MAPK signal-integrating kinase controls cap-independent translation and cell type-specific cytotoxicity of an oncolytic poliovirus

Molecular Therapy

Volumn 18, Issue 11, 2010, Pages 1937-1946

  Goetz, Christian ^a   Everson, Richard G ^a   Zhang, Linda C ^a   Gromeier, Matthias ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; INITIATION FACTOR 4E; MITOGEN ACTIVATED PROTEIN KINASE SIGNAL INTEGRATING KINASE 1; ONCOLYTIC POLIOMYELITIS VIRUS; ONCOLYTIC VIRUS; PHOSPHOTRANSFERASE; RAS PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CATALYSIS; CELL SPECIFICITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; EMBRYO; ENZYME ACTIVITY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOLYTIC VIROTHERAPY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; VIROGENESIS; VIRUS REPLICATION;

ANIMALIA; EUKARYOTA; POLIOVIRUS;

EID: 78049452625     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.145     Document Type: Article

References (43)

1. Gromeier, M, Lachmann, S, Rosenfeld, MR, Gutin, PH and Wimmer, E (2000). Intergeneric poliovirus recombinants for the treatment of malignant glioma. Proc Natl Acad Sci USA 97: 6803-6808.
2. Gromeier, M, Alexander, L and Wimmer, E (1996). Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc Natl Acad Sci USA 93: 2370-2375.
3. Campbell, SA, Lin, J, Dobrikova, EY and Gromeier, M (2005). Genetic determinants of cell type-specifc poliovirus propagation in HEK 293 cells. J Virol 79: 6281-6290.
4. Yang, X, Chen, E, Jiang, H, Muszynski, K, Harris, RD, Giardina, SL et al. (2009). Evaluation of IRES-mediated, cell-type-specifc cytotoxicity of poliovirus using a colorimetric cell proliferation assay. J Virol Methods 155: 44-54.
5. Dobrikova, EY, Broadt, T, Poiley-Nelson, J, Yang, X, Soman, G, Giardina, S et al. (2008). Recombinant oncolytic poliovirus eliminates glioma in vivo without genetic adaptation to a pathogenic phenotype. Mol Ther 16: 1865-1872.
6. Sonenberg, N, Morgan, MA, Merrick, WC and Shatkin, AJ (1978). A polypeptide in eukaryotic initiation factors that crosslinks specifcally to the 5'-terminal cap in mRNA. Proc Natl Acad Sci USA 75: 4843-4847.
7. Morley, SJ, Curtis, PS and Pain, VM (1997). eIF4G: translation's mystery factor begins to yield its secrets. RNA 3: 1085-1104.
8. Hentze, MW (1997). eIF4G: a multipurpose ribosome adapter? Science 275: 500-501.
9. Pelletier, J and Sonenberg, N (1988). Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334: 320-325.
10. Jang, SK, Kräusslich, HG, Nicklin, MJ, Duke, GM, Palmenberg, AC and Wimmer, E (1988). A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol 62: 2636-2643.
11. Nomoto, A, Lee, YF and Wimmer, E (1976). The 5' end of poliovirus mRNA is not capped with m7G(5')ppp(5')Np. Proc Natl Acad Sci USA 73: 375-380.
12. De Breyne, S, Yu, Y, Unbehaun, A, Pestova, TV and Hellen, CU (2009). Direct functional interaction of initiation factor eIF4G with type 1 internal ribosomal entry sites. Proc Natl Acad Sci 37: 5167-5182.
13. Kaiser, C, Dobrikova, EY, Bradrick, SS, Shveygert, M, Herbert, JT and Gromeier, M (2008). Activation of cap-independent translation by variant eukaryotic initiation factor 4G in vivo. RNA 14: 2170-2182.
14. Pause, A, Belsham, GJ, Gingras, AC, Donzé, O, Lin, TA, Lawrence, JC Jr et al. (1994). Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5'-cap function. Nature 371: 762-767.
15. Raught, B, Gingras, AC, Gygi, SP, Imataka, H, Morino, S, Gradi, A et al. (2000). Serum-stimulated, rapamycin-sensitive phosphorylation sites in the eukaryotic translation initiation factor 4GI. EMBO J 19: 434-444.
16. Beretta, L, Gingras, AC, Svitkin, YV, Hall, MN and Sonenberg, N (1996). Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J 15: 658-664.
17. Fukunaga, R and Hunter, T (1997). MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J 16: 1921-1933.
18. Waskiewicz, AJ, Flynn, A, Proud, CG and Cooper, JA (1997). Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16: 1909-1920.
19. Pyronnet, S, Imataka, H, Gingras, AC, Fukunaga, R, Hunter, T and Sonenberg, N (1999). Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J 18: 270-279.
20. Svitkin, YV, Herdy, B, Costa-Mattioli, M, Gingras, AC, Raught, B and Sonenberg, N (2005). Eukaryotic translation initiation factor 4E availability controls the switch between cap-dependent and internal ribosomal entry site-mediated translation. Mol Cell Biol 25: 10556-10565.
21. Cancer Genome Atlas Research Network (2008). Comprehensive genomic characterization defnes human glioblastoma genes and core pathways. Nature 455: 1061-1068.
22. Gupta, AK, Cerniglia, GJ, Mick, R, Ahmed, MS, Bakanauskas, VJ, Muschel, RJ et al. (2003). Radiation sensitization of human cancer cells in vivo by inhibiting the activity of PI3K using LY294002. Int J Radiat Oncol Biol Phys 56: 846-853.
23. Fan, QW, Specht, KM, Zhang, C, Goldenberg, DD, Shokat, KM and Weiss, WA (2003). Combinatorial effcacy achieved through two-point blockade within a signaling pathway-a chemical genetic approach. Cancer Res 63: 8930-8938.
24. Liu, TC, Wakimoto, H, Martuza, RL and Rabkin, SD (2007). Herpes simplex virus Us3(-) mutant as oncolytic strategy and synergizes with phosphatidylinositol 3-kinase-Akt targeting molecular therapeutics. Clin Cancer Res 13: 5897-5902.
25. Merrill, MK and Gromeier, M (2006). The double-stranded RNA binding protein 76:NF45 heterodimer inhibits translation initiation at the rhinovirus type 2 internal ribosome entry site. J Virol 80: 6936-6942.
26. Ueda, T, Watanabe-Fukunaga, R, Fukuyama, H, Nagata, S and Fukunaga, R (2004). Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol Cell Biol 24: 6539-6549.
27. Hirota, T, Irie, K, Okamoto, R, Ikeda, W and Takai, Y (2005). Transcriptional activation of the mouse Necl-5/Tage4/PVR/CD155 gene by fbroblast growth factor or oncogenic Ras through the Raf-MEK-ERK-AP-1 pathway. Oncogene 24: 2229-2235.
28. Walsh, D and Mohr, I (2004). Phosphorylation of eIF4E by Mnk-1 enhances HSV-1 translation and replication in quiescent cells. Genes Dev 18: 660-672.
29. Castelló, A, Quintas, A, Sánchez, EG, Sabina, P, Nogal, M, Carrasco, L et al. (2009). Regulation of host translational machinery by African swine fever virus. PLoS Pathog 5: e1000562.
30. Coffey, MC, Strong, JE, Forsyth, PA and Lee, PW (1998). Reovirus therapy of tumors with activated Ras pathway. Science 282: 1332-1334.
31. Noser, JA, Mael, AA, Sakuma, R, Ohmine, S, Marcato, P, Lee, PW et al. (2007). The RAS/Raf1/MEK/ERK signaling pathway facilitates VSV-mediated oncolysis: implication for the defective interferon response in cancer cells. Mol Ther 15: 1531-1536.
32. Alain, T, Lun, X, Martineau, Y, Sean, P, Pulendran, B, Petroulakis, E et al. (2010). Vesicular stomatitis virus oncolysis is potentiated by impairing mTORC1-dependent type I IFN production. Proc Natl Acad Sci USA 107: 1576-1581.
33. Etchison, D, Milburn, SC, Edery, I, Sonenberg, N and Hershey, JW (1982). Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J Biol Chem 257: 14806-14810.
34. Kuyumcu-Martinez, NM, Van Eden, ME, Younan, P and Lloyd, RE (2004). Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol Cell Biol 24: 1779-1790.
35. Gustin, KE and Sarnow, P (2001). Effects of poliovirus infection on nucleo-cytoplasmic traffcking and nuclear pore complex composition. EMBO J 20: 240-249.
36. Dobrikova, EY, Grisham, RN, Kaiser, C, Lin, J and Gromeier, M (2006). Competitive translation effciency at the picornavirus type 1 internal ribosome entry site facilitated by viral cis and trans factors. J Virol 80: 3310-3321.
37. Duncan, R, Milburn, SC and Hershey, JW (1987). Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control. Heat shock effects on eIF-4F. J Biol Chem 262: 380-388.
38. Marcotrigiano, J, Gingras, AC, Sonenberg, N and Burley, SK (1997). Cocrystal structure of the messenger RNA 5' cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89: 951-961.
39. Minich, WB, Balasta, ML, Goss, DJ and Rhoads, RE (1994). Chromatographic resolution of in vivo phosphorylated and nonphosphorylated eukaryotic translation initiation factor eIF-4E: increased cap affnity of the phosphorylated form. Proc Natl Acad Sci USA 91: 7668-7672.
40. Scheper, GC, van Kollenburg, B, Hu, J, Luo, Y, Goss, DJ and Proud, CG (2002). Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affnity for capped mRNA. J Biol Chem 277: 3303-3309.
41. Slepenkov, SV, Darzynkiewicz, E and Rhoads, RE (2006). Stopped-fow kinetic analysis of eIF4E and phosphorylated eIF4E binding to cap analogs and capped oligoribonucleotides: evidence for a one-step binding mechanism. J Biol Chem 281: 14927-14938.
42. Knauf, U, Tschopp, C and Gram, H (2001). Negative regulation of protein translation by mitogen-activated protein kinase-interacting kinases 1 and 2. Mol Cell Biol 21: 5500-5511.
43. Florez de Sessions, P, Dobrikova, E and Gromeier, M (2007). Genetic adaptation to untranslated region-mediated enterovirus growth defcits by mutations in the nonstructural proteins 3AB and 3CD. J Virol 81: 8396-8405.