Transgenic mouse model for the study of enterovirus 71 neuropathogenesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 36, 2013, Pages 14753-14758

  Fujii, Ken ^a   Nagata, Noriyo ^b   Sato, Yuko ^b   Ong, Kien Chai ^c   Wong, Kum Thong ^c   Yamayoshi, Seiya ^a   Shimanuki, Midori ^a   Shitara, Hiroshi ^a   Taya, Choji ^a   Koike, Satoshi ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Neurotropism; Picornavirus; Viral receptor

Indexed keywords

CELL RECEPTOR; SCAVENGER RECEPTOR B; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; SCARB2 PROTEIN, HUMAN; SCAVENGER RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASIA; BRAIN; BRAIN STEM; CEREBELLUM; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENCEPHALOMYELITIS; ENTEROVIRUS 71; EPIDEMIC; HAND FOOT AND MOUTH DISEASE; HAPLORHINI; HUMAN; HYPOTHALAMUS; MORTALITY; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; THALAMUS; TRANSGENIC MOUSE; VIRUS REPLICATION; ANIMAL; CENTRAL NERVOUS SYSTEM DISEASE; CHLOROCEBUS AETHIOPS; DISEASE MODEL; ENTEROVIRUS; ENTEROVIRUS INFECTION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TIME; TUMOR CELL LINE; VERO CELL LINE; VIROLOGY; WESTERN BLOTTING;

ANIMALIA; HUMAN ENTEROVIRUS 71; MUS; MUS MUSCULUS; PICORNAVIRIDAE;

ANIMALS; BLOTTING, WESTERN; BRAIN; CELL LINE, TUMOR; CENTRAL NERVOUS SYSTEM DISEASES; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; RECEPTORS, SCAVENGER; SPINAL CORD; TIME FACTORS; VERO CELLS;

EID: 84883418885     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1217563110     Document Type: Article

References (58)

1. 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(3):304-309.
2. Pallansch M, Roos R (2007) Enteroviruses: Polioviruses, Coxsackieviruses, Echoviruses, and newer Enteroviruses. Fields Virology, eds Knipe DM et al. (Lippincott Williams & Wilkins, Philadelphia), 5th Ed, Vol 1, pp 839-893.
3. Ho M, et al.; Taiwan Enterovirus Epidemic Working Group (1999) An epidemic of enterovirus 71 infection in Taiwan. N Engl J Med 341(13):929-935. (Pubitemid 29441546)
4. Huang CC, et al. (1999) Neurologic complications in children with enterovirus 71 infection. N Engl J Med 341(13):936-942.
5. Wong KT, et al. (2012) Enterovirus 71 encephalomyelitis and Japanese encephalitis can be distinguished by topographic distribution of inflammation and specific intraneuronal detection of viral antigen and RNA. Neuropathol Appl Neurobiol 38(5):443-453.
6. Wong KT, et al. (2008) The distribution of inflammation and virus in human enterovirus 71 encephalomyelitis suggests possible viral spread by neural pathways. J Neuropathol Exp Neurol 67(2):162-169.
7. Shindarov LM, et al. (1979) Epidemiological, clinical, and pathomorphological characteristics of epidemic poliomyelitis-like disease caused by enterovirus 71. J Hyg Epidemiol Microbiol Immunol 23(3):284-295. (Pubitemid 10151251)
8. Nagy G, Takátsy S, Kukán E, Mihály I, Dömök I (1982) Virological diagnosis of enterovirus type 71 infections: Experiences gained during an epidemic of acute CNS diseases in Hungary in 1978. Arch Virol 71(3):217-227. (Pubitemid 12072656)
9. AbuBakar S, et al. (1999) Identification of enterovirus 71 isolates from an outbreak of hand, foot and mouth disease (HFMD) with fatal cases of encephalomyelitis in Malaysia. Virus Res 61(1):1-9.
10. Wang Y, et al. (2011) Hand, foot, and mouth disease in China: Patterns of spread and transmissibility. Epidemiology 22(6):781-792.
11. Hashimoto I, Hagiwara A, Kodama H (1978) Neurovirulence in cynomolgus monkeys of enterovirus 71 isolated from a patient with hand, foot and mouth disease. Arch Virol 56(3):257-261. (Pubitemid 8303880)
12. Hashimoto I, Hagiwara A (1982) Studies on the pathogenesis of and propagation of enterovirus 71 in Poliomyelitis-like disease in monkeys. Acta Neuropathol 58(2):125-132. (Pubitemid 12000125)
13. Hashimoto I, 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(2):149-156. (Pubitemid 12045034)
14. Nagata N, et al. (2002) Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol 67(2):207-216. (Pubitemid 34493434)
15. Nagata N, et al. (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(Pt 10):2981-2989. (Pubitemid 39360042)
16. Chumakov M, et al. (1979) Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol 60(3-4):329-340. (Pubitemid 9221445)
17. Chen YC, et al. (2004) A murine oral enterovirus 71 infection model with central nervous system involvement. J Gen Virol 85(Pt 1):69-77.
18. Wang YF, et al. (2004) A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J Virol 78(15):7916-7924.
19. Wang W, et al. (2011) A mouse muscle-adapted enterovirus 71 strain with increased virulence in mice. Microbes Infect 13(10):862-870.
20. Khong WX, et al. (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(4):2121-2131.
21. Bergelson JM (2010) Receptors. The Picornaviruses, eds Ehrenfeld E, Domingo E, Roos RP (ASM Press, Washington, DC), pp 73-86.
22. Ren RB, Costantini F, Gorgacz EJ, Lee JJ, Racaniello VR (1990) Transgenic mice expressing a human poliovirus receptor: A new model for poliomyelitis. Cell 63(2):353-362.
23. Koike S, et al. (1991) Transgenic mice susceptible to poliovirus. Proc Natl Acad Sci USA 88(3):951-955. (Pubitemid 21916142)
24. Bartlett NW, et al. (2008) Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat Med 14(2):199-204. (Pubitemid 351214556)
25. Yang B, Chuang H, Yang KD (2009) Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol J 6:141.
26. Yang SL, Chou YT, Wu CN, Ho MS (2011) Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J Virol 85(22):11809-11820.
27. Nishimura Y, et al. (2009) Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15(7):794-797.
28. Yamayoshi S, et al. (2009) Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 15(7):798-801.
29. Kuronita T, et al. (2002) A role for the lysosomal membrane protein LGP85 in the biogenesis and maintenance of endosomal and lysosomal morphology. J Cell Sci 115(Pt 21):4117- 4131.
30. Reczek D, et al. (2007) LIMP-2 is a receptor for lysosomal mannose-6-phosphatein-dependent targeting of beta-glucocerebrosidase. Cell 131(4):770-783. (Pubitemid 350087202)
31. Yamayoshi S, Koike S (2011) Identification of a human SCARB2 region that is important for enterovirus 71 binding and infection. J Virol 85(10):4937-4946.
32. Yamayoshi S, et al. (2012) Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J Virol 86(10):5686-5696.
33. Yamayoshi S, Ohka S, Fujii K, Koike S (2013) Functional comparison of SCARB2 and PSGL1 as receptors for enterovirus 71. J Virol 87(6):3335-3347.
34. Tabuchi N, Akasaki K, Sasaki T, Kanda N, Tsuji H (1997) Identification and characterization of a major lysosomal membrane glycoprotein, LGP85/LIMP II in mouse liver. J Biochem 122(4):756-763. (Pubitemid 27474945)
35. Gamp AC, et al. (2003) LIMP-2/LGP85 deficiency causes ureteric pelvic junction obstruction, deafness and peripheral neuropathy in mice. Hum Mol Genet 12(6):631-646.
36. Ritsch A, et al. (2004) Molecular characterization of rabbit scavenger receptor class B types I and II: Portal to central vein gradient of expression in the liver. J Lipid Res 45(2):214-222. (Pubitemid 38228818)
37. Liu J, et al. (2012) Transgenic expression of human P-selectin glycoprotein ligand-1 is not sufficient for enterovirus 71 infection in mice. Arch Virol 157(3):539-543.
38. Ranzenhofer ER, Dizon FC, Lipton MM, Steigman AJ (1958) Clinical paralytic poliomyelitis due to Coxsackie virus group A, type 7. N Engl J Med 259(4):182.
39. Helin I, Widell A, Borulf S, Walder M, Ulmsten U (1987) Outbreak of coxsackievirus A-14 meningitis among newborns in a maternity hospital ward. Acta Paediatr Scand 76(2):234-238. (Pubitemid 17051377)
40. Xu W, et al. (2012) Distribution of enteroviruses in hospitalized children with hand, foot and mouth disease and relationship between pathogens and nervous system complications. Virol J 9(1):8.
41. Samuda GM, Chang WK, Yeung CY, Tang PS (1987) Monoplegia caused by Enterovirus 71: An outbreak in Hong Kong. Pediatr Infect Dis J 6(2):206-208. (Pubitemid 17116144)
42. Melnick JL (1984) Enterovirus type 71 infections: A varied clinical pattern sometimes mimicking paralytic poliomyelitis. Rev Infect Dis 6(Suppl 2):S387-S390.
43. Lum LC, et al. (1998) Fatal enterovirus 71 encephalomyelitis. J Pediatr 133(6):795-798. (Pubitemid 28563953)
44. Wang SM, et al. (1999) Clinical spectrum of enterovirus 71 infection in children in southern Taiwan, with an emphasis on neurological complications. Clin Infect Dis 29(1):184-190.
45. Dong C, et al. (2011) Immunoprotection elicited by an enterovirus type 71 experimental inactivated vaccine in mice and rhesus monkeys. Vaccine 29(37):6269-6275.
46. Chang JY, et al. (2012) Selection and characterization of vaccine strain for Enterovirus 71 vaccine development. Vaccine 30(4):703-711.
47. Ong KC, Devi S, Cardosa MJ, Wong KT (2010) Formaldehyde-inactivated whole-virus vaccine protects a murine model of enterovirus 71 encephalomyelitis against disease. J Virol 84(1):661-665.
48. Lin YW, et al. (2013) Human SCARB2 transgenic mice as an infectious animal model for enterovirus 71. PLoS ONE 8(2):e57591.
49. Koike S, et al. (1994) Characterization of three different transgenic mouse lines that carry human poliovirus receptor gene - influence of the transgene expression on pathogenesis. Arch Virol 139(3-4):351-363.
50. Abe S, et al. (1995) Studies on neurovirulence in poliovirus-sensitive transgenic mice and cynomolgus monkeys for the different temperature-sensitive viruses derived from the Sabin type 3 virus. Virology 210(1):160-166.
51. Horie H, et al. (1994) Transgenic mice carrying the human poliovirus receptor: New animal models for study of poliovirus neurovirulence. J Virol 68(2):681-688. (Pubitemid 24022169)
52. Abe S, et al. (1995) Neurovirulence test for oral live poliovaccines using poliovirus-sensitive transgenic mice. Virology 206(2):1075-1083.
53. Dragunsky E, et al. (2003) Transgenic mice as an alternative to monkeys for neurovirulence testing of live oral poliovirus vaccine: Validation by a WHO collaborative study. Bull World Health Organ 81(4):251-260. (Pubitemid 36542141)
54. Kew O, et al. (2002) Outbreak of poliomyelitis in Hispaniola associated with circulating type 1 vaccine-derived poliovirus. Science 296(5566):356-359. (Pubitemid 34303692)
55. Jegouic S, et al. (2009) Recombination between polioviruses and co-circulating Coxsackie A viruses: Role in the emergence of pathogenic vaccine-derived polioviruses. PLoS Pathog 5(5):e1000412.
56. Shimizu H, 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(1):12-15. (Pubitemid 29414613)
57. Shimizu H, et al. (2004) Molecular epidemiology of enterovirus 71 infection in the Western Pacific Region. Pediatr Int 46(2):231-235. (Pubitemid 38526625)
58. Sickles GM, Mutterer M, Feorino P, Plager H (1955) Recently classified types of Coxsackie virus, group A: Behavior in tissue culture. Proc Soc Exp Biol Med 90(2):529-531.