Viral oncolysis that targets raf-1 signaling control of nuclear transport

Journal of Virology

Volumn 84, Issue 4, 2010, Pages 2090-2099

  Riolobos, Laura ^a,c   Valle, Noelia ^a,d   Hernando, Eva ^a,e   Maroto, Beatriz ^a,f   Kann, Michael ^b,g   Almendral, José M ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c PROALT Parque Científico de Madrid PTM   (Spain)

^d INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f PROJECH Science to Technology Parque Cientifico de Madrid PTM   (Spain)

^g UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; ONCOLYTIC VIRUS; RAF PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INSECT CELL; LIFE CYCLE; MAMMAL CELL; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PARVOVIRUS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRUS CAPSID; VIRUS REPLICATION; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CAPSID PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL TRANSFORMATION, VIRAL; HELA CELLS; HUMANS; MICE; MINUTE VIRUS OF MICE; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PHOSPHORYLATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-RAF; RATS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SPODOPTERA; VIRUS ASSEMBLY;

HEXAPODA; MAMMALIA; MINUTE VIRUS OF MICE; MIRIDAE; PARVOVIRUS;

EID: 75449087432     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01550-09     Document Type: Article

References (83)

1. Adam, S. A., R. S. Marr, and L. Gerace. 1990. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111:807-816.
2. Berns, K., and C. R. Parrish. 2007. Parvoviridae, p. 2437-2477. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott-Raven Publishers, Philadelphia, PA.
3. Bialojan, C., and A. Takai. 1988. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases: specificity and kinetics. Biochem. J. 256:283-290.
4. Boehmer, T., S. Jeudy, Ian C. Berke, and T. U. Schwartz. 2008. Structural and functional studies of Nup107/Nup133 interaction and its implications for the architecture of the nuclear pore complex. Mol. Cell 30:721-731.
5. Caillet-Fauquet, P., M. Perros, A. Brandenburge, P. Spegelaere, and J. Rommelaere. 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding nonstructural proteins. EMBO J. 9:2989-2995.
6. Carreira, A., M. Menéndez, J. Reguera, J. M. Almendral, and M. G. Mateu. 2004. In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J. Biol. Chem. 279:6517-6525.
7. Chiocca, E. A. 2002. Oncolytic viruses. Nat. Rev. Cancer 2:938-950.
8. Chong, H., H. G. Vikis, and K. L. Guan. 2003. Mechanisms of regulating the Raf kinase family. Cell Signal. 15:463-469.
9. Cingolani, G., J. Bednenko, M. T. Gillespie, and L. Gerace. 2002. Molecular basis for the recognition of a nonclassical nuclear localization signal by importin beta. Mol. Cell 10:1345-1353.
10. Citovsky, V., D. Warnick, and P. Zambryski. 1994. Nuclear import of Agrobacterium Vird2 and VirE2 proteins in maize and tobacco. Proc. Natl. Acad. Sci. U. S. A. 91:3210-3214.
11. Cornelis, J. J., L. Deleu, U. Koch, and R. Rommelaere. 2006. Parvovirus oncosuppression, p. 365-378. In J. R. Kerr, S. F. Cotmore, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hodder Arnold, London, United Kingdom.
12. Cotmore, S. F., and P. Tattersall. 2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183-232.
13. Crawford, L. V. 1966. A minute virus of mice. Virology 29:605-612.
14. Cukor, G., N. R. Blacklow, S. Kibrick, and I. C. Swan. 1975. Effect of adeno-associated virus on cancer expression by herpesvirus-transformed hamster cells. J. Natl. Cancer Inst. 44:957-959.
15. Davies, H., G. R. Bignell, C. Cox, P. Stephens, S. Edkins, S. Clegg, J. Teague, H. Woffendin, M. J. Garnett, W. Bottomley, N. Davis, E. Dicks, R. Ewing, Y. Floyd, K. Gray, S. Hall, R. Hawes, J. Hughes, V. Kosmidou, A. Menzies, C. Mould, A. Parker, C. Stevens, S. Watt, S. Hooper, R. Wilson, H. Jayatilake, B. A. Gusterson, C. Cooper, J. Shipley, D. Hargrave, K. Pritchard-Jones, N. Maitland, G. Chenevix-Trench, G. J. Riggins, D. D. Bigner, G. Palmieri, A. Cossu, A. Flanagan, A. Nicholson, J. W. Ho, S. Y. Leung, S. T. Yuen, B. L. Weber, H. F. Seigler, T. L. Darrow, H. Paterson, R. Marais, C. J. Marshall, R. Wooster, M. R. Stratton, and P. A. Futreal. 2002. Mutations of the BRAF in human cancer. Nature 417:949-954.
16. Dhomen, N., J. S. Reis-Filho, S. da Rocha Dias, R. Hayward, K. Savage, V. Delmas, L. Larue, C. Pritchard, and R. Marais. 2009. Oncogenic Braf induces melanocyte senescente and melanoma in mice. Cancer Cell 15:294-303.
17. Finlay, D. R., D. D. Newmeywe, T. M. Price, and D. J. Forbes. 1987. Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J. Cell Biol. 104:189-200.
18. Gorlich, D., S. Prehn, R. A. Laskey, and E. Hartmann. 1994. Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79:767-778.
19. Gray-Schopfer, V., C. Wellbrock, and R. Marais. 2007. Melanoma biology and new targeted therapy. Nature 445:851-857.
20. Hernando, E., A. L. Llamas-Saiz, C. Foces-Foces, R. McKenna, L. Portman, M. Agbandje-McKenna, and J. M. Almendral. 2000. Biochemical and physical characterization of parvovirus minute virus of mice virus-like particles. Virology 267:299-309.
21. Hoss, A., I. Moarefi, K. H. Scheidtmann, L. J. Cisek, J. L. Corden, I. Dornreiter, A. K. Arthur, and E. Fanning. 1990. Altered phosphorylation pattern of simian virus 40 T antigen expressed in insect cells by using a baculovirus vector. J. Virol. 64:4799-4807.
22. Kalderon, D., W. D. Richardson, A. F. Markham, and A. E. Smith. 1984. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 311:33-38.
23. Kaufmann, B., A. López-Bueno, M. G. Mateu, P. R. Chipman, C. D. S. Nelson, C. R. Parrish, J. M. Almendral, and M. G. Rossmann. 2007. Minute virus of mice, a parvovirus, in complex with the Fab fragment of a neutralizing monoclonal antibody. J. Virol. 81:9851-9858.
24. Kerr, J. K., S. F. Cotmore, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.). 2006. Parvoviruses. Hodder Arnold, London, United Kingdom.
25. Khokhlatchev, A. V., B. Canagarajah, J. Wilsbacher, M. Robinson, M. Atkinson, E. Goldsmith, and M. H. Cobb. 1998. Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 93:605-615.
26. Kinkade, R., P. Dasgupta, A. Carie, D. Pernazza, M. Carless, S. Pillai, N. Lawrence, S. M. Sebti, and S. Chellappan. 2008. A small molecule disruptor of Rb/Raf-1 interaction inhibits cell proliferation, angiogenesis, and growth of human tumor xenografts in nude mice. Canc. Res. 68:3810-3818.
27. Kontou, M., L. Govindasamy, H. J. Nam, N. Bryant, A. L. Llamas-Saiz, C. Foces-Foces, E. Hernando, M. P. Rubio, R. McKenna, J. M. Almendral, and M. Agbandje-McKenna. 2005. Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice. J. Virol. 79:10931-10943.
28. Kosugi, S., M. Hasebe, N. Matsumura, H. Takashima, E. Miyamoto-Sato, M. Tomita, and H. Yanagawa. 2009. Six classes of nuclear localization signals specific to different binding grooves of importin α. J. Biol. Chem. 284:478-485.
29. Lange, A., R. E. Mills, S. E. Devine, and A. H. Corbett. 2008. A PY-NLS nuclear targeting signal is required for nuclear localization and function of the Saccharomyces cerevisiae mRNA-binding protein Hrp1. J. Biol. Chem. 283:12926-12934.
30. Larkin, J. M., S. Chowdhury, and M. E. Gore. 2007. Drug insight: advances in renal cell carcinoma and the role of targeted therapies. Nat. Clin. Pract. Oncol. 4:470-479.
31. Lee, B., A. E. Cansizoglu, K. E. Suel, T. H. Louis, Z. Zhang, and Y. M. Chook. 2006. Rules for nuclear localization sequence recognition by karyopherin β2. Cell 126:543-558.
32. Lee, S. J., T. Sekimoto, E. Yamashita, E. Nagoshi, A. Nakagawa, N. Imamoto, M. Yoshimura, H. Sakai, K. T. Chong, T. Tsukihara, and Y. Yoneda. 2003. The structure of importin-β bound to SREBP-2: nuclear import of a transcription factor. Science 302:1571-1575.
33. Leevers, S. J., H. F. Paterson, and C. J. Marshall. 1994. Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369:411-414.
34. Li, M., S. E. Delos, L. Montross, and R. L. Garcea. 1995. Polyomavirus VP1 phosphorylation: coexpression with the VP2 capsid protein modulates VP1 phosphorylation in Sf9 insect cells. Proc. Natl. Acad. Sci. U. S. A. 92:5992-5996.
35. Li, W., M. Melnick, and N. Perrimon. 1998. Dual function of Ras in Raf activation. Development 125:4999-5008.
36. Lombardo, E., J. C. Ramírez, J. García, and J. M. Almendral. 2002. Complementary roles of multiple nuclear targeting signals in the capsid proteins of the parvovirus minute virus of mice during assembly and onset of infection. J. Virol. 76:7049-7059.
37. Lombardo, E., J. C. Ramírez, M. Agbandje-Mckenna, and J. M. Almendral. 2000. A β-stranded motif drives capsid proteins oligomers of the parvovirus minute virus of mice into the nucleus for viral assembly. J. Virol. 74:3804-3814.
38. Lyustikman, Y., H. Momota, W. Pao, and E. C. Holland. 2008. Constitutive activation of Raf-1 induces glioma formation in mice. Neoplasia 10:501-510.
39. Madhunapantula, S. V., and G. P. Robertson. 2008. Is B-Raf a good therapeutic target for melanoma and other malignancies? Cancer Res. 68:5-8.
40. Mansour, S. J., W. T. Matten, A. S. Hermann, J. M. Candia, S. Rong, K. Fukasawa, G. F. Vande Woude, and N. G. Ahn. 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265:966-970.
41. Marais, R., and C. J. Marshall. 1996. Control of the ERK MAP kinase cascade by Ras and Raf. Cancer Surv. 27:101-125.
42. Maroto, B., J. C. Ramírez, and J. M. Almendral. 2000. Phosphorylation status of the parvovirus minute virus of mice particle: mapping and biological relevance of the major phosphorylation sites. J. Virol. 74:10892-10902.
43. Maroto, B., N. Valle, R. Saffrich, and J. M. Almendral. 2004. Nuclear export of the non-enveloped parvovirus virion is directed by an unordered protein signal exposed on the capsid surface. J. Virol. 78:10685-10694.
44. Mattaj, I. W., and L. Englmeier. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265-306.
45. McCubrey, J. A., L. S. Steelman, W. H. Chappell, S. L. Abrams, E. W. T. Wong, F. Chang, B. Lehmann, D. M. Terrian, M. Milella, A. Tafuri, F. Stivala, M. Libra, J. Basecke, C. Evangelisti, A. M. Martelli, and R. A. Franklin. 2007. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation, and drug resistance. Biochem. Biophys. Acta 1773:1263-1284.
46. Mogila, V., F. Xia, and W. X. Li. 2006. An intrinsic cell cycle checkpoint pathway mediated by MEK and ERK in Drosophila. Dev. Cell 11:575-582.
47. Mousset, S., and J. Rommelaere. 1982. Minute virus of mice inhibits cell transformation by simian virus 40. Nature 300:537-539.
48. Noble, C., K. Mercer, J. Hussain, L. Carragher, S. Giblett, R. Hayward, C. Patterson, R. Marais, and C. A. Pritchard. 2008. CRAF autophosphorylation of serine 621 is required to prevent its proteasome-mediated degradation. Mol. Cell 31:862-872.
49. Nuesch, J. P. F., and J. Rommelaere. 2007. A viral adaptor protein modulating casein kinase II activity induces cytopathic effects in permissive cells. Proc. Natl. Acad. Sci. U. S. A. 104:12482-12487.
50. Old, W. M., J. B. Shabb, S. Houel, H. Wang, K. L. Couts, C. Y. Yen, E. S. Litman, C. H. Croy, K. Meyer-Arendt, J. G. Miranda, R. A. Brown, E. S. Witze, R. E. Schweppe, K. A. Resing, and N. G. Ahn. 2009. Functional proteomics identifies targets of phosphorylation by B-Raf signalling in melanoma. Mol. Cell 34:115-131.
51. Parato, K. A., D. Senger, P. A. J. Forsyth, and J. C. Bell. 2005. Recent progress in the battle between oncolytic viruses and tumours. Nat. Rev. Cancer 5:965-976.
52. Pleschka, S., T. Wolff, C. Ehrhardt, G. Hobom, O. Planz, U. R. Rapp, and S. Ludwig. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell Biol. 3:301-305.
53. Pollard, V. W., W. M. Michael, S. Nakielny, M. C. Siomi, F. Wang, and G. Dreyfuss. 1996. A novel receptor-mediated nuclear protein import pathway. Cell 86:985-994.
54. Ponnazhagan, S. 2008. Adeno-associated virus, p. 55-68. In K. J. Harrington, R. G. Vile, and H. S. Pandha (ed.), Viral therapy of cancer. John Wiley & Sons, Ltd., West Sussex, United Kingdom.
55. Pratilas, C. A., B. S. Taylor, Q. Ye, A. Viale, C. Sander, D. B. Solit, and N. Rosen. 2009. v600EBRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc. Natl. Acad. Sci. U. S. A. 106:4519-4524.
56. Rabe, B., A. Vlachou, N. Pante, A. Helenius, and M. Kann. 2003. Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc. Natl. Acad. Sci. U. S. A. 100:9849-9854.
57. Raj, K., P. Ogston, and P. Beard. 2001. Virus-mediated killing of cells that lack p53 activity. Nature 412:914-918.
58. Raman, M., W. Chen, and M. H. Cobb. 2007. Differential regulation and properties of MAPKs. Oncogene 26:3100-3112.
59. Reguera, J., A. Carreira, L. Riolobos, J. M. Almendral, and M. G. Mateu. 2004. Role of interfacial amino acid residues in assembly, stability, and conformation of a spherical virus capsid. Proc. Natl. Acad. Sci. U. S. A. 101:2724-2729.
60. Rihs, H.-P., D. A. Jans, H. Fan, and R. Peters. 1991. The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen. EMBO J. 10:633-639.
61. Riolobos, L., J. Reguera, M. G. Mateu, and J. M. Almendral. 2006. Nuclear transport of trimeric assembly intermediates exerts a morphogenetic control on the icosahedral parvovirus capsid. J. Mol. Biol. 357:1026- 1038.
62. Robbins, J., S. M. Dilworth, R. A. Laskey, and C. Dingwall. 1991. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64:651-653.
63. Roberts, P. J., and C. J. Der. 2007. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26:3291-3310.
64. Rodriguez-Viciana, P., C. Collins, and M. Fried. 2006. Polyoma and SV40 proteins differentially regulate PP2A to activate distinct cellular signaling pathways involved in growth control. Proc. Natl. Acad. Sci. U. S. A. 103:19290-19295.
65. Rubio, M. P., S. Guerra, and J. M. Almendral. 2001. Genome replication and postencapsidation functions mapping to the nonstructural gene restrict the host range of a murine parvovirus in human cells. J. Virol. 75:11573-11582.
66. Salomé, N., B. van Hille, N. Duponchel, G. Meneguzzi, F. Cuzin, J. Rommelaere, and J. J. Cornelis. 1990. Sensitization of transformed rat cells to parvovirus MVMp is restricted to specific oncogenes. Oncogene 5:123-130.
67. Schubbert, S., K. Shannon, and G. Bollag. 2007. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 7:295-308.
68. Soga, S., T. Kozawa, H. Narumi, S. Akinaga, K. Matsumoto, K. Irie, S. V. Sharma, H. Nakano, T. Mizukami, and M. Harai. 1998. Radicicol leads to selective depletion of raf kinase and disrupts K-ras-activated aberrant signalling pathway. J. Biol. Chem. 273:822-828.
69. Spegelaere, P., B. van Hille, N. Spruyt, S. Faisst, J. J. Cornelis, and J. Rommelaere. 1991. Initiation of transcription from the minute virus of mice P4 promoter is stimulated in rat cells expressing a c-Ha-ras oncogene. J. Virol. 65:4919-4928.
70. Stewart, M. 2007. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell. Biol. 8:195-208.
71. Strong, J. E., G. Wong, S. E. Jones, A. Grolla, S. Theriault, G. P. Kobinger, and H. Feldmann. 2008. Stimulation of Ebola virus production from persistent infection through activation of the Ras/MAPK pathway. Proc. Natl. Acad. Sci. U. S. A. 105:17982-17987.
72. Tattersall, P., and J. Bratton. 1983. Reciprocal productive and restrictive virus-cell interaction of immunosuppressive and prototype strains of minute virus of mice. J. Virol. 46:944-955.
73. Telerman, A., M. Tuynder, T. Dupressoir, B. Robaye, F. Sigaux, E. Shaulian, M. Oren, J. Rommelaere, and R. Amson. 1993. A model of tumor suppression using H-1 parvovirus. Proc. Natl. Acad. Sci. U. S. A. 90:8702-8706.
74. Toolan, H., and N. Ledinko. 1965. Growth and cytopathogenicity of H-viruses in human and simian cell cultures. Nature 208:812-813.
75. Tran, E. J., and S. R. Wente. 2006. Dynamic nuclear pore complexes: life on the edge. Cell 125:1041-1053.
76. Tsao, J., M. S. Chapman, M. Agbandje, W. Séller, K. Smith, H. Wu, M. Luo, T. J. Smith, M. G. Rossmann, R. W. Compans, and C. R. Parrish. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456-1464.
77. Wan, P. T., M. J. Garnett, S. M. Roe, S. Lee, D. Niculescu-Duvaz, V. M. Good, C. M. Jones, C. J. Marshall, C. J. Springer, D. Barford, and R. Marais. 2004. Mechanism of activation of the RAF-ERK signalling pathway by oncogenic mutations of B-RAF. Cell 116:855-867.
78. Wellbrock, C., M. Karasarides, and R. Marais. 2004. The Raf proteins take centre stage. Nat. Rev. Mol. Cell. Biol. 5:875-885.
79. Williams, N. G., H. Paradis, S. Agarwal, D. L. Charest, S. L. Pelech, and T. M. Roberts. 1993. Raf-1 and p21v-ras cooperate in the activation of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. U. S. A. 90:5772-5779.
80. Williams, N. G., T. M. Roberts, and P. Li. 1992. Both p21ras and pp60v-src are required, but neither alone is sufficient, to activate the Raf-1 kinase. Proc. Natl. Acad. Sci. U. S. A. 89:2922-2926.
81. ras-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 93:11681-11686.
82. Yuan, W., and C. R. Parrish. 2001. Canine parvovirus capsid assembly and differences in mammalian and insect cells. Virology 279:546-557.
83. Zheng, Y., J. Li, D. L. Johnson, and J. H. Ou. 2003. Regulation of hepatitis B virus replication by the ras-mitogen-activated protein kinase signaling pathway. J. Virol. 77:7707-7712.