Pyrrolidine dithiocarbamate inhibits enterovirus 71 replication by down-regulating ubiquitin-proteasome system

Virus Research

Volumn 195, Issue , 2015, Pages 207-216

  Lin, Lexun ^a   Qin, Ying ^a   Wu, Heng ^a   Chen, Yang ^a   Wu, Shuo ^a   Si, Xiaoning ^a   Wang, Hui ^a   Wang, Tianying ^a   Zhong, Xiaoyan ^a   Zhai, Xia ^a   Tong, Lei ^a   Pan, Bo ^a   Zhang, Fengmin ^a   Zhong, Zhaohua ^a   Wang, Yan ^a   Zhao, Wenran ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Antioxidant; Apoptosis; Enterovirus 71; Pyrrolidine dithiocarbamate; Ubiquitin proteasome system

Indexed keywords

ACETYLCYSTEINE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; PROTEASOME; PROTEIN; PYRROLIDINE DITHIOCARBAMATE; REGULATOR PROTEIN; REGULATORY PROTEINS P21; REGULATORY PROTEINS P53; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; ANTIVIRUS AGENT; PYRROLIDINE DERIVATIVE; PYRROLIDINE DITHIOCARBAMIC ACID; THIOCARBAMIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DOWN REGULATION; ENTEROVIRUS 71; NONHUMAN; PROGENY; PROTEIN SYNTHESIS; SYNTHESIS; UBIQUITINATION; VERO CELL LINE; VIRUS EXPRESSION; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; CHLOROCEBUS AETHIOPS; DRUG EFFECTS; ENTEROVIRUS A; METABOLISM; PHYSIOLOGY;

HUMAN ENTEROVIRUS 71; HUMAN ENTEROVIRUS B;

ANIMALS; ANTIVIRAL AGENTS; CERCOPITHECUS AETHIOPS; CYTOPATHOGENIC EFFECT, VIRAL; ENTEROVIRUS A, HUMAN; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRROLIDINES; RNA, VIRAL; THIOCARBAMATES; UBIQUITIN; UBIQUITINATION; VERO CELLS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84919371945     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.10.012     Document Type: Article

References (74)

1. Arzberger S., Hosel M., Protzer U. Apoptosis of hepatitis B virus-infected hepatocytes prevents release of infectious virus. J. Virol. 2010, 84:11994-12001.
2. Badran S.A., Midgley S., Andersen P., Bottiger B. Clinical and virological features of enterovirus 71 infections in Denmark, 2005 to 2008. Scand. J. Infect. Dis. 2011, 43:642-648.
3. Chang L.Y., Huang L.M., Gau S.S., Wu Y.Y., Hsia S.H., Fan T.Y., Lin K.L., Huang Y.C., Lu C.Y., Lin T.Y. Neurodevelopment and cognition in children after enterovirus 71 infection. N. Engl. J. Med. 2007, 356:1226-1234.
4. Chang S.C., Lin J.Y., Lo L.Y., Li M.L., Shih S.R. Diverse apoptotic pathways in enterovirus 71-infected cells. J. Neurovirol. 2004, 10:338-349.
5. Chen D., Dou Q.P. The ubiquitin-proteasome system as a prospective molecular target for cancer treatment and prevention. Curr. Protein Pept. Sci. 2010, 11:459-470.
6. Chen L.C., Shyu H.W., Chen S.H., Lei H.Y., Yu C.K., Yeh T.M. Enterovirus 71 infection induces Fas ligand expression and apoptosis of Jurkat cells. J. Med. Virol. 2006, 78:780-786.
7. Chen S.P., Huang Y.C., Li W.C., Chiu C.H., Huang C.G., Tsao K.C., Lin T.Y. Comparison of clinical features between coxsackievirus A2 and enterovirus 71 during the enterovirus outbreak in Taiwan, 2008: a children's hospital experience. J. Microbiol. Immunol. Infect. 2010, 43:99-104.
8. Chen T.C., Chang H.Y., Lin P.F., Chern J.H., Hsu J.T., Chang C.Y., Shih S.R. Novel antiviral agent DTriP-22 targets RNA-dependent RNA polymerase of enterovirus 71. Antimicrob. Agents Chemother. 2009, 53:2740-2747.
9. Chen T.C., Lai Y.K., Yu C.K., Juang J.L. Enterovirus 71 triggering of neuronal apoptosis through activation of Abl-Cdk5 signalling. Cell. Microbial. 2007, 9:2676-2688.
10. Chen T.C., Liu S.C., Huang P.N., Chang H.Y., Chern J.H., Shih S.R. Antiviral activity of pyridyl imidazolidinones against enterovirus 71 variants. J. Biomed. Sci. 2008, 15:291-300.
11. Cheng Q., Chen L., Li Z., Lane W.S., Chen J. ATM activates p53 by regulating MDM2 oligomerization and E3 processivity. EMBO J. 2009, 28:3857-3867.
12. Chiang L.C., Ng L.T., Cheng P.W., Chiang W., Lin C.C. Antiviral activities of extracts and selected pure constituents of Ocimum basilicum. Clin. Exp. Pharmacol. Physiol. 2005, 32:811-816.
13. Choudhury S., Kolukula V.K., Preet A., Albanese C., Avantaggiati M.L. Dissecting the pathways that destabilize mutant p53: the proteasome or autophagy?. Cell Cycle 2013, 12:1022-1029.
14. Falah N., Montserret R., Lelogeais V., Schuffenecker I., Lina B., Cortay J.C., Violot S. Blocking human enterovirus 71 replication by targeting viral 2A protease. J. Antimicrob. Chemother. 2012, 67:2865-2869.
15. Fraternale A., Paoletti M.F., Casabianca A., Orlandi C., Schiavano G.F., Chiarantini L., Clayette P., Oiry J., Vogel J.U., Cinatl J., Magnani M. Inhibition of murine AIDS by pro-glutathione (GSH) molecules. Antiviral Res. 2008, 77:120-127.
16. Hayakawa M., Miyashita H., Sakamoto I., Kitagawa M., Tanaka H., Yasuda H., Karin M., Kikugawa K. Evidence that reactive oxygen species do not mediate NF-kappaB activation. EMBO J. 2003, 22:3356-3366.
17. Herold S., Ludwig S., Pleschka S., Wolff T. Apoptosis signaling in influenza virus propagation, innate host defense, and lung injury. J. Leukocyte Biol. 2012, 92:75-82.
18. Hung H.C., Chen T.C., Fang M.Y., Yen K.J., Shih S.R., Hsu J.T., Tseng C.P. Inhibition of enterovirus 71 replication and the viral 3D polymerase by aurintricarboxylic acid. J. Antimicrob. Chemother. 2010, 65:676-683.
19. Ji X.Y., Wang H.Q., Hao L.H., He W.Y., Gao R.M., Li Y.P., Li Y.H., Jiang J.D., Li Z.R. Synthesis and antiviral activity of N-phenylbenzamide derivatives, a novel class of enterovirus 71 inhibitors. Molecules 2013, 18:3630-3640.
20. Kanlaya R., Pattanakitsakul S.N., Sinchaikul S., Chen S.T., Thongboonkerd V. The ubiquitin-proteasome pathway is important for dengue virus infection in primary human endothelial cells. J. Proteome Res. 2010, 9:4960-4971.
21. Karpe Y.A., Meng X.J. Hepatitis E virus replication requires an active ubiquitin-proteasome system. J. Virol. 2012, 86:5948-5952.
22. Kash J.C., Xiao Y., Davis A.S., Walters K.A., Chertow D.S., Easterbrook J.D., Dunfee R.L., Sandouk A., Jagger B.W., Schwartzman L.M., Kuestner R.E., Wehr N.B., Huffman K., Rosenthal R.A., Ozinsky A., Levine R.L., Doctrow S.R., Taubenberger J.K. Treatment with the reactive oxygen species scavenger EUK-207 reduces lung damage and increases survival during 1918 influenza virus infection in mice. Free Radical Biol. Med. 2014, 67:235-247.
23. Krenn B.M., Holzer B., Gaudernak E., Triendl A., van Kuppeveld F.J., Seipelt J. Inhibition of polyprotein processing and RNA replication of human rhinovirus by pyrrolidine dithiocarbamate involves metal ions. J. Virol. 2005, 79:13892-13899.
24. Kuo R.L., Shih S.R. Strategies to develop antivirals against enterovirus 71. Virol. J. 2013, 10:28.
25. Lanke K., Krenn B.M., Melchers W.J., Seipelt J., van Kuppeveld F.J. PDTC inhibits picornavirus polyprotein processing and RNA replication by transporting zinc ions into cells. J. Gen. Virol. 2007, 88:1206-1217.
26. Lee J.C., Shih S.R., Chang T.Y., Tseng H.Y., Shih Y.F., Yen K.J., Chen W.C., Shie J.J., Fang J.M., Liang P.H., Chao Y.S., Hsu J.T. A mammalian cell-based reverse two-hybrid system for functional analysis of 3C viral protease of human enterovirus 71. Anal. Biochem. 2008, 375:115-123.
27. Liang C.C., Sun M.J., Lei H.Y., Chen S.H., Yu C.K., Liu C.C., Wang J.R., Yeh T.M. Human endothelial cell activation and apoptosis induced by enterovirus 71 infection. J. Med. Virol. 2004, 74:597-603.
28. Lin T.Y., Liu Y.C., Jheng J.R., Tsai H.P., Jan J.T., Wong W.R., Horng J.T. Anti-enterovirus 71 activity screening of chinese herbs with anti-infection and inflammation activities. Am. J. Chin. Med. 2009, 37:143-158.
29. Ling J.X., Wei F., Li N., Li J.L., Chen L.J., Liu Y.Y., Luo F., Xiong H.R., Hou W., Yang Z.Q. Amelioration of influenza virus-induced reactive oxygen species formation by epigallocatechin gallate derived from green tea. Acta Pharmacol. Sin. 2012, 33:1533-1541.
30. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
31. Lu J.R., Lu W.W., Lai J.Z., Tsai F.L., Wu S.H., Lin C.W., Kung S.H. Calcium flux and calpain-mediated activation of the apoptosis-inducing factor contribute to enterovirus 71-induced apoptosis. J. Gen. Virol. 2013, 94:1477-1485.
32. Luo H., Zhang J., Dastvan F., Yanagawa B., Reidy M.A., Zhang H.M., Yang D., Wilson J.E., McManus B.M. Ubiquitin-dependent proteolysis of cyclin D1 is associated with coxsackievirus-induced cell growth arrest. J. Virol. 2003, 77:1-9.
33. Morais C., Gobe G., Johnson D.W., Healy H. Inhibition of nuclear factor kappa B transcription activity drives a synergistic effect of pyrrolidine dithiocarbamate and cisplatin for treatment of renal cell carcinoma. Apoptosis 2010, 15:412-425. (An International Journal on Programmed Cell Death).
34. Narayanan A., Amaya M., Voss K., Chung M., Benedict A., Sampey G., Kehn-Hall K., Luchini A., Liotta L., Bailey C., Kumar A., Bavari S., Hakami R.M., Kashanchi F. Reactive oxygen species activate NFkappaB (p65) and p53 and induce apoptosis in RVFV infected liver cells. Virology 2014, 449:270-286.
35. Navon A., Ciechanover A. The 26 S proteasome: from basic mechanisms to drug targeting. J. Biol. Chem. 2009, 284:33713-33718.
36. Ooi M.H., Wong S.C., Lewthwaite P., Cardosa M.J., Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol. 2010, 9:1097-1105.
37. Qiu M., Chen Y., Cheng L., Chu Y., Song H.Y., Wu Z.W. Pyrrolidine dithiocarbamate inhibits herpes simplex virus 1 and 2 replication, and its activity may be mediated through dysregulation of the ubiquitin-proteasome system. J. Virol. 2013, 87:8675-8686.
38. Rastogi N., Mishra D.P. Therapeutic targeting of cancer cell cycle using proteasome inhibitors. Cell Div. 2012, 7:26.
39. Savarino A., Mai A., Norelli S., El Daker S., Valente S., Rotili D., Altucci L., Palamara A.T., Garaci E. Shock and kill effects of class I-selective histone deacetylase inhibitors in combination with the glutathione synthesis inhibitor buthionine sulfoximine in cell line models for HIV-1 quiescence. Retrovirology 2009, 6:52.
40. Shang L., Xu M., Yin Z. Antiviral drug discovery for the treatment of enterovirus 71 infections. Antiviral Res. 2013, 97:183-194.
41. Shen M., Schmitt S., Buac D., Dou Q.P. Targeting the ubiquitin-proteasome system for cancer therapy. Expert Opin. Ther. Targets 2013, 17:1091-1108.
42. Shi W., Hou X., Li X., Peng H., Shi M., Jiang Q., Liu X., Ji Y., Yao Y., He C., Lei X. Differential gene expressions of the MAPK signaling pathway in enterovirus 71-infected rhabdomyosarcoma cells. Braz. J. Infect. Dis. 2013, 17:410-417. (An Official Publication of the Brazilian Society of Infectious Diseases).
43. Shi W., Li X., Hou X., Peng H., Jiang Q., Shi M., Ji Y., Liu X., Liu J. Differential apoptosis gene expressions of rhabdomyosarcoma cells in response to enterovirus 71 infection. BMC Infect. Dis. 2012, 12:327.
44. Shia K.S., Li W.T., Chang C.M., Hsu M.C., Chern J.H., Leong M.K., Tseng S.N., Lee C.C., Lee Y.C., Chen S.J., Peng K.C., Tseng H.Y., Chang Y.L., Tai C.L., Shih S.R. Design, synthesis, and structure-activity relationship of pyridyl imidazolidinones: a novel class of potent and selective human enterovirus 71 inhibitors. J. Med. Chem. 2002, 45:1644-1655.
45. Shih S.R., Tsai M.C., Tseng S.N., Won K.F., Shia K.S., Li W.T., Chern J.H., Chen G.W., Lee C.C., Lee Y.C., Peng K.C., Chao Y.S. Mutation in enterovirus 71 capsid protein VP1 confers resistance to the inhibitory effects of pyridyl imidazolidinone. Antimicrob. Agents Chemother. 2004, 48:3523-3529.
46. Shih S.R., Weng K.F., Stollar V., Li M.L. Viral protein synthesis is required for Enterovirus 71 to induce apoptosis in human glioblastoma cells. J. Neurovirol. 2008, 14:53-61.
47. Si X., McManus B.M., Zhang J., Yuan J., Cheung C., Esfandiarei M., Suarez A., Morgan A., Luo H. Pyrrolidine dithiocarbamate reduces coxsackievirus B3 replication through inhibition of the ubiquitin-proteasome pathway. J. Virol. 2005, 79:8014-8023.
48. Si X., Wang Y., Wong J., Zhang J., McManus B.M., Luo H. Dysregulation of the ubiquitin-proteasome system by curcumin suppresses coxsackievirus B3 replication. J. Virol. 2007, 81:3142-3150.
49. Song J., Yeo S.G., Hong E.H., Lee B.R., Kim J.W., Kim J., Jeong H., Kwon Y., Kim H., Lee S., Park J.H., Ko H.J. Antiviral Activity of Hederasaponin B from Hedera helix against Enterovirus 71 Subgenotypes C3 and C4a. Biomolecules Ther. 2014, 22:41-46.
50. Spada C., Treitinger A., Reis M., Masokawa I.Y., Verdi J.C., Luiz M.C., Silveira M.V., Oliveira O.V., Michelon C.M., Avila-Junior S., Gil l D., Ostrowsky S. An evaluation of antiretroviral therapy associated with alpha-tocopherol supplementation in HIV-infected patients. Clin. Chem. Lab. Med.: CCLM/FESCC 2002, 40:456-459.
51. Thoa le P.K., Chiang P.S., Khanh T.H., Luo S.T., Dan T.N., Wang Y.F., Thuong T.C., Chung W.Y., Hung N.T., Wang J.R., Nhan le N.T., Thinh le Q., Su I.J., Dung T.D., Lee M.S. Genetic and antigenic characterization of enterovirus 71 in Ho Chi Minh city, Vietnam, 2011. PLoS One 2013, 8:e69895.
52. Thompson J.S., Asmis R., Tapp A.A., Nelson B., Chu Y., Glass J., Moneyhon M., Brown S.A. Pyrrolidine dithiocarbamate (PDTC) blocks apoptosis and promotes ionizing radiation-induced necrosis of freshly-isolated normal mouse spleen cells. Apoptosis 2010, 15:705-714. (an international journal on programmed cell death).
53. Tsai M.T., Cheng Y.H., Liu Y.N., Liao N.C., Lu W.W., Kung S.H. Real-time monitoring of human enterovirus (HEV)-infected cells and anti-HEV 3C protease potency by fluorescence resonance energy transfer. Antimicrob. Agents Chemother. 2009, 53:748-755.
54. Tu Y., Chen C., Pan J., Xu J., Zhou Z.G., Wang C.Y. The ubiquitin proteasome pathway (UPP) in the regulation of cell cycle control and DNA damage repair and its implication in tumorigenesis. Int. J. Clin. Exp. Pathol. 2012, 5:726-738.
55. Uchide N., Ohyama K. Antiviral function of pyrrolidine dithiocarbamate against influenza virus: the inhibition of viral gene replication and transcription. J. Antimicrob. Chemother. 2003, 52:8-10.
56. Uchide N., Ohyama K., Bessho T., Yuan B., Yamakawa T. Effect of antioxidants on apoptosis induced by influenza virus infection: inhibition of viral gene replication and transcription with pyrrolidine dithiocarbamate. Antiviral Res. 2002, 56:207-217.
57. Vlahos R., Stambas J., Selemidis S. Suppressing production of reactive oxygen species (ROS) for influenza A virus therapy. Trends Pharmacol. Sci. 2012, 33:3-8.
58. Wang J., Wu Z., Jin Q. COPI is required for enterovirus 71 replication. PLoS One 2012, 7:e38035.
59. Wang T., Weinman S.A. Interactions Between Hepatitis C Virus and Mitochondria: Impact on Pathogenesis and Innate Immunity. Curr. Pathobiol. Rep. 2013, 1:179-187.
60. White E. Mechanisms of apoptosis regulation by viral oncogenes in infection and tumorigenesis. Cell Death Differ. 2006, 13:1371-1377.
61. Wiesener N., Zimmer C., Jarasch-Althof N., Wutzler P., Henke A. Therapy of experimental influenza virus infection with pyrrolidine dithiocarbamate. Med. Microbial. Immunol. 2011, 200:115-126.
62. Williams V.M., Filippova M., Filippov V., Payne K.J., Duerksen-Hughes P. HPV16 E6* induces oxidative stress and DNA damage. J. Virol. 2014, 88:6751-6761.
63. Xu H., Zhang Z., Li M., Zhang R. MDM2 promotes proteasomal degradation of p21Waf1 via a conformation change. J. Biol. Chem. 2010, 285:18407-18414.
64. Yan Y., Guo J., Zhou J.Z., Tang G.P., Wang D.M. [Analysis on molecular epidemiological features of enterovirus type 71 in Guizhou Province, 2008-2011]. Bing du xue bao 2013, 29:176-179.
65. Yucel M., Kucuk A., Bayraktar A.C., Tosun M., Yalcinkaya S., Hatipoglu N.K., Erkasap N., Kavutcu M. Protective effects of the nuclear factor kappa B inhibitor pyrrolidine dithiocarbamate in bladder ischemia-reperfusion injury in rats. Mol. Biol. Rep. 2013, 40:5733-5740.
66. Zhang G., Zhou F., Gu B., Ding C., Feng D., Xie F., Wang J., Zhang C., Cao Q., Deng Y., Hu W., Yao K. In vitro and in vivo evaluation of ribavirin and pleconaril antiviral activity against enterovirus 71 infection. Arch. Virol. 2012, 157:669-679.
67. Zhang H., Tao L., Fu W.W., Liang S., Yang Y.F., Yuan Q.H., Yang D.J., Lu A.P., Xu H.X. Prenylated benzoylphloroglucinols and xanthones from the leaves of Garcinia oblongifolia with antienteroviral activity. J. Nat. Prod. 2014.
68. Zhang Y.C., Jiang S.W., Gu W.Z., Hu A.R., Lu C.T., Liang X.Y., Hu Y.R., Zhu D.D., Xie L. Clinicopathologic features and molecular analysis of enterovirus 71 infection: report of an autopsy case from the epidemic of hand, foot and mouth disease in China. Pathol. Int. 2012, 62:565-570.
69. Zheng X., Lv J., Shen Q., Chen Y., Zhou Q., Zhang W., Zhu X. Synergistic Effect of Pyrrolidine Dithiocarbamate and Cisplatin in Human Cervical Carcinoma. Reprod. Sci. 2014, 21:1319-1325.
70. Zhong Z., Li X., Zhao W., Tong L., Liu J., Wu S., Lin L., Zhang Z., Tian Y., Zhang F. Mutations at nucleotides 573 and 579 within 5'-untranslated region augment the virulence of coxsackievirus B1. Virus Res. 2008, 135:255-259.
71. Zhou X., Fan G., Xia W., He F., Hu M., Ni X., Zhang Y., Chen H. Molecular epidemiology of human enterovirus 71 strains in the Nanchang region of China in 2011. Jpn. J. Infect. Dis. 2013, 66:149-150.
72. Zhu D.M., Shi J., Liu S., Liu Y., Zheng D. HIV infection enhances TRAIL-induced cell death in macrophage by down-regulating decoy receptor expression and generation of reactive oxygen species. PLoS One 2011, 6:e18291.
73. Zhu H., Dong H., Eksioglu E., Hemming A., Cao M., Crawford J.M., Nelson D.R., Liu C. Hepatitis C virus triggers apoptosis of a newly developed hepatoma cell line through antiviral defense system. Gastroenterology 2007, 133:1649-1659.
74. Zhu J., Luo Z., Wang J., Xu Z., Chen H., Fan D., Gao N., Ping G., Zhou Z., Zhang Y., An J. Phylogenetic analysis of Enterovirus 71 circulating in Beijing, China from 2007 to 2009. PLoS One 2013, 8:e56318.