Inhibition of host extracellular signal-regulated kinase (ERK) activation decreases new world alphavirus multiplication in infected cells

Virology

Volumn 468, Issue , 2014, Pages 490-503

  Voss, Kelsey ^a   Amaya, Moushimi ^a   Mueller, Claudius ^a   Roberts, Brian ^b   Kehn Hall, Kylene ^a   Bailey, Charles ^a   Petricoin, Emanuel ^a   Narayanan, Aarthi ^a  

^a GEORGE MASON UNIVERSITY   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

Ag 126; Alphavirus; ERK; Extracellular signal regulated kinase; Kinase; MAPK

Indexed keywords

AG 126; ENZYME INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG; AG 127; MITOGEN ACTIVATED PROTEIN KINASE; TYRPHOSTIN;

ANTIVIRAL ACTIVITY; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY TEST; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS TITRATION; ANIMAL; CELL LINE; DRUG EFFECTS; EASTERN EQUINE ENCEPHALOMYELITIS VIRUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; WESTERN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS;

ALPHAVIRUS;

ANIMALS; CELL LINE; CELL SURVIVAL; ENCEPHALITIS VIRUS, EASTERN EQUINE; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; ENCEPHALITIS VIRUS, WESTERN EQUINE; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, VIRAL; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TYRPHOSTINS; VIRUS REPLICATION;

EID: 84907554507     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.09.005     Document Type: Article

References (56)

1. Amaya M., Voss K., Sampey G., Senina S., de la Fuente C., Mueller C., Calvert V., Kehn-Hall K., Carpenter C., Kashanchi F., Bailey C., Mogelsvang S., Petricoin E., Narayanan A. The role of IKKβ in venezuelan equine encephalitis virus infection. PLoS One 2014, 9:e86745. 10.1371/journal.pone.0086745.
2. Atasheva S., Krendelchtchikova V., Liopo A., Frolova E., Frolov I. Interplay of acute and persistent infections caused by Venezuelan equine encephalitis virus encoding mutated capsid protein. J. Virol. 2010, 84:10004-10015. 10.1128/JVI.01151-10.
3. Barrett, Alan D.T., Stanberry, Lawrence R. (Eds.), 2009. Preface. In: Vaccines for Biodefense and Emerging and Neglected Diseases. Academic Press, London, p. xvii, ISBN: 9780123694089, http://dx.doi.org/10.1016/B978-0-12-369408-9.00079-2.
4. Boldogh I., AbuBakar S., Albrecht T. Activation of proto-oncogenes: an immediate early event in human cytomegalovirus infection. Science 1990, 247:561-564.
5. Burke C.W., Gardner C.L., Steffan J.J., Ryman K.D., Klimstra W.B. Characteristics of alpha/beta interferon induction after infection of murine fibroblasts with wild-type and mutant alphaviruses. Virology 2009, 395:121-132. 10.1016/j.virol.2009.08.039.
6. Cai Y., Liu Y., Zhang X. Suppression of coronavirus replication by inhibition of the MEK signaling pathway. J. Virol. 2007, 81:446-456. 10.1128/JVI.01705-06.
7. Canonico P.G., Kende M., Luscri B.J., Huggins J.W. In-vivo activity of antivirals against exotic RNA viral infections. J. Antimicrob. Chemother. 1984, 14:27-41. 10.1093/jac/14.suppl_A.27.
8. Carrera J.-P., Forrester N., Wang E., Vittor A.Y., Haddow A.D., López-Vergès S., Abadía I., Castaño E., Sosa N., Báez C., Estripeaut D., Díaz Y., Beltrán D., Cisneros J., Cedeño H.G., Travassos da Rosa A.P., Hernandez H., Martínez-Torres A.O., Tesh R.B., Weaver S.C. Eastern equine encephalitis in Latin America. N. Engl. J. Med. 2013, 369:732-744. 10.1056/NEJMoa1212628.
9. Carter A.B., Hunninghake G.W. A constitutive active MEK --> ERK pathway negatively regulates NF-kappa B-dependent gene expression by modulating TATA-binding protein phosphorylation. J. Biol. Chem. 2000, 275:27858-27864. 10.1074/jbc.M003599200.
10. Chatterjee P.K., Patel N.S.A., Kvale E.O., Brown P.A.J., Stewart K.N., Britti D., Cuzzocrea S., Mota-Filipe H., Thiemermann C. The tyrosine kinase inhibitor tyrphostin AG126 reduces renal ischemia/reperfusion injury in the rat. Kidney Int. 2003, 64:1605-1619. 10.1046/j.1523-1755.2003.00254.x.
11. Chuderland D., Seger R. Protein-protein interactions in the regulation of the extracellular signal-regulated kinase. Mol. Biotechnol. 2005, 29:57-74. 10.1385/MB:29:1:57.
12. Cruzalegui F.H., Cano E., Treisman R. ERK activation induces phosphorylation of Elk-1 at multiple S/T-P motifs to high stoichiometry. Oncogene 1999, 18:7948-7957. 10.1038/sj.onc.1203362.
13. Fine D.L., Jenkins E., Martin S.S., Glass P., Parker M.D., Grimm B. A multisystem approach for development and evaluation of inactivated vaccines for Venezuelan equine encephalitis virus (VEEV). J. Virol. Methods 2010, 163:424-432. 10.1016/j.jviromet.2009.11.006.
14. Furler R.L., Uittenbogaart C.H. Signaling through the P38 and ERK pathways: a common link between HIV replication and the immune response. Immunol. Res. 2010, 48:99-109. 10.1007/s12026-010-8170-1.
15. Garmashova N., Gorchakov R., Volkova E., Paessler S., Frolova E., Frolov I. The old world and new world alphaviruses use different virus-specific proteins for induction of transcriptional shutoff. J. Virol. 2007, 81:2472-2484. 10.1128/JVI.02073-06.
16. Griffin D.E., Hardwick J.M. Regulators of apoptosis on the road to persistent alphavirus infection. Annu. Rev. Microbiol. 1997, 51:565-592. 10.1146/annurev.micro.51.1.565.
17. Hans A., Syan S., Crosio C., Sassone-Corsi P., Brahic M., Gonzalez-Dunia D. Borna disease virus persistent infection activates mitogen-activated protein kinase and blocks neuronal differentiation of PC12 Cells. J. Biol. Chem. 2001, 276:7258-7265.
18. Hong S.-K., Yoon S., Moelling C., Arthan D., Park J.-I. Noncatalytic function of ERK1/2 can promote Raf/MEK/ERK-mediated growth arrest signaling. J. Biol. Chem. 2009, 284:33006-33018. 10.1074/jbc.M109.012591.
19. Hu P., Han Z., Couvillon A.D., Exton J.H. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J. Biol. Chem. 2004, 279:49420-49429. 10.1074/jbc.M407700200.
20. Jacqué J.M., Mann A., Enslen H., Sharova N., Brichacek B., Davis R.J., Stevenson M. Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase. EMBO J. 1998, 17:2607-2618. 10.1093/emboj/17.9.2607.
21. Johnson R.A., Ma X.L., Yurochko A.D., Huang E.S. The role of MKK1/2 kinase activity in human cytomegalovirus infection. J. Gen. Virol. 2001, 82:493-497.
22. Julander J.G., Skirpstunas R., Siddharthan V., Shafer K., Hoopes J.D., Smee D.F., Morrey J.D. C3H/HeN mouse model for the evaluation of antiviral agents for the treatment of Venezuelan equine encephalitis virus infection. Antiviral Res. 2008, 78:230-241. 10.1016/j.antiviral.2008.01.007.
23. Kehn-Hall K., Narayanan A., Lundberg L., Sampey G., Pinkham C., Guendel I., Van Duyne R., Senina S., Schultz K.L., Stavale E., Aman M.J., Bailey C., Kashanchi F. Modulation of GSK-3β activity in Venezuelan equine encephalitis virus infection. PLoS One 2012, 7:e34761. 10.1371/journal.pone.0034761.
24. Li G.P., La Starza M.W., Hardy W.R., Strauss J.H., Rice C.M. Phosphorylation of Sindbis virus nsP3 in vivo and in vitro. Virology 1990, 179:416-427.
25. Liu X., Cohen J.I. Inhibition of Bim enhances replication of varicella-zoster virus and delays plaque formation in virus-infected cells. J. Virol. 2014, 88:1381-1388. 10.1128/JVI.01695-13.
26. Liu X., Li Q., Dowdell K., Fischer E.R., Cohen J.I. Varicella-Zoster virus ORF12 protein triggers phosphorylation of ERK1/2 and inhibits apoptosis. J. Virol. 2012, 86:3143-3151. 10.1128/JVI.06923-11.
27. Luo H., Yanagawa B., Zhang J., Luo Z., Zhang M., Esfandiarei M., Carthy C., Wilson J.E., Yang D., McManus B.M. Coxsackievirus B3 replication is reduced by inhibition of the extracellular signal-regulated kinase (ERK) signaling pathway. J. Virol. 2002, 76:3365-3373.
28. Martin S.S., Bakken R.R., Lind C.M., Garcia P., Jenkins E., Glass P.J., Parker M.D., Hart M.K., Fine D.L. Evaluation of formalin inactivated V3526 virus with adjuvant as a next generation vaccine candidate for Venezuelan equine encephalitis virus. Vaccine 2010, 28:3143-3151. 10.1016/j.vaccine.2010.02.056.
29. Mizutani T., Fukushi S., Saijo M., Kurane I., Morikawa S. Regulation of p90RSK phosphorylation by SARS-CoV infection in Vero E6 cells. FEBS Lett. 2006, 580:1417-1424. 10.1016/j.febslet.2006.01.066.
30. Narayanan A., Kehn-Hall K., Senina S., Lundberg L., Van Duyne R., Guendel I., Das R., Baer A., Bethel L., Turell M., Hartman A.L., Das B., Bailey C., Kashanchi F. Curcumin inhibits Rift valley fever virus replication in human cells. J. Biol. Chem. 2012, 287:33198-33214. 10.1074/jbc.M112.356535.
31. Novogrodsky A., Vanichkin A., Patya M., Gazit A., Osherov N., Levitzki A. Prevention of lipopolysaccharide-induced lethal toxicity by tyrosine kinase inhibitors. Science 1994, 264:1319-1322.
32. Paessler S., Weaver S.C. Vaccines for Venezuelan equine encephalitis. Vaccine 2009, 27(Suppl. 4):SD80-SD85. 10.1016/j.vaccine.2009.07.095.
33. Parra J.L., Buxadé M., Proud C.G. Features of the catalytic domains and C termini of the MAPK signal-integrating kinases Mnk1 and Mnk2 determine their differing activities and regulatory properties. J. Biol. Chem. 2005, 280:37623-37633. 10.1074/jbc.M508356200.
34. Peltier D.C., Lazear H.M., Farmer J.R., Diamond M.S., Miller D.J. Neurotropic arboviruses induce interferon regulatory factor 3-mediated neuronal responses that are cytoprotective, interferon independent, and inhibited by Western equine encephalitis virus capsid. J. Virol. 2013, 87:1821-1833. 10.1128/JVI.02858-12.
35. Peränen J., Takkinen K., Kalkkinen N., Kääriäinen L. Semliki forest virus-specific non-structural protein nsP3 is a phosphoprotein. J. Gen. Virol. 1988, 69(9):2165-2178. (Pt).
36. Planz O., Pleschka S., Ludwig S. MEK-specific inhibitor U0126 blocks spread of Borna disease virus in cultured cells. J. Virol. 2001, 75:4871-4877. 10.1128/JVI.75.10.4871-4877.2001.
37. Pleschka S. RNA viruses and the mitogenic Raf/MEK/ERK signal transduction cascade. Biol. Chem. 2008, 389:1273-1282. 10.1515/BC.2008.145.
38. Pleschka S., Wolff T., Ehrhardt C., Hobom G., Planz O., Rapp U.R., Ludwig S. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell Biol. 2001, 3:301-305. 10.1038/35060098.
39. Popova T.G., Turell M.J., Espina V., Kehn-Hall K., Kidd J., Narayanan A., Liotta L., Petricoin E.F., Kashanchi F., Bailey C., Popov S.G. Reverse-phase phosphoproteome analysis of signaling pathways induced by Rift valley fever virus in human small airway epithelial cells. PLoS One 2010, 5:e13805. 10.1371/journal.pone.0013805.
40. Popova T.G., Turell M.J., Espina V., Kehn-Hall K., Kidd J., Narayanan A., Liotta L., Petricoin E.F., Kashanchi F., Bailey C., Popov S.G. Reverse-phase phosphoproteome analysis of signaling pathways induced by Rift valley fever virus in human small airway epithelial cells. PLoS One 2010, 5. 10.1371/journal.pone.0013805.
41. Raines M.A., Kolesnick R.N., Golde D.W. Sphingomyelinase and ceramide activate mitogen-activated protein kinase in myeloid HL-60 cells. J. Biol. Chem. 1993, 268:14572-14575.
42. Rodríguez M.E., Brunetti J.E., Wachsman M.B., Scolaro L.A., Castilla V. Raf/MEK/ERK pathway activation is required for Junin virus replication. J. Gen. Virol. 2014, 10.1099/vir.0.061242-0.
43. Roskoski R. ERK1/2 MAP kinases: structure, function, and regulation. Pharmacol. Res. Off. J. Ital. Pharmacol. Soc 2012, 66:105-143. 10.1016/j.phrs.2012.04.005.
44. Roskoski R. MEK1/2 dual-specificity protein kinases: structure and regulation. Biochem. Biophys. Res. Commun. 2012, 417:5-10. 10.1016/j.bbrc.2011.11.145.
45. Sharma A., Bhattacharya B., Puri R.K., Maheshwari R.K. Venezuelan equine encephalitis virus infection causes modulation of inflammatory and immune response genes in mouse brain. BMC Genomics 2008, 9:289. 10.1186/1471-2164-9-289.
46. Sharma A., Gupta P., Glass P.J., Parker M.D., Maheshwari R.K. Safety and protective efficacy of INA-inactivated Venezuelan equine encephalitis virus: implication in vaccine development. Vaccine 2011, 29:953-959. 10.1016/j.vaccine.2010.11.033.
47. Shaul Y.D., Seger R. The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim. Biophys. Acta 2007, 1773:1213-1226. 10.1016/j.bbamcr.2006.10.005.
48. Snyder A.J., Mukhopadhyay S. The alphavirus E3 glycoprotein functions in a clade-specific manner. J. Virol. 2012, 86:13609-13620. 10.1128/JVI.01805-12.
49. Vihinen H., Saarinen J. Phosphorylation site analysis of semliki forest virus nonstructural protein 3. J. Biol. Chem. 2000, 275:27775-27783. 10.1074/jbc.M002195200.
50. Volkova E., Frolova E., Darwin J., Forrester N.L., Weaver S.C., Frolov I. IRES-dependent replication of Venezuelan equine encephalitis virus makes it highly attenuated and incapable of replicating in mosquito cells. Virology 2008, 377:160-169. 10.1016/j.virol.2008.04.020.
51. Weaver S.C., Reisen W.K. Present and future arboviral threats. Antiviral Res. 2010, 85:328. 10.1016/j.antiviral.2009.10.008.
52. Wulfkuhle J.D., Edmiston K.H., Liotta L.A., Petricoin E.F. Technology insight: pharmacoproteomics for cancer--promises of patient-tailored medicine using protein microarrays. Nat. Clin. Pract. Oncol. 2006, 3:256-268. 10.1038/ncponc0485.
53. Xing Z., Cardona C.J., Anunciacion J., Adams S., Dao N. Roles of the ERK MAPK in the regulation of proinflammatory and apoptotic responses in chicken macrophages infected with H9N2 avian influenza virus. J. Gen. Virol. 2010, 91:343-351. 10.1099/vir.0.015578-0.
54. Yoon S., Seger R. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors Church Switz. 2006, 24:21-44. 10.1080/02699050500284218.
55. Zacks M.A., Paessler S. Encephalitic alphaviruses. Vet. Microbiol. 2010, 140:281. 10.1016/j.vetmic.2009.08.023.
56. Zhang Y., Cho Y.-Y., Petersen B.L., Zhu F., Dong Z. Evidence of STAT1 phosphorylation modulated by MAPKs, MEK1 and MSK1. Carcinogenesis 2004, 25:1165-1175. 10.1093/carcin/bgh115.