Enterovirus 71-induced autophagy increases viral replication and pathogenesis in a suckling mouse model

Journal of Biomedical Science

Volumn 21, Issue 1, 2014, Pages

  Lee, Ying Ray ^a   Wang, Po Shun ^b   Wang, Jen Ren ^b   Liu, Hsiao Sheng ^b  

^a CHIA YI CHRISTIAN HOSPITAL   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Amphisome; Autophagy; EV71; Suckling mice

Indexed keywords

3 METHYLADENINE; AMMONIUM CHLORIDE; NONSTRUCTURAL PROTEIN 2; PROTEIN 2C; PROTEIN LC3; PROTEIN VP1; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; VINBLASTINE; VIRAL PROTEIN; ANTINEOPLASTIC AGENT; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; VIRUS PROTEIN;

ACIDIFICATION; AMPHISOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN INFECTION; CELL FUSION; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; ENTEROVIRUS A71; ENTEROVIRUS INFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INOCULATION; INTRACRANIAL DRUG ADMINISTRATION; MORTALITY; MOUSE; NEUROBLASTOMA CELL LINE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RHABDOMYOSARCOMA CELL LINE; SUCKLING ANIMAL; VIRUS PATHOGENESIS; VIRUS REPLICATION; WEIGHT REDUCTION; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; ENTEROVIRUS A; GENE EXPRESSION REGULATION; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; NEWBORN; PHYSIOLOGY; TUMOR CELL LINE;

AMMONIUM CHLORIDE; ANIMALS; ANIMALS, NEWBORN; ANTINEOPLASTIC AGENTS, PHYTOGENIC; AUTOPHAGY; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ENTEROVIRUS A, HUMAN; GENE EXPRESSION REGULATION, VIRAL; HUMANS; MICE; MICE, INBRED ICR; MICROTUBULE-ASSOCIATED PROTEINS; VINBLASTINE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84925884548     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Schmidt NJ, Lennette EH, Ho HH: An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis 1974, 129: 304-309.
2. 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, Rodin V: Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol 1979, 60: 329-340.
3. Gilbert GL, Dickson KE, Waters MJ, Kennett ML, Land SA, Sneddon M: Outbreak of enterovirus 71 infection in Victoria, Australia, with a high incidence of neurologic involvement. Pediatr Infect Dis J 1988, 7: 484-488.
4. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shih SR: An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N Engl J Med 1999, 341: 929-935.
5. Fujimoto T, Chikahira M, Yoshida S, Ebira H, Hasegawa A, Totsuka A, Nishio O: 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 2002, 46: 621-627.
6. Yang F, Ren L, Xiong Z, Li J, Xiao Y, Zhao R, He Y, Bu G, Zhou S, Wang J, Qi J: Enterovirus 71 outbreak in the People's Republic of China in 2008. J Clin Microbiol 2009, 47: 2351-2352.
7. Chang LY, Lin TY, Huang YC, Tsao KC, Shih SR, Kuo ML, Ning HC, Chung PW, Kang CM: Comparison of enterovirus 71 and coxsackie-virus A16 clinical illnesses during the Taiwan enterovirus epidemic, 1998. Pediatr Infect Dis J 1999, 18: 1092-1096.
8. McMinn PC: An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 2002, 26: 91-107.
9. Hsueh C, Jung SM, Shih SR, Kuo TT, Shieh WJ, Zaki S, Lin TY, Chang LY, Ning HC, Yen DC: Acute encephalomyelitis during an outbreak of enterovirus type 71 infection in Taiwan: report of an autopsy case with pathologic, immunofluorescence, and molecular studies. Mod Pathol 2000, 13: 1200-1205.
10. Yan JJ, Wang JR, Liu CC, Yang HB, Su IJ: 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 2000, 17: 13-22.
11. Kuo RL, Kung SH, Hsu YY, Liu WT: Infection with enterovirus 71 or expression of its 2A protease induces apoptotic cell death. J Gen Virol 2002, 83: 1367-1376.
12. Li ML, Hsu TA, Chen TC, Chang SC, Lee JC, Chen CC, Stollar V, Shih SR: The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology 2002, 293: 386-395.
13. Liang CC, Sun MJ, Lei HY, Chen SH, Yu CK, Liu CC, Wang JR, Yeh TM: Human endothelial cell activation and apoptosis induced by enterovirus 71 infection. J Med Virol 2004, 74: 597-603.
14. Nagata N, Shimizu H, Ami Y, Tano Y, Harashima A, Suzaki Y, Sato Y, Miyamura T, Sata T, Iwasaki T: Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol 2002, 67: 207-216.
15. Chen YC, Yu CK, Wang YF, Liu CC, Su IJ, Lei HY: A murine oral enterovirus 71 infection model with central nervous system involvement. J Gen Virol 2004, 85: 69-77.
16. Wang YF, Chou CT, Lei HY, Liu CC, Wang SM, Yan JJ, Su IJ, Wang JR, Yeh TM, Chen SH, Yu CK: A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J Virol 2004, 78: 7916-7924.
17. Liu L, Zhao H, Zhang Y, Wang J, Che Y, Dong C, Zhang X, Na R, Shi H, Jiang L, Wang L, Xie Z, Cui P, Xiong X, Liao Y, Zhao S, Gao J, Tang D, Li Q: Neonatal rhesus monkey is a potential animal model for studying pathogenesis of EV71 infection. Virology 2011, 412: 91-100.
18. Chen H, Zhang Y, Yang E, Liu L, Che Y, Wang J, Zhao H, Tang D, Dong C, Yang L, Shen D, Wang X, Liao Y, Wang L, Na R, Liang Y, Li Q: The effect of enterovirus 71 immunization on neuropathogenesis and protein expression profiles in the thalamus of infected rhesus neonates. Virology 2012, 432: 417-426.
19. Klionsky DJ: The molecular machinery of autophagy: unanswered questions. J Cell Sci 2005, 118: 7-18.
20. Kundu M, Thompson CB: Autophagy: basic principles and relevance to disease. Annu Rev Pathol 2008, 3: 427-455.
21. Levine B, Kroemer G: Autophagy in the pathogenesis of disease. Cell 2008, 132: 27-42.
22. Panyasrivanit M, Khakpoor A, Wikan N, Smith DR: Linking dengue virus entry and translation/replication through amphisomes. Autophagy 2009, 5: 434-435.
23. Khakpoor A, Panyasrivanit M, Wikan N, Smith DR: A role for autophagolysosomes in dengue virus 3 production in HepG2 cells. J Gen Virol 2009, 90: 1093-1103.
24. Xie Z, Klionsky DJ: Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007, 9: 1102-1109.
25. Espert L, Codogno P, Biard-Piechaczyk M: Involvement of autophagy in viral infections: antiviral function and subversion by viruses. J Mol Med (Berl) 2007, 85: 811-823.
26. Talloczy Z, Virgin HW, Levine B: PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2006, 2: 24-29.
27. Sinha S, Colbert CL, Becker N, Wei Y, Levine B: Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 2008, 4: 989-997.
28. Ku B, Woo JS, Liang C, Lee KH, Hong HS, E X, Kim KS, Jung JU, Oh BH: Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog 2008, 4: e25.
29. Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K: Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 2005, 3: e156.
30. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR: Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 2004, 279: 10136-10141.
31. Paludan C, Schmid D, Landthaler M, Vockerodt M, Kube D, Tuschl T, Munz C: Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 2005, 307: 593-596.
32. Lee YR, Lei HY, Liu MT, Wang JR, Chen SH, Jiang-Shieh YF, Lin YS, Yeh TM, Liu CC, Liu HS: Autophagic machinery activated by dengue virus enhances virus replication. Virology 2008, 374: 240-248.
33. Ait-Goughoulte M, Kanda T, Meyer K, Ryerse JS, Ray RB, Ray R: Hepatitis C virus genotype 1a growth and induction of autophagy. J Virol 2008, 82: 2241-2249.
34. Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, Luo H: Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 2008, 82: 9143-9153.
35. Espert L, Denizot M, Grimaldi M, Robert-Hebmann V, Gay B, Varbanov M, Codogno P, Biard-Piechaczyk M: Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 2006, 116: 2161-2172.
36. Huang SC, Chang CL, Wang PS, Tsai Y, Liu HS: Enterovirus 71-induced autophagy detected in vitro and in vivo promotes viral replication. J Med Virol 2009, 81: 1241-1252.
37. Lee HK, Iwasaki A: Autophagy and antiviral immunity. Curr Opin Immunol 2008, 20: 23-29.
38. Lee YR, Hu HY, Kuo SH, Lei HY, Lin YS, Yeh TM, Liu CC, Liu HS: Dengue virus infection induces autophagy: an in vivo study. J Biomed Sci 2013, 20: 65.
39. Tang WF, Yang SY, Wu BW, Jheng JR, Chen YL, Shih CH, Lin KH, Lai HC, Tang P, Horng JT: Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication. J Biol Chem 2007, 282: 5888-5898.
40. Tang H, Da L, Mao Y, Li Y, Li D, Xu Z, Li F, Wang Y, Tiollais P, Li T, Zhao M: Hepatitis B virus X protein sensitizes cells to starvation-induced autophagy via up-regulation of beclin 1 expression. Hepatology 2009, 49: 60-71.
41. Taylor MP, Kirkegaard K: Modification of cellular autophagy protein LC3 by poliovirus. J Virol 2007, 81: 12543-12553.
42. McLean JE, Wudzinska A, Datan E, Quaglino D, Zakeri Z: Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. J Biol Chem 2011, 286: 22147-22159.
43. Greninger AL, Knudsen GM, Betegon M, Burlingame AL, Derisi JL: The 3A protein from multiple picornaviruses utilizes the golgi adaptor protein ACBD3 to recruit PI4KIIIbeta. J Virol 2012, 86: 3605-3616.
44. Takahashi MN, Jackson W, Laird DT, Culp TD, Grose C, Haynes JI 2nd, Benetti L: Varicella-zoster virus infection induces autophagy in both cultured cells and human skin vesicles. J Virol 2009, 83: 5466-5476.
45. Klein KA, Jackson WT: Picornavirus subversion of the autophagy pathway. Viruses 2011, 3: 1549-1561.
46. Sun MX, Huang L, Wang R, Yu YL, Li C, Li PP, Hu XC, Hao HP, Ishag HA, Mao X: Porcine reproductive and respiratory syndrome virus induces autophagy to promote virus replication. Autophagy 2012, 8: 1434-1447.
47. Yoon SY, Ha YE, Choi JE, Ahn J, Lee H, Kweon HS, Lee JY, Kim DH: Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. J Virol 2008, 82: 11976-11978.
48. Gannage M, Dormann D, Albrecht R, Dengjel J, Torossi T, Ramer PC, Lee M, Strowig T, Arrey F, Conenello G, Pypaert M, Andersen J, Garcia-Sastre A, Munz C: Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 2009, 6: 367-380.
49. Kyei GB, Dinkins C, Davis AS, Roberts E, Singh SB, Dong C, Wu L, Kominami E, Ueno T, Yamamoto A, Federico M, Panganiban A, Vergne I, Deretic V: Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 2009, 186: 255-268.
50. Martyniszyn L, Szulc L, Boratynska A, Niemialtowski MG: Beclin 1 is involved in regulation of apoptosis and autophagy during replication of ectromelia virus in permissive L929 cells. Arch Immunol Ther Exp (Warsz) 2011, 59: 463-471.
51. McLean JE, Datan E, Matassov D, Zakeri ZF: Lack of Bax prevents influenza A virus-induced apoptosis and causes diminished viral replication. J Virol 2009, 83: 8233-8246.
52. Joubert PE, Werneke SW, de la Calle C, Guivel-Benhassine F, Giodini A, Peduto L, Levine B, Schwartz O, Lenschow DJ, Albert ML: Chikungunya virus-induced autophagy delays caspase-dependent cell death. J Exp Med 2012, 209: 1029-1047.
53. Xi X, Zhang X, Wang B, Wang T, Wang J, Huang H, Jin Q, Zhao Z: The interplays between autophagy and apoptosis induced by enterovirus 71. PLoS One 2013, 8: e56966.
54. van der Schaar HM, Rust MJ, Chen C, van der Ende-Metselaar H, Wilschut J, Zhuang X, Smit JM: Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 2008, 4: e1000244.
55. Zaitseva E, Yang ST, Melikov K, Pourmal S, Chernomordik LV: Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog 2010, 6: e1001131.
56. Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, Ong CN, Codogno P, Shen HM: Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010, 285: 10850-10861. doi: 10.1186/s12929-014-0080-4