Scavenger receptor B2 as a receptor for hand, foot, and mouth disease and severe neurological diseases

Frontiers in Microbiology

Volumn 3, Issue FEB, 2012, Pages

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

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Ev71; HFMD; Neurological disease; Scarb2

Indexed keywords

EID: 84875780953     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00032     Document Type: Review

References (68)

1. Abe, S., Ota, Y., Koike, S., Kurata, T., Horie, H., Nomura, T., Hashizume, S., and Nomoto, A. (1995). Neurovirulence test for oral live polio vaccines using poliovirus-sensitive transgenic mice. Virology 206, 1075-1083.
2. Ahmad, K. (2000). Hand, foot, and mouth disease outbreak reported in Singapore. Lancet 356, 1338.
3. Arita, M., Ami, Y., Wakita, T., and Shimizu, H. (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.
4. Arita, M., Nagata, N., Iwata, N., Ami, Y., Suzaki, Y., Mizuta, K., Iwasaki, T., Sata, T., Wakita, T., and Shimizu, H. (2007). An attenuated strain of enterovirus 71 belonging to genotype a showed a broad spectrum of antigenicity with attenuated neurovirulence in cynomolgus monkeys.J. Virol. 81, 9386-9395.
5. Arita, M., Shimizu, H., Nagata, N., Ami, Y., Suzaki, Y., Sata, T., Iwasaki, T., and Miyamura, T. (2005). Temperature-sensitive mutants of enterovirus 71 show attenuation in cynomolgus monkeys. J. Gen. Virol. 86, 1391-1401.
6. Bergelson, J. M. (2010). Receptors, in The Picornaviruses, eds E. Ehrenfeld, E. Domingo, and R. P. Roos (Washington, DC: ASM Press), 73-86.
7. Berkovic, S. F., Dibbens, L. M., Oshlack, A., Silver, J. D., Katerelos, M., Vears, D. F., Lullmann-Rauch, R., Blanz, J., Zhang, K. W., Stankovich, J., Kalnins, R. M., Dowling, J. P., Andermann, E., Andermann, F., Faldini, E., D'Hooge, R., Vadlamudi, L., Macdonell, R. A., Hodgson, B. L., Bayly, M. A., Savige, J., Mulley, J. C., Smyth, G. K., Power, D. A., Saftig, P., and Bahlo, M. (2008). Array-based gene discovery with three unrelated subjects shows SCARB2/LIMP-2 deficiency causes myoclonus epilepsy and glomerulosclerosis. Am. J. Hum. Genet. 82, 673-684.
8. Blanz, J., Groth, J., Zachos, C., Wehling, C., Saftig, P., and Schwake, M. (2010). Disease-causing mutations within the lysosomal integral membrane protein type 2 (LIMP-2) reveal the nature of binding to its ligand beta-glucocerebrosidase. Hum. Mol. Genet. 19,563-572.
9. Calvo, D., Dopazo, J., and Vega, M. A. (1995). The CD36, CLA-1 (CD36L1), and LIMPII (CD36L2) gene family: cellular distribution, chromosomal location, and genetic evolution. Genomics 25, 100-106.
10. Chan, L. G., Parashar, U. D., Lye, M. S., Ong,F.G.,Zaki,S.R., Alexander, J. P., Ho, K. K., Han, L. L., Pallansch, M. A., Suleiman, A. B., Jegathesan, M., and Anderson, L. J. (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.
11. 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., and Li, W. (2012). Molecular determinants of enterovirus 71 viral entry: a cleft around Q172 on VP1 interacts with a variable region on scavenge receptor B 2. J. Biol Chem. [Epub ahead of print].
12. Chen,Y. C.,Yu, C. K., Wang, Y E, Liu, C. C., Su, I. J., and Lei, H. Y (2004). A murine oral enterovirus 71 infection model with central nervous system involvement.J. Gen. Virol. 85,69-77.
13. Chua, B. H., Phuektes, P., Sanders, S. A., Nicholls, P. K., and McMinn, P. C. (2008). The molecular basis of mouse adaptation by human enterovirus 71. J. Gen. Virol. 89, 1622-1632.
14. Chumakov, K. M., Lavrova, I. K., Martianova, L. I., Korolev, M. B., Bashkirtsev, V. N., and Voroshilova, M. K. (1979a). Investigation of physicochemical properties of Bulgarian strain 258 of enterovirus type 71. Brief report. Arch. Virol. 60, 359-362.
15. Chumakov, M., Voroshilova, M., Shindarov, L., Lavrova, I., Gracheva, L., Koroleva, G., Vasilenko, S., Brodvarova, I., Nikolova, M., Gyurova, S., Gacheva, M., Mitov, G., Ninov, N., Tsylka, E., Robinson, I., Frolova, M., Bashkirtsev, V., Martiyanova, L., and Rodin, V (1979b). Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch. Virol. 60, 329-340.
16. De, W., Changwen, K., Wei, L., Monagin, C., Jin, Y., Cong, M., Hanri, Z., and Jun, S. (2011). A large outbreak of hand, foot, and mouth disease caused by EV71 and CAV16 in Guangdong, China, 2009. Arch. Virol. 156, 945-953.
17. Eskelinen, E. L., Tanaka, Y., and Saftig, P. (2003). At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13, 137-145.
18. Evans, D. M., Dunn, G., Minor, P. D., Schild, G. C., Cann, A. J., Stanway, G., Almond, J. W., Currey, K., and Maizel, J. V. Jr. (1985). Increased neurovirulence associated with a single nucleotide change in a non-coding region of the Sabin type 3 polio vaccine genome. Nature 314, 548-550.
19. Fujimoto, T., Chikahira, M., Yoshida, S., Ebira, H., Hasegawa, A., Totsuka, A., and 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.
20. Gamp, A. C., Tanaka, Y., Lullmann-Rauch, R., Wittke, D., D'hooge, R., De Deyn, P. P., Moser, T., Maier, H., Hartmann, D., Reiss, K., Illert, A. L., Von Figura, K., and Saftig, P. (2003). LIMP-2/LGP85 deficiency causes ureteric pelvic junction obstruction, deafness and peripheral neuropathy in mice. Hum. Mol. Genet. 12, 631-646.
21. Hagiwara, A., Yoneyama, T., and Hashimoto, I. (1983). Isolation of a temperature-sensitive strain of enterovirus 71 with reduced neurovirulence for monkeys. J Gen. Virol. 64(PT 2), 499-502.
22. Hagiwara, A., Yoneyama, T., Takami, S., and Hashimoto, I. (1984). Genetic and phenotypic characteristics of enterovirus 71 isolates from patients with encephalitis and with hand, foot and mouth disease. Arch. Virol. 79,273-283.
23. Han, J. F., Cao, R. Y., Deng, Y Q., Tian, X., Jiang, T., Qin, E. D., and Qin, C. F. (2010). Antibody dependent enhancement infection of enterovirus 71 in vitro and in vivo. Virol. J. 8, 106.
24. Hashimoto, I., and Hagiwara, A. (1982). Pathogenicity of a poliomyelitis-like disease in monkeys infected orally with enterovirus 71: a model for human infection. Neuropathol. Appl. Neurobiol. 8, 149-156.
25. Hashimoto, I., Hagiwara, A., and Kodama, H. (1978). Neurovirulence in cynomolgus monkeys of enterovirus 71 isolated from a patient with hand, foot and mouth disease. Arch. Virol. 56,257-261.
26. Ho, M., Chen, E. R., Hsu, K. H., Twu, S. J., Chen, K. T., Tsai, S. F., Wang, J. R., and Shih, S. R. (1999). An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med. 341, 929-935.
27. Horie, H., Koike, S., Kurata, T., Sato-Yoshida, Y., Ise, I., Ota, Y., Abe, S., Hioki, K., Kato, H., Taya, C., Nomura, T., Hashizume, S., Yonekawa, H., and Nomoto, A. (1994). Transgenic mice carrying the human poliovirus receptor: new animal models for study of poliovirus neurovirulence. J. Virol. 68, 681-688.
28. Huang, S. W., Wang, Y. F., Yu, C. K., Su, I. J., and Wang, J. R. (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.
29. Hussain, K. M., Leong, K. L., Ng, M. M., and Chu, J. J. (2011). The essential role of clathrin-mediated endocytosis in the infectious entry of human enterovirus 71. J. Biol Chem. 286, 309-321.
30. Kawamura, N., Kohara, M., Abe, S., Komatsu, T., Tago, K., Arita, M., and Nomoto, A. (1989). Determinants in the 5' noncoding region of poliovirus Sabin 1 RNA that influence the attenuation phenotype. J. Virol. 63,1302-1309.
31. Khong, W. X., Yan, B., Yeo, H., Tan, E. L., Lee, J. J., Ng, J. K., Chow, V. T., and Alonso, S. (2012). A non mouse-adapted enterovirus 71 (EV71) strain exhibits neurotropism causing neurological manifestations in a novel mouse model of EV71 infection.J. Virol. 86,2121-2131.
32. Koike, S., Taya, C., Kurata, T., Abe, S., Ise, I., Yonekawa, H., and Nomoto, A. (1991). Transgenic mice suscep tible to poliovirus. Proc. Natl. Acad. Sci. U.S.A. 88,951-955.
33. Komatsu, H., Shimizu, Y., Takeuchi, Y., Ishiko, H., and Takada, H. (1999). Outbreak of severe neurologic involvement associated with enterovirus 71 infection. Pediatr. Neurol. 20, 17-23.
34. Kuronita, T., Eskelinen, E. L., Fujita, H., Saftig, P., Himeno, M., and Tanaka, Y (2002). A role for the lysosomal membrane protein LGP85 in the biogenesis and maintenance of endosomal and lysosomal morphology.J. Cell. Sci. 115,4117-4131.
35. Le Borgne, R., Planque, N., Martin, P., Dewitte, F., Saule, S., and Hoflack, B (2001). The AP-3-dependent tar geting of the melanosomal glycoprotein QNR-71 requires a dileucine-based sorting signal. J Cell. Sci. 114, 2831-2841.
36. Li, R., Zou, Q., Chen, L., Zhang, H., and Wang, Y (2011). Molecular analysis of virulent determinants of enterovirus 71. PLoS ONE 6, e26237. doi:10.1371/journal.pone.0026237
37. Liu, J., Dong, W., Quan, X., Ma, C., Qin, C., and Zhang, L. (2011). Transgenic expression of human P-selectin glycoprotein ligand-1 is not sufficient for enterovirus 71 infection in mice. Arch. Virol. doi: 10.1007/s00705-011-1198-2
38. Lum, L. C., Wong, K. T., Lam, S. K., Chua, K. B., Goh, A. Y., Lim, W.L., Ong, B. B., Paul, G., Abubakar, S., and Lambert, M. (1998). Fatal enterovirus 71 encephalomyelitis./Pediatr. 133,795-798.
39. McMinn, P., Lindsay, K., Perera, D., Chan, H. M., Chan, K. P., and Cardosa, M. J. (2001a). Phylogenetic analysis of enterovirus 71 strains isolated during linked epidemics in Malaysia, Singapore, and Western Australia. J. Virol. 75, 7732-7738.
40. McMinn, P., Stratov, I., Nagarajan, L., and Davis, S. (2001b). Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin. Infect. Dis. 32, 236-242.
41. Melnick, J. L. (1984). Enterovirus type 71 infections: a varied clinical pattern sometimes mimicking paralytic poliomyelitis. Rev. Infect. Dis. 6(SUPPL.2),S387-S390.
42. Miyamura, K., Nishimura, Y., Abo, M., Wakita, T., and 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.
43. Mizuta, K., Abiko, C., Murata, T., Matsuzaki, Y., Itagaki, T., Sanjoh, K., Sakamoto, M., Hongo, S., Murayama, S., and Hayasaka, K. (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.
44. Mizuta, K., Aoki, Y., Suto, A., Ootani, K., Katsushima, N., Itagaki, T., Ohmi, A., Okamoto, M., Nishimura, H., Matsuzaki, Y., Hongo, S., Sugawara, K., Shimizu, H., and Ahiko, T. (2009). Cross-antigenicity among EV71 strains from different genogroups isolated in Yamagata, Japan, between 1990 and 2007. Vaccine 27, 3153-3158.
45. Nagata, N., Iwasaki, T., Ami, Y., Tano, Y., Harashima, A., Suzaki, Y., Sato, Y., Hasegawa, H., Sata, T., Miyamura, T., and Shimizu, H. (2004). 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. 85, 2981-2989.
46. Nagata, N., Shimizu, H., Ami, Y., Tano, Y., Harashima, A., Suzaki, Y., Sato, Y., Miyamura, T., Sata, T., and Iwasaki, T. (2002). Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71.J. Med. Virol. 67, 207-216.
47. Nishimura, Y., Shimojima, M., Tano, Y., Miyamura, T., Wakita, T., and Shimizu, H. (2009). Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat. Med. 15, 794-797.
48. Oberste, M. S., Jiang, X., Maher, K., Nix, W A., and Jiang, B. (2008). The complete genome sequences for three simian enteroviruses isolated from captive primates. Arch. Virol. 153, 2117-2122.
49. Oberste, M. S., Maher, K., and Pallansch, M. A. (2007). Complete genome sequences for nine simian enteroviruses./Gen. Virol. 88, 3360-3372.
50. Omata, T., Kohara, M., Kuge, S., Komatsu, T., Abe, S., Semler, B. L., Kameda, A., Itoh, H., Arita, M., Wimmer,E.,and Nomoto,A. (1986). Genetic analysis of the attenuation phenotype of poliovirus type 1./Virol. 58, 348-358.
51. Ong, K. C., Badmanathan, M., Devi, S., Leong, K. L., Cardosa, M. J., and Wong, K. T. (2008). Pathologic characterization of a murine model of human enterovirus 71 encephalomyelitis./Neuropathol. Exp. Neurol. 67, 532-542.
52. Pallansch, M., and Roos, R. (2007). Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses, in Fields Virology, 5th Edn, eds D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (Philadelphia: Lippincott Williams &Wilkins), 839-893.
53. Qiu, J. (2008). Enterovirus 71 infection: a new threat to global public health? Lancet Neurol. 7, 868-869.
54. Ren, R. B., Costantini, F., Gorgacz, E. J., Lee, J.J.,and Racaniello,V.R. (1990). Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell 63, 353-362.
55. Rodionov, D. G., Honing, S., Silye, A., Kongsvik, T. L., Von Figura, K., and Bakke, O. (2002). Structural requirements for interactions between leucine-sorting signals and clathrin-associated adaptor protein complex AP3./Biol. Chem. 277, 47436-47443.
56. Schmidt, N. J., Lennette, E. H., and Ho, H. H. (1974). An apparently new enterovirus isolated from patients with disease of the central nervous system./Infect. Dis. 129, 304-309.
57. Shieh, W J., Jung, S. M., Hsueh, C., Kuo, T. T., Mounts, A., Parashar, U., Yang, C. F., Guarner, J., Ksiazek, T. G., Dawson, J., Goldsmith, C., Chang, G. J., Oberste, S. M., Pallansch, M. A., Anderson, L. J., and Zaki, S. R. (2001). Pathologic studies of fatal cases in outbreak of hand, foot, and mouth disease, Taiwan. Emerging Infect. Dis. 7, 146-148.
58. Wang, J. R., Tuan, Y C, Tsai, H. P., Yan, J. J., Liu, C. C., and Su, I. J. (2002). Change of major genotype of enterovirus 71 in outbreaks of hand-foot-and-mouth disease in Taiwan between 1998 and 2000. J Clin. Microbiol. 40,10-15.
59. Wang, S. M., Liu, C. C., Tseng, H. W., Wang, J. R., Huang, C. C., Chen, Y. J., Yang, Y J., Lin, S. J., and Yeh, T. E. (1999). Clinical spectrum of enterovirus 71 infection in children in southern Taiwan, with an emphasis on neurological complications. Clin. Infect. Dis. 29,184-190.
60. Wang, W., Duo, J., Liu, J., Ma, C., Zhang, L., Wei, Q., and Qin, C. (2011). A mouse muscle-adapted enterovirus 71 strain with increased virulence in mice. Microbes Infect. 13, 862-870.
61. Wang, Y E, Chou, C. T., Lei, H. Y., Liu, C. C., Wang, S. M., Yan, J. J., Su, I. J., Wang, J. R., Yeh, T. M., Chen, S. H., and Yu, C. K. (2004). A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection./Virol. 78, 7916-7924.
62. Westrop, G. D., Wareham, K. A., Evans, D. M., Dunn, G., Minor, P. D., Magrath, D. I., Taffs, F., Marsden, S., Skinner, M. A., Schild, G. C., and Almond, J. W. (1989). Genetic basis of attenuation of the Sabin type 3 oral poliovirus vaccine. J Virol. 63, 1338-1344.
63. Yamayoshi, S., and Koike, S. (2011). Identification of a human SCARB2 region that is important for enterovirus 71 binding and infection. J Virol. 85, 4937-4946.
64. Yamayoshi, S.,Yamashita,Y., Li, J., Hanagata, N., Minowa, T., Takemura, T., and Koike, S. (2009). Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat. Med. 15, 798-801.
65. Yang, B., Chuang, H., and Yang, K. D. (2009). Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol. J. 6, 141.
66. Yang, S. L., Chou, Y. T., Wu, C. N., and Ho, M. S. (2011). Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity./Virol. 85, 11809-11820.
67. Yu, C. K., Chen, C. C., Chen, C. L., Wang, J. R., Liu, C. C., Yan, J. J., and Su, I. J. (2000). Neutralizing antibody provided protection against enterovirus type 71 lethal challenge in neonatal mice./Biomed. Sci. 7, 523-528.
68. Zhang, Y., Cui, W., Liu, L., Wang, J., Zhao, H., Liao, Y., Na, R., Dong, C.,Wang, L., Xie, Z., Gao, J., Cui, P., Zhang, X., and Li, Q. (2011). Pathogenesis study of enterovirus 71 infection in rhesus monkeys. Lab. Invest. 91,1337-1350.