Inhibition of viral protein translation by indomethacin in vesicular stomatitis virus infection: Role of eIF2α kinase PKR

Cellular Microbiology

Volumn 17, Issue 9, 2015, Pages 1391-1404

  Amici, Carla ^a   La Frazia, Simone ^a   Brunelli, Claudia ^a   Balsamo, Mirna ^a,c   Angelini, Mara ^a   Santoro, M Gabriella ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; ENDOPLASMIC RETICULUM RESIDENT PROTEIN KINASE; INDOMETACIN; INITIATION FACTOR 2ALPHA; INTERFERON; PROTEIN KINASE; PROTEIN KINASE R; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; ANTIVIRUS AGENT; ENZYME ACTIVATOR; INITIATION FACTOR 2;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BHK CELL LINE; CELL PROTECTION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; FEMALE; GENE SILENCING; GENETIC TRANSFECTION; HAPLORHINI; HEK293 CELL LINE; HELA CELL LINE; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RHABDOVIRIDAE; RNA INTERFERENCE; RNA TRANSLATION; TRANSCRIPTION INITIATION; TRANSLATION REGULATION; VESICULAR STOMATITIS; VESICULOVIRUS; VIRUS ATTACHMENT; VIRUS REPLICATION; VIRUS TITRATION; BIOSYNTHESIS; CELL LINE; DRUG EFFECTS; IC50; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS;

EUKARYOTA; RHABDOVIRIDAE; VESICULAR STOMATITIS VIRUS;

ANTIVIRAL AGENTS; CELL LINE; EIF-2 KINASE; ENZYME ACTIVATORS; EUKARYOTIC INITIATION FACTOR-2; HUMANS; INDOMETHACIN; INHIBITORY CONCENTRATION 50; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; VESICULOVIRUS; VIRAL PROTEINS;

EID: 84940437927     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12446     Document Type: Article

References (44)

1. Amici, C., Rossi, A., and Santoro, M.G. (1995) Aspirin enhances thermotolerance in human erythroleukemic cells: an effect associated with the modulation of the heat shock response. Cancer Res 55: 452-457.
2. Amici, C., Di Caro, A., Ciucci, A., Chiappa, L., Castelletti, C., Martella, V., etal. (2006) Indomethacin has a potent antiviral activity against SARS coronavirus. Antivir Ther 11: 1021-1030.
3. Bahrami, H., Daryani, N.E., Haghpanah, B., Moayyeri, A., Moghadam, K.F., Mirmomen, S., and Kamangar, F. (2005) Effects of indomethacin on viral replication markers in asymptomatic carriers of hepatitis B: a randomized, placebo-controlled trial. Am J Gastroenterol 100: 856-861.
4. Baltzis, D., Qu, L.K., Papadopoulou, S., Blais, J.D., Bell, J.C., Sonenberg, N., and Koromilas, A.E. (2004) Resistance to vesicular stomatitis virus infection requires a functional cross talk between the eukaryotic translation initiation factor 2alpha kinases PERK and PKR. J Virol 78: 12747-12761.
5. Benet, L.Z. (1996) Design and optimization of dosage regiments; pharmacokinetic data. In Goodman & Gilman's: The Pharmacological Basis of Therapeutics. Hardman, J.G., Limbird, L.E., Molinoff, P.B., Ruddon, R.W., and Gilman, A.G. (eds). New York: McGraw-Hill, pp. 1707-1793.
6. Berlanga, J.J., Ventoso, I., Harding, H.P., Deng, J., Ron, D., Sonenberg, N., etal. (2006) Antiviral effect of the mammalian translation initiation factor 2α kinase GCN2 against RNA viruses. EMBO J 5: 1730-1740.
7. Bourinbaiar, A.S., and Lee-Huang, S. (1995) The non-steroidal anti-inflammatory drug, indomethacin, as an inhibitor of HIV replication. FEBS Lett 360: 85-88.
8. Brunelli, C., Amici, C., Angelini, M., Fracassi, C., Belardo, G., and Santoro, M.G. (2012) The non-steroidal anti-inflammatory drug indomethacin activates the eIF2α kinase PKR, causing a translational block in human colorectal cancer cells. Biochem J 443: 379-386.
9. Caselli, E., Fiorentini, S., Amici, C., Di Luca, D., Caruso, A., and Santoro, M.G. (2007) Human herpesvirus 8 acute infection of endothelial cells induces monocyte chemoattractant protein 1-dependent capillary-like structure formation: role of the IKK/NF-κB pathway. Blood 109: 2718-2726.
10. Chen, N., Warner, J.L., and Reiss, C.S. (2000) NSAID treatment suppresses VSV propagation in mouse CNS. Virology 276: 44-51.
11. Chen, N., Restivo, A., and Reiss, C.S. (2002) Selective inhibition of COX-2 is beneficial to mice infected intranasally with VSV. Prostaglandins Other Lipid Mediat 67: 143-155.
12. Clemens, M.J. (2004) Targets and mechanisms for the regulation of translation in malignant transformation. Oncogene 23: 3180-3188.
13. Connor, J.H., and Lyles, D.S. (2002) Vesicular stomatitis virus infection alters the eIF4F translation initiation complex and causes dephosphorylation of the eIF4E binding protein 4E-BP1. J Virol 70: 10177-10187.
14. Connor, J.H., and Lyles, D.S. (2005) Inhibition of host translation during vesicular stomatitis virus infection. J Biol Chem 280: 13512-13519.
15. Cotto, J.J., Kline, M., and Morimoto, R.I. (1996) Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J Biol Chem 271: 3355-3358.
16. Dabo, S., and Meurs, E.F. (2012) dsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses 4: 2598-2635.
17. Donzé, O., Deng, J., Curran, J., Sladek, R., Picard, D., and Sonenberg, N. (2004) The protein kinase PKR: a molecular clock that sequentially activates survival and death programs. EMBO J 23: 564-571.
18. Durbin, R.K., Mertz, S.E., Koromilas, A.E., and Durbin, J.E. (2002) PKR protection against intranasal vesicular stomatitis virus infection is mouse strain dependent. Viral Immunol 15: 41-51.
19. Gallione, C.J., Greene, J.R., Iverson, L.E., and Rose, J.K. (1981) Nucleotide sequences of the mRNA's encoding the vesicular stomatitis virus N and NS proteins. J Virol 39: 529-535.
20. García, M.A., Gil, J., Ventoso, I., Guerra, S., Domingo, E., Rivas, C., and Esteban, M. (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70: 1032-1060.
21. Gebauer, F., and Hentze, M.W. (2004) Molecular mechanisms of translational control. Nature Rev Mol Cell Biol 5: 827-835.
22. Gil, J., Alcamí, J., and Esteban, M. (2000) Activation of NF-κB by the dsRNA-dependent protein kinase, PKR involves the IκB kinase complex. Oncogene 19: 1369-1378.
23. Holcik, M., and Sonenberg, N. (2005) Translational control in stress and apoptosis. Nature Rev Mol Cell Biol 6: 6318-6327.
24. Inglot, A.D. (1969) Comparison of the antiviral activity in vitro of some non-steroidal anti-inflammatory drugs. J Gen Virol 4: 203-214.
25. Krishnamoorthy, J., Mounir, Z., Raven, J.F., and Koromilas, A.E. (2008) The eIF2α kinases inhibit vesicular stomatitis virus replication independently of eIF2α phosphorylation. Cell Cycle 7: 2346-2351.
26. Lyles, D.S., Kuzmin, I.V., and Rupprecht, C.E. (2013) Rhabdoviridae. In Field's Virology. Knipe, D.M., and Howley, P. (eds). New York: Raven Press, pp. 885-922.
27. Morimoto, R.I., and Santoro, M.G. (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nature Biotechnol 16: 833-838.
28. Mukherjee, P.K., and Simpson, R.W. (1987) Transcriptionally defective nucleocapsids of vesicular stomatitis virus from cells treated with indomethacin. Virology 156: 25-31.
29. Neznanov, N., Dragunsky, E.M., Chumakov, K.M., Neznanova, L., Wek, R.C., Gudkov, A.V., and Banerjee, A.K. (2008) Different effect of proteasome inhibition on vesicular stomatitis virus and poliovirus replication. PLoS ONE 3: e1887.
30. Ramirez, J., Alcami, J., Arnaiz-Villena, A., Regueiro, J.R., Rioperez, E., Yague, J., and Fernandez, F. (1986) Indomethacin in the relief of AIDS symptoms. Lancet 2: 570.
31. Rossen, J.W., Bouma, J., Raatgeep, R.H., Büller, H.A., and Einerhand, A.W. (2004) Inhibition of cyclooxygenase activity reduces rotavirus infection at a postbinding step. J Virol 78: 9721-9730.
32. Rossi, A., Elia, G., and Santoro, M.G. (1996) 2-Cyclopenten-1-one, a new inducer of heat shock protein 70 with antiviral activity. J Biol Chem 271: 32192-32196.
33. Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M., and Santoro, M.G. (2000) Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature 403: 103-118.
34. Rossi, A., Ciafrè, S., Balsamo, M., Pierimarchi, P., and Santoro, M.G. (2006) Targeting the heat shock factor 1 by RNA interference: a potent tool to enhance hyperthermochemotherapy efficacy in cervical cancer. Cancer Res 66: 7678-7685.
35. Santoro, M.G. (1997) Antiviral activity of cyclopentenone prostanoids. Trends Microbiol 5: 276-281.
36. Santoro, M.G., Rossi, A., and Amici, C. (2003) NF-kappaB and virus infection: who controls whom. EMBO J 22: 2552-2560.
37. Scheuner, D., Patel, R., Wang, F., Lee, K., Kumar, K., Wu, J., etal. (2006) Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor-2 mediates apoptosis. J Biol Chem 281: 21458-21468.
38. Schneider, R.J., and Mohr, I. (2003) Translation initiation and viral tricks. Trends Biochem Sci 28: 130-136.
39. Schröer, J., and Shenk, T. (2008) Inhibition of cyclooxygenase activity blocks cell-to-cell spread of human cytomegalovirus. Proc Natl Acad Sci USA 105: 19468-19473.
40. Stojdl, D.F., Abraham, N., Knowles, S., Marius, R., Brasey, A., Lichty, B.D., etal. (2000) The murine double-stranded RNA-dependent protein kinase PKR is required for resistance to vesicular stomatitis virus. J Virol 74: 9580-9585.
41. Symensma, T.L., Martinez-Guzman, D., Jia, Q., Bortz, E., Wu, T.T., Rudra-Ganguly, N., etal. (2003) COX-2 induction during murine gammaherpesvirus 68 infection leads to enhancement of viral gene expression. J Virol 77: 12753-12763.
42. Taylor, S.S., Haste, N.M., and Ghosh, G. (2005) PKR and eIF2alpha: integration of kinase dimerization, activation, and substrate docking. Cell 122: 823-825.
43. Vane, J.R., and Botting, R.M. (1997) Mechanism of action of anti-inflammatory drugs. Adv Exp Med Biol 433: 131-138.
44. Zhu, H., Cong, J.P., Yu, D., Bresnahan, W.A., and Shenk, T.E. (2002) Inhibition of cyclooxygenase 2 blocks human cytomegalovirus replication. Proc Natl Acad Sci USA 99: 3932-3937.