Antiviral potential of ERK/MAPK and PI3K/AKT/mTOR signaling modulation for Middle East respiratory syndrome coronavirus infection as identified by temporal kinome analysis

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 2, 2015, Pages 1088-1099

  Kindrachuk, Jason ^a   Ork, Britini ^a   Hart, Brit J ^a   Mazur, Steven ^a   Holbrook, Michael R ^a   Frieman, Matthew B ^b   Traynor, Dawn ^a   Johnson, Reed F ^a   Dyall, Julie ^a   Kuhn, Jens H ^a   Olinger, Gene G ^a   Hensley, A Lisa E ^a   Jahrlinga, Peter B ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 3 (3,5 DIBROMO 4 HYDROXYBENZYLIDENE) 1,3 DIHYDRO 5 IODO 2 INDOLONE; 3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; DABRAFENIB; EVEROLIMUS; MAMMALIAN TARGET OF RAPAMYCIN; MIDOSTAURIN; MILTEFOSINE; MITOGEN ACTIVATED PROTEIN KINASE; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; N(G) NITROARGININE METHYL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; SELUMETINIB; SORAFENIB; TRAMETINIB; UO 126; WORTMANNIN; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

ANTIVIRAL ACTIVITY; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; CORONAVIRUS INFECTION; DRUG POTENCY; DRUG TARGETING; HUMAN; HUMAN CELL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS INFECTION; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE CULTURE; BIOLOGY; CELL LINE; ENZYME LINKED IMMUNOSORBENT ASSAY; LIVER CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; VIROLOGY; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; COMPUTATIONAL BIOLOGY; CORONAVIRUS INFECTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEPATOCYTES; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84921899175     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.03659-14     Document Type: Article

References (48)

1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814-1820. http://dx.doi.org/10.1056 /NEJMoa1211721.
2. Raj VS, Osterhaus AD, Fouchier RA, Haagmans BL. 2014. MERS: emergence of a novel human coronavirus. Curr Opin Virol 5:58-62. http: //dx.doi.org/10.1016/j.coviro.2014.01.010.
3. Bialek SR, Allen D, Alvarado-Ramy F, Arthur R, Balajee A, Bell D, Best S, Blackmore C, Breakwell L, Cannons A, Brown C, Cetron M, Chea N, Chommanard C, Cohen N, Conover C, Crespo A, Creviston J, Curns AT, Dahl R, Dearth S, DeMaria A, Echols F, Erdman DD, Feikin D, Frias M, Gerber SI, Gulati R, Hale C, Haynes LM, Heberlein-Larson L, Holton K, Ijaz K, Kapoor M, Kohl K, Kuhar DT, Kumar AM, Kundich M, Lippold S, Liu L, Lovchik JC, Madoff L, Martell S, Matthews S, Moore J, Murray LR, Onofrey S, Pallansch MA, Pesik N, Pham H, et al. 2014. First confirmed cases of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in the United States, updated information on the epidemiology of MERS-CoV infection, and guidance for the public, clinicians, and public health authorities-May 2014.MMWRMorb Mortal Wkly Rep 63:431-436.
4. Peiris JS, Yuen KY, Osterhaus AD, Stohr K. 2003. The severe acute respiratory syndrome. N Engl J Med 349:2431-2441. http://dx.doi.org/10 .1056/NEJMra032498.
5. Pyrc K, Sims AC, Dijkman R, Jebbink M, Long C, Deming D, Donaldson E, Vabret A, Baric R, van der Hoek L, Pickles R. 2010. Culturing the unculturable: human coronavirus HKU1 infects, replicates, and produces progeny virions in human ciliated airway epithelial cell cultures. J Virol 84:11255-11263. http://dx.doi.org/10.1128/JVI.00947-10.
6. Lau SK, Li KS, Tsang AK, Lam CS, Ahmed S, Chen H, Chan KH, Woo PC, Yuen KY. 2013. Genetic characterization of Betacoronavirus lineage C viruses in bats reveals marked sequence divergence in the spike protein of Pipistrellus bat coronavirus HKU5 in Japanese pipistrelle: implications for the origin of the novel Middle East respiratory syndrome coronavirus. J Virol 87:8638-8650. http://dx.doi.org/10.1128/JVI.01055-13.
7. van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus AD, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RA. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. mBio 3(6):e00473-12. http://dx.doi.org/10.1128/mBio.00473-12.
8. Coleman CM, Frieman MB. 2013. Emergence of the Middle East respiratory syndrome coronavirus. PLoS Pathog 9:e1003595. http://dx.doi.org /10.1371/journal.ppat.1003595.
9. Alagaili AN, Briese T, Mishra N, Kapoor V, Sameroff SC, de Wit E, Munster VJ, Hensley LE, Zalmout IS, Kapoor A, Epstein JH, Karesh WB, Daszak P, Mohammed OB, Lipkin WI. 2014. Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. mBio 5(2):e00884-14. http://dx.doi.org/10.1128/mBio.00884-14.
10. Ferguson NM, Van Kerkhove MD. 2014. Identification of MERS-CoV in dromedary camels. Lancet Infect Dis 14:93-94. http://dx.doi.org/10.1016 /S1473-3099(13)70691-1.
11. Zumla AI, Memish ZA. 2014. Middle East respiratory syndrome coronavirus: epidemic potential or a storm in a teacup? Eur Respir J 43:1243-1248. http://dx.doi.org/10.1183/09031936.00227213.
12. Bermingham A, Chand MA, Brown CS, Aarons E, Tong C, Langrish C, Hoschler K, Brown K, Galiano M, Myers R, Pebody RG, Green HK, Boddington NL, Gopal R, Price N, Newsholme W, Drosten C, Fouchier RA, Zambon M. 2012. Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012. Euro Surveill 17(40):pii-20290. http://www .eurosurveillance.org/ViewArticle.aspx?ArticleId-20290.
13. Geng H, Tan W. 2013. A novel human coronavirus: Middle East respiratory syndrome human coronavirus. Sci China Life Sci 56:683-687. http: //dx.doi.org/10.1007/s11427-013-4519-8.
14. Al-Tawfiq JA, Memish ZA. 2014. What are our pharmacotherapeutic options for MERS-CoV? Expert Rev Clin Pharmacol 7:235-238. http://dx .doi.org/10.1586/17512433.2014.890515.
15. Zielecki F, Weber M, Eickmann M, Spiegelberg L, Zaki AM, Matrosovich M, Becker S, Weber F. 2013. Human cell tropism and innate immune system interactions of human respiratory coronavirus EMC compared to those of severe acute respiratory syndrome coronavirus. J Virol 87:5300-5304. http://dx.doi.org/10.1128/JVI.03496-12.
16. Kindler E, Jonsdottir HR, Muth D, Hamming OJ, Hartmann R, Rodriguez R, Geffers R, Fouchier RA, Drosten C, Muller MA, Dijkman R, Thiel V. 2013. Efficient replication of the novel human betacoronavirus EMC on primary human epithelium highlights its zoonotic potential. mBio 4(1):e00611-12. http://dx.doi.org/10.1128/mBio.00611-12.
17. Hart BJ, Dyall J, Postnikova E, Zhou H, Kindrachuk J, Johnson RF, Olinger GG, Jr, Frieman MB, Holbrook MR, Jahrling PB, Hensley L. 2014. Interferon-beta and mycophenolic acid are potent inhibitors of Middle East respiratory syndrome coronavirus in cell-based assays. J Gen Virol 95:571-577. http://dx.doi.org/10.1099/vir.0.061911-0.
18. Chan JF, Chan KH, Kao RY, To KK, Zheng BJ, Li CP, Li PT, Dai J, Mok FK, Chen H, Hayden FG, Yuen KY. 2013. Broad-spectrum antivirals for the emerging Middle East respiratory syndrome coronavirus. J Infect 67: 606-616. http://dx.doi.org/10.1016/j.jinf.2013.09.029.
19. Falzarano D, de Wit E, Martellaro C, Callison J, Munster VJ, Feldmann H. 2013. Inhibition of novel - coronavirus replication by a combination of interferon-2b and ribavirin. Sci Rep 3:1686. http://dx.doi.org/10.1038 /srep01686.
20. Josset L, Menachery VD, Gralinski LE, Agnihothram S, Sova P, Carter VS, Yount BL, Graham RL, Baric RS, Katze MG. 2013. Cell host response to infection with novel human coronavirusEMCpredicts potential antivirals and important differences with SARS coronavirus. mBio 4(3): e00165-13. http://dx.doi.org/10.1128/mBio.00165-13.
21. Clarke P, Leser JS, Bowen RA, Tyler KL. 2014. Virus-induced transcriptional changes in the brain include the differential expression of genes associated with interferon, apoptosis, interleukin 17 receptor A, and glutamate signaling as well as flavivirus-specific upregulation of tRNA synthetases. mBio 5(2):e00902-14. http://dx.doi.org/10.1128/mBio.00902-14.
22. Kindrachuk J, Arsenault R, Kusalik A, Kindrachuk KN, Trost B, Napper S, Jahrling PB, Blaney JE. 2012. Systems kinomics demonstrates Congo Basin monkeypox virus infection selectively modulates host cell signaling responses as compared to West African monkeypox virus. Mol Cell Proteomics 11:M111.015701. http://dx.doi.org/10.1074/mcp.M111.015701.
23. Maattanen P, Trost B, Scruten E, Potter A, Kusalik A, Griebel P, Napper S. 2013. Divergent immune responses to Mycobacterium avium subsp. paratuberculosis infection correlate with kinome responses at the site of intestinal infection. Infect Immun 81:2861-2872. http://dx.doi.org /10.1128/IAI.00339-13.
24. Mulongo M, Prysliak T, Scruten E, Napper S, Perez-Casal J. 2014. In vitro infection of bovine monocytes with Mycoplasma bovis delays apoptosis and suppresses production of gamma interferon and tumor necrosis factor alpha but not interleukin-10. Infect Immun 82:62-71. http://dx .doi.org/10.1128/IAI.00961-13.
25. Cohen P. 2002. Protein kinases-the major drug targets of the twentyfirst century? Nat Rev Drug Discov 1:309-315. http://dx.doi.org/10.1038 /nrd773.
26. Hopkins AL, Groom CR. 2002. The druggable genome. Nat Rev Drug Discov 1:727-730. http://dx.doi.org/10.1038/nrd892.
27. de Wilde AH, Raj VS, Oudshoorn D, Bestebroer TM, van Nieuwkoop S, Limpens RW, Posthuma CC, van der Meer Y, Barcena M, Haagmans BL, Snijder EJ, van den Hoogen BG. 2013. MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J Gen Virol 94:1749-1760. http://dx.doi.org/10.1099/vir.0.052910-0.
28. de Wit E, Rasmussen AL, Falzarano D, Bushmaker T, Feldmann F, Brining DL, Fischer ER, Martellaro C, Okumura A, Chang J, Scott D, Benecke AG, Katze MG, Feldmann H, Munster VJ. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. Proc Natl Acad Sci U S A 110:16598-16603. http://dx.doi.org/10.1073/pnas.1310744110.
29. Li Y, Arsenault RJ, Trost B, Slind J, Griebel PJ, Napper S, Kusalik A. 2012. A systematic approach for analysis of peptide array kinome data. Sci Signal 5:pl2. http://dx.doi.org/10.1126/scisignal.2002429.
30. Trost B, Kindrachuk J, Maattanen P, Napper S, Kusalik A. 2013. PIIKA 2: an expanded, web-based platform for analysis of kinome microarray data. PLoS One 8:e80837. http://dx.doi.org/10.1371/journal.pone.0080837.
31. Lynn DJ, Winsor GL, Chan C, Richard N, Laird MR, Barsky A, Gardy JL, Roche FM, Chan TH, Shah N, Lo R, Naseer M, Que J, Yau M, Acab M, Tulpan D, Whiteside MD, Chikatamarla A, Mah B, Munzner T, Hokamp K, Hancock RE, Brinkman FS. 2008. InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol 4:218. http://dx.doi.org/10.1038/msb.2008.55.
32. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. http://dx.doi.org/10 .1038/nmeth.2089.
33. Dorlo TP, Balasegaram M, Beijnen JH, de Vries PJ. 2012. Miltefosine: a review of its pharmacology and therapeutic efficacy in the treatment of leishmaniasis. J Antimicrob Chemother 67:2576-2597. http://dx.doi.org /10.1093/jac/dks275.
34. Bowick GC, Fennewald SM, Scott EP, Zhang L, Elsom BL, Aronson JF, Spratt HM, Luxon BA, Gorenstein DG, Herzog NK. 2007. Identification of differentially activated cell-signaling networks associated with pichinde virus pathogenesis by using systems kinomics. J Virol 81:1923-1933. http: //dx.doi.org/10.1128/JVI.02199-06.
35. Knuutila S, Bjorkqvist AM, Autio K, Tarkkanen M, Wolf M, Monni O, Szymanska J, Larramendy ML, Tapper J, Pere H, El-Rifai W, Hemmer S, Wasenius VM, Vidgren V, Zhu Y. 1998. DNA copy number amplifications in human neoplasms: review of comparative genomic hybridization studies. Am J Pathol 152:1107-1123.
36. Ji WT, Liu HJ. 2008. PI3K-Akt signaling and viral infection. Recent Pat Biotechnol 2:218-226. http://dx.doi.org/10.2174/187220808786241042.
37. Ehrhardt C, Ludwig S. 2009. A new player in a deadly game: influenza viruses and the PI3K/Akt signalling pathway. Cell Microbiol 11:863-871. http://dx.doi.org/10.1111/j.1462-5822.2009.01309.x.
38. Pleschka S. 2008. RNA viruses and the mitogenic Raf/MEK/ERK signal transduction cascade. Biol Chem 389:1273-1282. http://dx.doi.org/10 .1515/BC.2008.145.
39. Ueda Y, Hirai S, Osada S, Suzuki A, Mizuno K, Ohno S. 1996. Protein kinase C activates the MEK-ERK pathway in a manner independent of Ras and dependent on Raf. J Biol Chem 271:23512-23519. http://dx.doi.org /10.1074/jbc.271.38.23512.
40. Falzarano D, de Wit E, Rasmussen AL, Feldmann F, Okumura A, Scott DP, Brining D, Bushmaker T, Martellaro C, Baseler L, Benecke AG, Katze MG, Munster VJ, Feldmann H. 2013. Treatment with interferonalpha2b and ribavirin improves outcome in MERS-CoV-infected rhesus macaques. Nat Med 19:1313-1317. http://dx.doi.org/10.1038/nm.3362.
41. Ludwig S. 2011. Disruption of virus-host cell interactions and cell signaling pathways as an anti-viral approach against influenza virus infections. Biol Chem 392:837-847. http://dx.doi.org/10.1515/BC.2011.121.
42. Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG. 2012. Into the eye of the cytokine storm. Microbiol Mol Biol Rev 76:16-32. http://dx.doi.org/10.1128/MMBR.05015-11.
43. Buchkovich NJ, Yu Y, Zampieri CA, Alwine JC. 2008. The TORrid affairs of viruses: effects of mammalian DNA viruses on the PI3K-AktmTOR signalling pathway. Nat Rev Microbiol 6:266-275. http://dx.doi .org/10.1038/nrmicro1855.
44. Wang G, Barrett JW, Stanford M, Werden SJ, Johnston JB, Gao X, Sun M, Cheng JQ, McFadden G. 2006. Infection of human cancer cells with myxoma virus requires Akt activation via interaction with a viral ankyrinrepeat host range factor. Proc Natl Acad Sci U S A 103:4640-4645. http: //dx.doi.org/10.1073/pnas.0509341103.
45. Qin D, Feng N, Fan W, Ma X, Yan Q, Lv Z, Zeng Y, Zhu J, Lu C. 2011. Activation of PI3K/AKT and ERK MAPK signal pathways is required for the induction of lytic cycle replication of Kaposi's sarcoma-associated herpesvirus by herpes simplex virus type 1. BMC Microbiol 11:240. http://dx .doi.org/10.1186/1471-2180-11-240.
46. Norman KL, Hirasawa K, Yang AD, Shields MA, Lee PW. 2004. Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc Natl Acad Sci U S A 101:11099-11104. http://dx.doi.org/10.1073/pnas.0404310101.
47. Nakamichi K, Inoue S, Takasaki T, Morimoto K, Kurane I. 2004. Rabies virus stimulates nitric oxide production and CXC chemokine ligand 10 expression in macrophages through activation of extracellular signalregulated kinases 1 and 2. J Virol 78:9376-9388. http://dx.doi.org/10.1128 /JVI.78.17.9376-9388.2004.
48. Chung TW, Lee YC, Kim CH. 2004. Hepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3K/AKT pathways: involvement of invasive potential. FASEB J 18:1123-1125. http://dx.doi.org/10.1096/fj.03-1429fje.