pulmonary edema. J. Infect. Dis. 188:564-570.