Targeting cell division cycle 25 homolog B to regulate influenza virus replication

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13775-13784

  Perwitasari, Olivia ^a   Torrecilhas, Ana Claudia ^a,b   Yan, Xiuzhen ^a   Johnson, Scott ^a   White, Caleb ^a   Mark Tompkins, S ^a   Tripp, Ralph A ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CELL DIVISION CYCLE 25 HOMOLOG B; DIMETHYL SULFOXIDE; DUAL SPECIFICITY PHOSPHATASE; NONSTRUCTURAL PROTEIN 1; NSC 95397; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL NUCLEUS; CHROMATIN; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN; HUMAN CELL; INFLUENZA A; INFLUENZA VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA SYNTHESIS; TRANSCRIPTION TERMINATION; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS REPLICATION;

ANIMALS; CDC25 PHOSPHATASES; CELL LINE; FEMALE; GENE TARGETING; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA, HUMAN; INTERFERON-BETA; MICE; MICE, INBRED BALB C; RNA INTERFERENCE; VIRUS REPLICATION;

EID: 84888024948     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01509-13     Document Type: Article

References (65)

1. Girard MP, Tam JS, Assossou OM, Kieny MP. 2010. The A (H1N1) influenza virus pandemic:a review. Vaccine 28:4895-4902.
2. Monto AS. 2003. The role of antivirals in the control of influenza. Vaccine 21:1796-1800.
3. McKimm-Breschkin JL. 2005. Management of influenza virus infections with neuraminidase inhibitors:detection, incidence, and implications of drug resistance. Treat Respir. Med. 4:107-116.
4. Pinto LH, Holsinger LJ, Lamb RA. 1992. Influenza virus M2 protein has ion channel activity. Cell 69:517-528.
5. Boltz DA, Aldridge JR, Jr, Webster RG, Govorkova EA. 2010. Drugs in development for influenza. Drugs 70:1349-1362.
6. Layne SP, Monto AS, Taubenberger JK. 2009. Pandemic influenza:an inconvenient mutation. Science 323:1560-1561.
7. Simonsen L, Clarke MJ, Williamson GD, Stroup DF, Arden NH, Schonberger LB. 1997. The impact of influenza epidemics on mortality:introducing a severity index. Am. J. Public Health 87:1944-1950.
8. Deyde VM, Xu X, Bright RA, Shaw M, Smith CB, Zhang Y, Shu Y, Gubareva LV, Cox NJ, Klimov AI. 2007. Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J. Infect. Dis. 196:249-257.
9. Nguyen JT, Hoopes JD, Le MH, Smee DF, Patick AK, Faix DJ, Blair PJ, de Jong MD, Prichard MN, Went GT. 2010. Triple combination of amantadine, ribavirin, and oseltamivir is highly active and synergistic against drug resistant influenza virus strains in vitro. PLoS One 5:e9332. doi:10.1371/journal.pone.0009332.
10. Min JY, Subbarao K. 2010. Cellular targets for influenza drugs. Nat. Biotechnol. 28:239-240.
11. Watanabe T, Watanabe S, Kawaoka Y. 2010. Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 7:427-439.
12. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, Ryan BJ, Weyer JL, van der Weyden L, Fikrig E, Adams DJ, Xavier RJ, Farzan M, Elledge SJ. 2009. The IFITM proteins mediate cellular resistance to influenzaAH1N1 virus, West Nile virus, and dengue virus. Cell 139:1243-1254.
13. Hao L, Sakurai A, Watanabe T, Sorensen E, Nidom CA, Newton MA, Ahlquist P, Kawaoka Y. 2008. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 454:890-893.
14. Karlas A, Machuy N, Shin Y, Pleissner K-P, Artarini A, Heuer D, Becker D, Khalil H, Ogilvie LA, Hess S, Maurer AP, Muller E, Wolff T, Rudel T, Meyer TF. 2010. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463:818-822.
15. König R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, Bhattacharyya S, Alamares JG, Tscherne DM, Ortigoza MB, Liang Y, Gao Q, Andrews SE, Bandyopadhyay S, De Jesus P, Tu BP, Pache L, Shih C, Orth A, Bonamy G, Miraglia L, Ideker T, Garcia-Sastre A, Young JAT, Palese P, Shaw ML, Chanda SK. 2010. Human host factors required for influenza virus replication. Nature 463:813-817.
16. Perwitasari O, Yan X, Johnson S, White C, Brooks P, Tompkins SM, Tripp RA. 5 November 2012. Targeting the organic anion transporter-3 (OAT3) with probenecid as a novel anti-influenza A virus strategy. Antimicrob. Agents Chemother. doi:10.1128/AAC.01532-12.
17. Melén K, Kinnunen L, Fagerlund R, Ikonen N, Twu KY, Krug RM, Julkunen I. 2007. Nuclear and nucleolar targeting of influenza A virus NS1 protein:striking differences between different virus subtypes. J. Virol. 81:5995-6006.
18. Goodman AG, Smith JA, Balachandran S, Perwitasari O, Proll SC, Thomas MJ, Korth MJ, Barber GN, Schiff LA, Katze MG. 2007. The cellular protein P58IPK regulates influenza virus mRNA translation and replication through a PKR-mediated mechanism. J. Virol. 81:2221-2230.
19. Meliopoulos VA, Andersen LE, Birrer KF, Simpson KJ, Lowenthal JW, Bean AG, Stambas J, Stewart CR, Tompkins SM, van Beusechem VW, Fraser I, Mhlanga M, Barichievy S, Smith Q, Leake D, Karpilow J, Buck A, Jona G, Tripp RA. 2012. Host gene targets for novel influenza therapies elucidated by high-throughput RNA interference screens. FASEB J. 26:1372-1386.
20. Meliopoulos VA, Andersen LE, Brooks P, Yan X, Bakre A, Coleman JK, Tompkins SM, Tripp RA. 2012. MicroRNA regulation of human protease genes essential for influenza virus replication. PLoS One 7:e37169. doi:10.1371/journal.pone.0037169.
21. Kristjánsdóttir K, Rudolph J. 2004. Cdc25 phosphatases and cancer. Chem. Biol. 11:1043-1051.
22. Nayak DP, Hui EK, Barman S. 2004. Assembly and budding of influenza virus. Virus Res. 106:147-165.
23. Samji T. 2009. Influenza A:understanding the viral life cycle. Yale J. Biol. Med. 82:153-159.
24. Paterson D, Fodor E. 2012. Emerging roles for the influenza A virus nuclear export protein (NEP). PLoS Pathog. 8:e1003019. doi:10.1371/journal.ppat.1003019.
25. Min J-Y, Krug RM. 2006. The primary function of RNA binding by the influenza A virus NS1 protein in infected cells:inhibiting the 2'-5' oligo (A) synthetase/RNase L pathway. Proc. Natl. Acad. Sci. U.S.A. 103:7100-7105.
26. Hale BG, Randall RE, Ortín J, Jackson D. 2008. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89:2359-2376.
27. Krug RM, Yuan W, Noah DL, Latham AG. 2003. Intracellular warfare between human influenza viruses and human cells:the roles of the viral NS1 protein. Virology 309:181-189.
28. Nemeroff ME, Barabino SM, Li Y, Keller W, Krug RM. 1998. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3'end formation of cellular pre-mRNAs. Mol. Cell 1:991-1000.
29. Qiu Y, Krug RM. 1994. The influenza virus NS1 protein is a poly(A)-binding protein that inhibits nuclear export of mRNAs containing poly(A). J. Virol. 68:2425-2432.
30. Lu Y, Wambach M, Katze MG, Krug RM. 1995. Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214:222-228.
31. Garfinkel MS, Katze MG. 1993. Translational control by influenza virus. Selective translation is mediated by sequences within the viral mRNA 5'-untranslated region. J. Biol. Chem. 268:22223-22226.
32. Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M, Jr, Garcia-Sastre A. 2007. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 81:514-524.
33. Opitz B, Rejaibi A, Dauber B, Eckhard J, Vinzing M, Schmeck B, Hippenstiel S, Suttorp N, Wolff T. 2007. IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell. Microbiol. 9:930-938.
34. Guo Z, Chen LM, Zeng H, Gomez JA, Plowden J, Fujita T, Katz JM, Donis RO, Sambhara S. 2007. NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am. J. Respir. Cell Mol. Biol. 36:263-269.
35. Satterly N, Tsai PL, van Deursen J, Nussenzveig DR, Wang Y, Faria PA, Levay A, Levy DE, Fontoura BM. 2007. Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc. Natl. Acad. Sci. U.S.A. 104:1853-1858.
36. Park YW, Katze MG. 1995. Translational control by influenza virus:identification of cis-acting sequences and trans-acting factors which may regulate selective viral mRNA translation. J. Biol. Chem. 270:28433-28439.
37. Marazzi I, Ho JS, Kim J, Manicassamy B, Dewell S, Albrecht RA, Seibert CW, Schaefer U, Jeffrey KL, Prinjha RK, Lee K, Garcia-Sastre A, Roeder RG, Tarakhovsky A. 2012. Suppression of the antiviral response by an influenza histone mimic. Nature 483:428-433.
38. Hale BG, Knebel A, Botting CH, Galloway CS, Precious BL, Jackson D, Elliott RM, Randall RE. 2009. CDK/ERK-mediated phosphorylation of the human influenza A virus NS1 protein at threonine-215. Virology 383:6-11.
39. Lazo JS, Nemoto K, Pestell KE, Cooley K, Southwick EC, Mitchell DA, Furey W, Gussio R, Zaharevitz DW, Joo B, Wipf P. 2002. Identification of a potent and selective pharmacophore for Cdc25 dual specificity phosphatase inhibitors. Mol. Pharmacol. 61:720-728.
40. Park H, Carr BI, Li M, Ham SW. 2007. Fluorinated NSC as a Cdc25 inhibitor. Bioorg. Med. Chem. Lett. 17:2351-2354.
41. Gaush CR, Smith TF. 1968. Replication and plaque assay of influenza virus in an established line of canine kidney cells. Appl. Microbiol. 16:588-594.
42. Szretter KJ, Balish AL, Katz JM. 2005. Influenza:propagation, quantification, and storage. Curr. Protoc. Microbiol. 3:15G.1.1-15G.1.22. doi:10.1002/0471729256.mc15g01s3.
43. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 27:493-497. http://aje.oxfordjournals.org/content/27/3/493.full.pdf+html.
44. Jones RE, Zheng W, McKew JC, Chen CZ. 24 May 2013. An alternative direct compound dispensing method using theHPD300 digital dispenser. J. Lab. Autom. [Epub ahead of print.]. doi:10.1177/2211068213491094.
45. Kawakami E, Watanabe T, Fujii K, Goto H, Watanabe S, Noda T, Kawaoka Y. 2011. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J. Virol. Methods 173:1-6.
46. Rustagi A, Doehle BP, McElrath MJ, Gale M, Jr. 2013. Two new monoclonal antibodies for biochemical and flow cytometric analyses of human interferon regulatory factor-3 activation, turnover, and depletion. Methods 59:225-232.
47. Nemoto K, Vogt A, Oguri T, Lazo JS. 2004. Activation of the Raf-1/ MEK/Erk kinase pathway by a novel Cdc25 inhibitor in human prostate cancer cells. Prostate 58:95-102.
48. Peyregne VP, Kar S, Ham SW, Wang M, Wang Z, Carr BI. 2005. Novel hydroxyl naphthoquinones with potent Cdc25 antagonizing and growth inhibitory properties. Mol. Cancer Ther. 4:595-602.
49. Bugler B, Schmitt E, Aressy B, Ducommun B. 2010. Unscheduled expression of CDC25B in S-phase leads to replicative stress and DNA damage. Mol. Cancer 9:29. doi:10.1186/1476-4598-9-29.
50. Boutros R, Lobjois V, Ducommun B. 2007. CDC25 phosphatases in cancer cells:key players? Good targets? Nat. Rev. Cancer 7:495-507.
51. Greenspan D, Palese P, Krystal M. 1988. Two nuclear location signals in the influenza virus NS1 nonstructural protein. J. Virol. 62:3020-3026.
52. Li Y, Yamakita Y, Krug RM. 1998. Regulation of a nuclear export signal by an adjacent inhibitory sequence:the effector domain of the influenza virus NS1 protein. Proc. Natl. Acad. Sci. U.S.A. 95:4864-4869.
53. Fortes P, Beloso A, Ortin J. 1994. Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J. 13:704-712.
54. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, McCauley J, Digard P. 2001. Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J. Virol. 75:408-419.
55. Chase GP, Rameix-Welti MA, Zvirbliene A, Zvirblis G, Götz V, Wolff T, Naffakh N, Schwemmle M. 2011. Influenza virus ribonucleoprotein complexes gain preferential access to cellular export machinery through chromatin targeting. PLoS Pathog. 7:e1002187. doi:10.1371/journal.ppat.1002187.
56. Shapira SD, Gat-Viks I, Shum BOV, Dricot A, de Grace MM, Wu L, Gupta PB, Hao T, Silver SJ, Root DE, Hill DE, Regev A, Hacohen N. 2009. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 139:1255-1267.
57. Sui B, Bamba D, Weng K, Ung H, Chang S, Van Dyke J, Goldblatt M, Duan R, Kinch MS, Li W-B. 2009. The use of random homozygous gene perturbation to identify novel host-oriented targets for influenza. Virology 387:473-481.
58. Lyon MA, Ducruet AP, Wipf P, Lazo JS. 2002. Dual-specificity phosphatases as targets for antineoplastic agents. Nat. Rev. Drug Discov. 1:961-976.
59. DeCaprio JA, Ludlow JW, Figge J, Shew JY, Huang CM, Lee WH, Marsilio E, Paucha E, Livingston DM. 1988. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 54:275-283.
60. Eckner R, Ewen ME, Newsome D, Gerdes M, DeCaprio JA, Lawrence JB, Livingston DM. 1994. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev. 8:869-884.
61. Goh WC, Rogel ME, Kinsey CM, Michael SF, Fultz PN, Nowak MA, Hahn BH, Emerman M. 1998. HIV-1 Vpr increases viral expression by manipulation of the cell cycle:a mechanism for selection of Vpr in vivo. Nat. Med. 4:65-71.
62. Parnell G, McLean A, Booth D, Huang S, Nalos M, Tang B. 2011. Aberrant cell cycle and apoptotic changes characterise severe influenza A infection-a meta-analysis of genomic signatures in circulating leukocytes. PLoS One 6:e17186. doi:10.1371/journal.pone.0017186.
63. Boulo S, Akarsu H, Ruigrok RW, Baudin F. 2007. Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res. 124:12-21.
64. Neumann G, Brownlee GG, Fodor E, Kawaoka Y. 2004. Orthomyxovirus replication, transcription, and polyadenylation. Curr. Top. Microbiol. Immunol. 283:121-143.
65. Vreede FT, Brownlee GG. 2007. Influenza virion-derived viral ribonucleoproteins synthesize both mRNA and cRNA in vitro. J. Virol. 81:2196-2204.