The Role of Misshapen NCK-related kinase (MINK), a Novel Ste20 Family Kinase, in the IRES-Mediated Protein Translation of Human Enterovirus 71

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-33

  Leong, Shi Yun ^a   Ong, Bryan Kit Teck ^a   Chu, Justin Jang Hann ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL) IMIDAZOLE; CGP57380; ENZYME; ENZYME INHIBITOR; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MISSHAPEN NCK RELATED KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; P21 ACTIVATED KINASE 1; PROTEIN SERINE THREONINE KINASE; RENILLA LUCIFERIN 2 MONOOXYGENASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; ANTIVIRUS AGENT; INTERNAL RIBOSOME ENTRY SITE; MINK1 PROTEIN, HUMAN;

ARTICLE; CELL VIABILITY ASSAY; ENTEROVIRUS 71; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; INTERNAL RIBOSOME ENTRY SITE; LUCIFERASE ASSAY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA REPLICATION; RNA TRANSLATION; VIRAL PLAQUE ASSAY; WESTERN BLOTTING; CELL LINE; DRUG EFFECTS; ENTEROVIRUS A; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

HUMAN ENTEROVIRUS 71;

ANTIVIRAL AGENTS; CELL LINE; ENTEROVIRUS A, HUMAN; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INTERNAL RIBOSOME ENTRY SITES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; RNA, SMALL INTERFERING; RNA, VIRAL; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 84926430577     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004686     Document Type: Article

References (67)

1. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, et al. (1999) An epidemic of enterovirus 71 infection in Taiwan. New Engl J Med 341: 929–935. 10498487
2. Schmidt NJ, Lennette EH, Ho HH, (1974) An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis 129:304–309. 4361245
3. Cardosa MJ, Krishnan S, Tio PH, Perera D, Wong SC, (1999) Isolation of subgenus B adenovirus during a fatal outbreak of enterovirus 71-associated hand, foot, and mouth disease in Sibu, Sarawak. Lancet 354: 987–991. 10501361
4. Chan LG, Parashar UD, Lye MS, Ong FG, Zaki SR, et al. (2000) Deaths of children during an outbreak of hand, foot, and mouth disease in sarawak, malaysia: clinical and pathological characteristics of the disease. For the Outbreak Study Group. Clinical Infectious Diseases 31: 678–683. 11017815
5. Chan KP, Goh KT, Chong CY, Teo ES, Lau G, et al. (2003) Epidemic hand, foot and mouth disease caused by human enterovirus 71, Singapore. Emerg Infect Dis 9: 78–85 12533285
6. Wang JR, Tuan YC, Tsai HP, Yan JJ, Liu CC, et al. (2002) Change of major genotype of enterovirus 71 in outbreaks of hand-foot-and mouth disease in Taiwan between 1998 and 2000. J Clin Microbiol 40: 10–15. 11773085
7. Solomon T, Lewthwaite P, Cardosa MJ, McMinn P, Ooi MH, (2010) Enterovirus 71—An Emerging Virus With Pandemic Potential. Lancet Infect Dis 10: 778–90. doi: 10.1016/S1473-3099(10)70194-8 20961813
8. Wu KX, Ng MML, Chu JJH, (2010) Developments towards antiviral therapies against enterovirus 71. Drug Discov Today 15(23–24): 1041–1051. doi: 10.1016/j.drudis.2008.12.006 19150413
9. Yang Y, Zhang L, Fan X, Qin C, Liu J, (2012) Antiviral effect of geraniin on human enterovirus 71 in vitro and in vivo. Bioorg Med Chem Lett 22(6): 2209–2211 doi: 10.1016/j.bmcl.2012.01.102 22342145
10. Smyth MS, Martin JH, (2002). Picornavirus uncoating. Mol Pathol 55(4): 214–219. 12147709
11. McMinn PC, (2002) An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 26(1): 91–107. 12007645
12. Bedard KM, Semler BL, (2004) Regulation of picornavirus gene expression. Microbes Infect 6: 702–713. 15158778
13. Wimmer E, Nomoto A, (1993) Molecular biology and cell-free synthesis of poliovirus. Biologicals 21:349–356. 8024750
14. Shih SR, Stollar V, Li ML, (2011) Host factors in enterovirus 71 replication. J Virol 85(19): 9658–9666. doi: 10.1128/JVI.05063-11 21715481
15. Back SH, Kim YK, Kim WJ, Cho S, Oh HR, et al. (2002) Translation of polioviral mRNA is inhibited by cleavage of polypyrimidine tract-binding proteins executed by polioviral 3C(pro). J Virol 76: 2529–2542. 11836431
16. Florez PM, Sessions OM, Wagner EJ, Gromeier M, Garcia-Blanco MA, (2005) The polypyrimidine tract binding protein is required for efficient picornavirus gene expression and propagation. J Virol 79: 6172–6179 15858002
17. Hellen CU, Witherell GW, Schmid M, Shin SH, Pestova TV, et al. (1993) A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc Natl Acad Sci U S A 90: 7642–7646 8395052
18. Blyn LB, Swiderek KM, Richards O, Stahl DC, Semler BL, et al. (1996) Poly(rC) binding protein 2 binds to stem-loop IV of the poliovirus RNA 5′ noncoding region: identification by automated liquid chromatography-tandem mass spectrometry. Proc Natl Acad Sci USA 93:11115–11120 8855318
19. Huang PN, Lin JY, Locker N, Kung YA, Hung CT, et al. (2011) Far upstream element binding protein 1 binds the internal ribosomal entry site of enterovirus 71 and enhances viral translation and viral growth. Nucleic Acids Res 39:9633–9648 doi: 10.1093/nar/gkr682 21880596
20. Lin JY, Shih SR, Pan M, Li C, Lue CF, et al. (2009) hnRNP A1 interacts with the 5′ untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J Virol. 83: 6106–6114. doi: 10.1128/JVI.02476-08 19339352
21. Kyriakis JM, (1999) Signaling by the Germinal Center Kinase Family of Protein Kinases. J Biol Chem 274(9): 5259–5262. 10026130
22. Hu Y, Leo C, Yu S, Huang BC, Wang H, et al. (2004) Identification and functional characterization of a novel human misshapen/Nck interacting kinase-related kinase, hMINK beta. J Biol Chem 279: 54387–54397. 15469942
23. Dan I, Watanabe NM, Kobayashi T, Yamashita-Suzuki K, Fukagaya Y, et al. (2000) Molecular cloning of MINK, a novel member of mammalian GCK family kinases, which is up-regulated during postnatal mouse cerebral development. FEBS Lett 469(1): 19–23. 10708748
24. Garrington TP, Johnson GL, (1999) Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr Opin in Cell Biol 11(2): 211–218. 10209154
25. Hirasawa K, Kim A, Han HS, Han J, Jun HS, (2003) Effect of p38 Mitogen-Activated Protein Kinase on the Replication of Encephalomyocarditis Virus. J Virol 77(10): 5649–5656. 12719557
26. Hussain KM, Leong KL, Ng MM, Chu JJ, (2011) The essential role of clathrin-mediated endocytosis in the infectious entry of human enterovirus 71. J Biol Chem 286: 309–321. doi: 10.1074/jbc.M110.168468 20956521
27. Tomida J, Kitao H, Kinoshita E, Takata M (2008) Detection of phosphorylation on large proteins by western blotting using Phos-tag containing gel. Protocol exchange. Available: www.nature.com/protocolexchange.protocols/501. Accessed 26 November 2013.
28. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minowa T, et al. (2009) Scavenger receptor B2 is a cellular receptor for Enterovirus 71. Nat Med 15(7):798–801. doi: 10.1038/nm.1992 19543282
29. Hasan NM, Adams GE, Joiner MC, (1999) Effect of serum starvation on expression and phosphorylation of PKC-α and p53 in V79 cells: Implications for cell death. Int J Cancer 80(3): 400–405. 9935181
30. Chakravortty D, Kato Y, Sugiyama T, Koide N, Mu MM, et al. (2001) Inhibition of p38 Mitogen-Activated Protein Kinase Augments Lipopolysaccharide-Induced Cell Proliferation in CD14-Expressing Chinese Hamster Ovary Cells. Infect Immun 69: 931–936 11159988
31. Si X, McManus BM, Zhang J, Yuan J, Cheung C, Esfandiarei M, Suarez A, Morgan A, Luo H, (2005) Pyrrolidine dithiocarbamate reduces coxsackievirus B3 replication through inhibition of the ubiquitin-proteasome pathway. J. Virol 79:8014–8023. 15956547
32. Bek EJ, McMinn PC, (2010) Recent advances in research on human enterovirus 71. Future Virol 5(4): 453–468.
33. Chen YJ, Ng SJ, Hsu JTA, Horng JT, Yang HM Shih, et al. (2008). Amantadine as a regulator of internal ribosome entry site. Acta Pharmacol Sin 29:1327–1333. doi: 10.1111/j.1745-7254.2008.00876.x 18954527
34. Goetz C, Everson RG, Zhang LC, Gromeier M, (2010) MAPK signal-integrating kinase controls cap-independent translation and cell type-specific cytotoxicity of an oncolytic poliovirus.Mol Ther 18: 1937–1946. doi: 10.1038/mt.2010.145 20648000
35. van der Houven van Oordt W, Diaz-Meco MT, Lozano J, Krainer AR, Moscat J, et al. (2000) The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J Cell Biol 149: 307–316 10769024
36. Manders EEM, Verbeek FJ, Aten JA, (1993) Measurement of colocalisation of objects in dual-colour confocal images. J. Microsc 169: 375–382.
37. Ziaei S, Shimada N, Kucharavy H, Hubbard K, (2012) MNK1 expression increases during cellular senescence and modulates the subcellular localization of hnRNP A1. Exp Cell Res 10; 318(5):500–8 doi: 10.1016/j.yexcr.2011.12.015 22227431
38. Caignard G, Guerbois M, Labernardiere JL, Jacob Y, Jones LM, et al. (2007) Measles virus V protein blocks Jak1-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signalling. Virology 368: 351–362. 17686504
39. Hsu MJ, Wu CY, Chiang HH, Lai YL, Hung SL, (2010) PI3K/Akt signaling mediated apoptosis blockage and viral gene expression in oral epithelial cells during herpes simplex virus infection. Virus Res 153: 36–43. doi: 10.1016/j.virusres.2010.07.002 20620179
40. Nemerow GR, Stewart PL, (1999) Role of alpha(v) integrins in adenovirus cell entry and gene delivery. Microbiol Mol Biol R 63: 725–734. 10477314
41. Barber SA, Bruett L, Douglass BR, Herbst DS, Zink MC, et al. (2002) Visna virus-induced activation of MAPK is required for virus replication and correlates with virus-induced neuropathology. J Virol 76: 817–828 11752171
42. Tung WH, Hsieh HL, Yang CM, (2010) Enterovirus 71 induces COX-2 expression via MAPKs, NF-kappaB, and AP-1 in SK-N-SH cells: Role of PGE(2) in viral replication. Cell Signal 22: 234–246. doi: 10.1016/j.cellsig.2009.09.018 19800403
43. Wong WR, Chen YY, Yang SM, Chen YL, Horng JT, (2005) Phosphorylation of PI3K/Akt and MAPK/ERK in an early entry step of enterovirus 71. Life Sci 78: 82–90. 16150462
44. Johnston JB, Barrett JW, Chang W, Chung CS, Zeng W, et al. (2003) Role of the Serine-Threonine Kinase PAK-1 in Myxoma Virus Replication. J Virol 77, 5877–5888. 12719581
45. Carreno S, Engqvist-Goldstein AE, Zhang CX, McDonald KL, Drubin DG, (2004) Actin dynamics coupled to clathrin-coated vesicle formation at the trans-Golgi network. J Cell Biol 165: 781–788. 15210728
46. Merrifield CJ, Feldman ME, Wan L, Almers W, (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4: 691–698. 12198492
47. Liu CC, Chou AH, Lien SP, Lin HY, Liu SJ, et al. (2011) Identification and characterization of a cross-neutralization epitope of EV71. Vaccine 29: 4362–73. doi: 10.1016/j.vaccine.2011.04.010 21501643
48. Liu CC, Guo MS, Lin FHY, Hsiao KN, Chang KHW, et al. (2011) Purification and characterization of EV71 viral particles produced from Vero cell grown in a serum-free microcarrier bioreactor system. PloS ONE
49. Nicke B, Bastien J, Khanna SJ, Warne PH, Cowling V, et al. (2005) Involvement of MINK, a Ste20 family kinase, in Ras oncogene-induced growth arrest in human ovarian surface epithelial cells. Molec Cell 20(5): 673–685. 16337592
50. Banerjee S, Narayanan K, Mizutani T, Makino S, (2002) Murine Coronavirus Replication-Induced p38 Mitogen-Activated Protein Kinase Activation Promotes Interleukin-6 Production and Virus Replication in Cultured Cells. J Virol 76: 5937–5948. 12021326
51. Chang WW, Su IJ, Chang WT, Hwang W, Lei HY, (2008) Suppression of p38 mitogen-activated protein kinase inhibits hepatitis B virus replication in human hepatoma cell: the antiviral role of nitric oxide. J Viral Hepat 15(7):490–497. doi: 10.1111/j.1365-2893.2007.00968.x 18221299
52. Thompson SR, Sarnow P, (2003) Enterovirus 71 contains a type I IRES element that functions when eukaryotic initiation factor eIF4G is cleaved. Virology 315(1): 259–266. 14592777
53. Ho BC, Yu SL, Chen JJ, Chang SY, Yan BS, et al. (2011) Enterovirus-induced miR-141 contributes to shutoff of host protein translation by targeting the translation initiation factor eIF4E. Cell Host Microbe 9: 58–69. doi: 10.1016/j.chom.2010.12.001 21238947
54. Welnowska E, Sanz MA, Redondo N, Carrasco L, (2011) Translation of Viral mRNA without Active eIF2: The Case of Picornaviruses. PLoS ONE 6(7): e22230. doi: 10.1371/journal.pone.0022230 21779397
55. Fernandez J, Yaman I, Sarnow P, Snider MD, Hatzoglou M, (2002) Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2alpha. J Biol Chem 277: 19198–19205. 11877448
56. Hershey JW, (1989) Protein phosphorylation controls translation rates. J Biol Chem 264: 20823–20826. 2687263
57. Pisarev AV, Shirokikh NE, Hellen CU, (2005) Translation initiation by factor-independent binding of eukaryotic ribosomes to internal ribosomal entry sites. CR Biol 328: 589–605. 15992743
58. Robert F, Kapp LD, Khan SN, Acker MG, Kolitz S, et al. (2006) Initiation of protein synthesis by hepatitis C virus is refractory to reduced eIF2.GTP.Met-tRNA(i) (Met) ternary complex availability. Mol Biol Cell 17: 4632–4644 16928960
59. Black TL, Safer B, Hovanessian A, Katze MG, (1989) The cellular 68,000-Mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J Virol 63: 2244–2251. 2539516
60. Spriggs KA, Bushell M, Mitchell SA, Willis AE, (2005) Internal ribosome entry segment-mediated translation during apoptosis: the role of IRES-trans-acting factors. Cell death and differentiation 12: 585–591. 15900315
61. Cammas A, Pileur F, Bonnal S, Lewis SM, Leveque N, et al. (2007) Cytoplasmic Relocalization of Heterogeneous Nuclear Ribonucleoprotein A1 Controls Translation Initiation of Specific mRNAs. Mol Biol Cell 18: 5048–5059. 17898077
62. Pin˜ol-Roma S, Dreyfuss G, (1992) Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355: 730–732. 1371331
63. Monette A, Ajamian L, Lopez-Lastra M, Mouland AJ, (2009) Human immunodeficiency virus type 1 (HIV-1) induces the cytoplasmic retention of heterogeneous nuclear ribonucleoprotein A1 by disrupting nuclear import: implications for HIV-1 gene expression. J Biol Chem 284: 31350–31362. doi: 10.1074/jbc.M109.048736 19737937
64. Nakielny S, Dreyfuss G, (1999) Transport of proteins and RNAs in and out of the nucleus. Cell 99: 677–690. 10619422
65. Singh S, Poh CL, Chow VT, (2002) Complete sequence analyses of enterovirus 71 strains from fatal and non-fatal cases of the hand, foot and mouth disease outbreak in Singapore (2000). Microbiol Immunol 46: 801–808. 12516778
66. Romero JR, Rotbart HA, (1995) Sequence analysis of the downstream 5′ nontranslated region of seven echoviruses with different neurovirulence phenotypes. J Virol 69: 1370–1375. 7815524
67. Phuektes P, Chua BH, Sanders S, Bek EJ, Kok CC, et al. (2011) Mapping genetic determinants of the cell-culture growth phenotype of enterovirus 71. J Gen Virol 92(6): 1380–1390. doi: 10.1099/vir.0.029371-0 21346025