Enterovirus 71 infection caused neuronal cell death and cytokine expression in cultured rat neural cells

IUBMB Life

Volumn 67, Issue 10, 2015, Pages 789-800

  Chang, Cheng Yi ^a,b   Li, Jian Ri ^c   Ou, Yen Chuan ^c   Chen, Wen Ying ^d   Liao, Su Lan ^c   Raung, Shue Ling ^c   Hsiao, An Lu ^c,d   Chen, Chun Jung ^c,d  

^a FENG YUAN HOSPITAL   (Taiwan)

^b CENTRAL TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^c TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

central nervous system; encephalitis; enterovirus; neuroinflammation; neurotoxicity

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYTOKINE; GLUTAMIC ACID; HERBIMYCIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PROTEIN TYROSINE KINASE; RANTES; SCAVENGER RECEPTOR B; SCAVENGER RECEPTOR CLASS B MEMBER 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; AGE; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BIOCHEMICAL ANALYSIS; CELL ACTIVATION; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EMBRYO; ENTEROVIRUS 71; ENTEROVIRUS INFECTION; FEMALE; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; MALE; MICROGLIA; NERVE CELL; NERVE CELL CULTURE; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS LOAD; ANIMAL; CELL CULTURE; CHLOROCEBUS AETHIOPS; ENTEROVIRUS A; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VERO CELL LINE; VIROLOGY;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CYTOKINES; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; FEMALE; MALE; NEURONS; RATS, SPRAGUE-DAWLEY; VERO CELLS;

EID: 84945122810     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1434     Document Type: Article

References (46)

1. Hsiung, G. D., and, Wang, J. R., (2000) Enterovirus infections with special reference to enterovirus 71. J. Microbiol. Immunol. Infect. 33, 1-8.
2. Ho, M., Chen, E. R., Hsu, K. H., Wu, S. J., Chen, K. T., et al., (1999) An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med. 341, 929-935.
3. Shimizu, H., Utama, A., Yoshii, K., Yoshida, H., Yoneyama, T., 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, 12-15.
4. Yan, J. J., Wang, J. R., Liu, C. C., Yang, H. B., and, Su, I. J., (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.
5. McMinn, P., Stratov, I., Nagarajan, L., and, Davis, S., (2001) 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.
6. Yang, F., Ren, L., Xiong, Z., Li, J., Xiao, Y., et al., (2009) Enterovirus 71 outbreak in the People's Republic of China in 2008. J. Clin. Microbiol. 47, 2351-2352.
7. Chen, Y. J., Meng, F. Y., Mao, Q., Li, J. X., Wang, H., et al., (2014) Clinical evaluation for batch consistency of an inactivated enterovirus 71 vaccine in a large-scale phase 3 clinical trial. Hum. Vaccin. Immunother. 10, 1366-1372.
8. Cao, L., Mao, F., Pang, Z., Yi, Y., Qiu, F., et al., (2015) Protective effect of enterovirus-71 (EV71) virus-like particle vaccine against lethal EV71 infection in a neonatal mouse model. Mol. Med. Rep. 12, 2473-2480.
9. Huang, C. C., Liu, C. C., Chang, Y. C., Chen, C. Y., Wang, S. T., et al., (1999) Neurologic complications in children with enterovirus 71 infection. N. Engl. J. Med. 341, 936-942.
10. Wang, S. M., Lei, H. Y., Huang, K. J., Wu, J. M., Wang, J. R., et al., (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.
11. Chen, Y. C., Yu, C. K., Wang, Y. F., Liu, C. C., Su, I. J., et al., (2004) A murine oral enterovirus 71 infection model with central nervous system involvement. J. Gen. Virol. 85, 69-77.
12. Fu, Y. C., Chi, C. S., Chiu, Y. T., Hsu, S. L., Hwang, B., et al., (2004) Cardiac complications of enterovirus rhombencephalitis. Arch. Dis. Child. 89, 368-373.
13. Wang, Y. F., Chou, C. T., Lei, H. Y., Liu, C. C., Wang, S. M., et al., (2004) A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J. Virol. 78, 7916-7924.
14. Wang, S. M., Lei, H. Y., Yu, C. K., Wang, J. R., Su, I. J., et al., (2008) Acute chemokine response in the blood and cerebrospinal fluid of children with enterovirus 71-associated brainstem encephalitis. J. Infect. Dis. 198, 1002-1006.
15. Yao, P. P., Qian, L., Xia, Y., Xu, F., Yang, Z. N., et al., (2012) Enterovirus 71-induced neurological disorders in young gerbils, Meriones unguiculatus: development and application of a neurological disease model. PLoS ONE 7, e51996.
16. Han, J., Wang, Y., Gan, X., Song, J., Sun, P., et al., (2014) Serum cytokine profiles of children with human enterovirus 71-associated hand, foot, and mouth disease. J. Med. Virol. 86, 1377-1385.
17. Yu, P., Gao, Z., Zong, Y., Bao, L., Xu, L., et al., (2014) Histopathological features and distribution of EV71 antigens and SCARB2 in human fatal cases and a mouse model of enterovirus 71 infection. Virus Res. 189, 121-132.
18. Chen, C. J., Ou, Y. C., Lin, S. Y., Raung, S. L., Liao, S. L., et al., (2010) Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J. Gen. Virol. 91, 1028-1037.
19. Koroleva, G. A., Karmysheva, V. Y., and, Lukashev, A. N., (2014) Enterovirus 71 pathogenicity in monkeys and cotton rats. Arch. Virol. 159, 1133-1138.
20. Chen, T. C., Lai, Y. K., Yu, C. K., and, Juang, J. L., (2007) Enterovirus 71 triggering of neuronal apoptosis through activation of Abl-Cdk5 signaling. Cell. Microbiol. 9, 2676-2688.
21. Tung, W. H., Hsieh, H. L., and, Yang, C. M., (2010) Enterovirus 71 induces COX-2 expression via MAPKs, NF-κB, and AP-1 in SK-N-SH cells: role of PGE2 in viral replication. Cell. Signal. 22, 234-246.
22. Tung, W. H., Lee, I. T., Hsieh, H. L., and, Yang, C. M., (2010) EV71 induces COX-2 expression via c-Src/PDGFR/PI3K/Akt/p42/p44/MAPK/Ap-1 and NF-κB in rat brain astrocytes. J. Cell. Physiol. 224, 376-386.
23. Huang, H. I., Lin, J. Y., Chen, H. H., Yeh, S. B., Kuo, R. L., et al., (2014) Enterovirus 71 infects brain-derived neural progenitor cells. Virology 468-470, 592-600.
24. Chen, H. L., Wang, L. C., Chang, C. H., Yen, C. C., Cheng, W. T. K., et al., (2008) Recombinant porcine lactoferrin expressed in the milk of transgenic mice protects neonatal mice from a lethal challenge with enterovirus type 71. Vaccine 26, 891-898.
25. Chen, C. J., Ou, Y. C., Chang, C. Y., Pan, H. C., Lin, S. Y., et al., (2011) Src signaling involvement in Japanese encephalitis virus-induced cytokine production in microglia. Neurochem. Int. 58, 924-933.
26. Majd, S., Zarifkar, A., Rastegar, K., and, Takhshid, M. A., (2008) Culturing adult rat hippocampal neurons with long-interval changing media. Iran. Biomed. J. 12, 101-107.
27. Kao, T. K., Ou, Y. C., Lin, S. Y., Pan, H. C., Song, P. J., et al., (2011) Luteolin inhibits cytokine expression in endotoxin/cytokine-stimulated microglia. J. Nutr. Biochem. 22, 612-624.
28. Chen, C. J., Ou, Y. C., Chang, C. Y., Pan, H. C., Liao, S. L., et al., (2012) Glutamate released by Japanese encephalitis virus-infected microglia involves TNF-α signaling and contributes to neuronal death. Glia 60, 487-501.
29. Wang, S. M., Lei, H. Y., and, Liu, C. C., (2012) Cytokine immunopathogenesis of enterovirus 71 brain stem encephalitis. Clin. Dev. Immunol. 2012, 876241.
30. Raung, S. L., Chen, S. Y., Liao, S. L., Chen, J. H., and, Chen, C. J., (2005) Tyrosine kinase inhibitors attenuate Japanese encephalitis virus-induced neurotoxicity. Biochem. Biophys. Res. Commun. 327, 399-406.
31. Raung, S. L., Chen, S. Y., Liao, S. L., Chen, J. H., and, Chen, C. J., (2007) Japanese encephalitis virus infection stimulates Src tyrosine kinase in neuron/glia. Neurosci. Lett. 419, 263-268.
32. Lin, Y. W., Lin, H. Y., Tsou, Y. L., Chitra, E., Hsiao, K. N., et al., (2012) Human SCARB2-mediated entry and endocytosis of EV71. PLoS ONE 7, e30507.
33. Lin, Y. W., Yu, S. L., Shao, H. Y., Lin, H. Y., Liu, C. C., et al., (2013) Human SCARB2 transgenic mice as an infectious animal model for enterovirus 71. PLoS ONE 8, e57971.
34. Yamayoshi, S., Iizuka, S., Yamashita, T., Minagawa, H., Mizuta, K., et al., (2012) Human SCARB2-dependent infection by coxsackievirus A7, A14, and A16 and enterovirus 71. J. Virol. 86, 5686-5696.
35. Hsiao, H. B., Chou, A. H., Lin, S. I., Lien, S. P., Liu, C. C., et al., (2014) Delivery of human EV71 receptors by adeno-associated virus increases EV71 infection-induced local inflammation in adult mice. BioMed. Res. Int. 2014, 878139.
36. Avdoshina, V., Biggio, F., Palchik, G., Campbell, L. A., and, Mocchetti, I., (2010) Morphine induces the release of CCL5 from astrocytes: potential neuroprotective mechanism against the HIV protein gp120. Glia 58, 1630-1639.
37. Lai, C. Y., Ou, Y. C., Chang, C. Y., Pan, H. C., Chang, C. J., et al., (2012) Endothelial Japanese encephalitis virus infection enhances migration and adhesion of leukocytes to brain microvascular endothelia via MEK-dependent expression of ICAM1 and the CINC and RANTES chemokines. J. Neurochem. 123, 250-261.
38. Liu, X., Shah, A., Gangwani, M. R., Silverstein, P. S., Fu, M., et al., (2014) HIV-1 Nef induces CCL5 production in astrocytes through p38-MAPK and PI3K/Akt pathway and utilizes NF-κB, CEBP and AP-1 transcription factors. Sci. Rep. 4, 4450.
39. Kong, L. Y., Lai, C., Wilson, B. C., Simpson, J. N., and, Hong, J. S., (1997) Protein tyrosine kinase inhibitors decrease lipopolysaccharide-induced proinflammatory cytokine production in mixed glia, microglia-enriched or astrocyte-enriched cultures. Neurochem. Int. 30, 491-497.
40. Pan, B., Yang, L., Wang, J., Wang, Y., Wang, J., et al., (2014) C-Abl tyrosine kinase mediates neurotoxic prion peptide-induced neuronal apoptosis via regulating mitochondrial homeostasis. Mol. Neurobiol. 49, 1102-1116.
41. Huber, M., Selinka, H. C., and, Kandolf, R., (1997) Tyrosine phosphorylation events during coxsackievirus B3 replication. J. Virol. 71, 595-600.
42. Yura, Y., Kusaka, J., Tsujimoto, H., Yoshioka, Y., Yoshida, H., et al., (1997) Effects of protein tyrosine kinase inhibitors on the replication of herpes simplex virus and the phosphorylation of viral proteins. Intervirology 40, 7-14.
43. Masters, J., Hinek, A. A., Uddin, S., Platanias, L. C., Zeng, W., et al., (2001) Poxvirus infection rapidly activates tyrosine kinase signal transduction. J. Biol. Chem. 276, 48371-48375.
44. Hanisch, U. K., (2002) Microglia as a source and target of cytokines. Glia 40, 140-155.
45. Zeng, J., Wang, G., Li, W., Zhang, D., Chen, X., et al., (2013) Induction of cytopathic effect and cytokines in coxsackievirus B3-infected murine astrocytes. Virol. J. 10, 157.
46. Kuronita, T., Eskelinen, E. L., Fujita, H., Saftig, P., Himeno, M., 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, 4117-4131.