Cutaneous human papillomavirus type 38 E7 regulates actin cytoskeleton structure for increasing cell proliferation through CK2 and the eukaryotic elongation factor 1A

Journal of Virology

Volumn 85, Issue 17, 2011, Pages 8477-8494

  Yue, Jiping ^a   Shukla, Ruchi ^a,d   Accardi, Rosita ^a   Zanella Cleon, Isabelle ^b   Siouda, Maha ^a   Cros, Marie Pierre ^a   Krutovskikh, Vladimir ^a   Hussain, Ishraq ^a,e   Niu, Yamei ^a,f   Hu, Shiqiong ^c   Becchi, Michel ^b   Jurdic, Pierre ^c   Tommasino, Massimo ^a   Sylla, Bakary S ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^c UNIVERSITÉ LYON 1   (France)

^d INSERM   (France)

^e SHER E KASHMIR UNIVERSITY OF AGRICULTURAL SCIENCES AND TECHNOLOGY OF KASHMIR   (India)

^f Chinese Academy of Sciences and China National Center for Bioinformation   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; ELONGATION FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN E7; RHO FACTOR;

ACTIN FILAMENT; ARTICLE; CELL DISRUPTION; CELL GROWTH; CELL IMMORTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATIONAL STUDY; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 38; IMMUNOFLUORESCENCE TEST; KERATINOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STRESS FIBER; TRANSCRIPTION REGULATION; WART VIRUS;

ACTINS; CASEIN KINASE II; CELL LINE; CELL PROLIFERATION; CYTOSKELETON; EUKARYOTIC INITIATION FACTOR-1; HUMANS; KERATINOCYTES; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PROTEIN BINDING;

EUKARYOTA; HUMAN PAPILLOMAVIRUS TYPE 38; MUS MUSCULUS;

EID: 80052293913     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02561-10     Document Type: Article

References (66)

1. Accardi, R., et al. 2006. Skin human papillomavirus type 38 alters p53 functions by accumulation of deltaNp73. EMBO Rep. 7:334-340.
2. Alunni-Fabbroni, M., et al. 2000. Induction of S phase and apoptosis by the human papillomavirus type 16 E7 protein are separable events in immortalized rodent fibroblasts. Oncogene 19:2277-2285.
3. Amano, M., et al. 1997. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275:1308-1311.
4. Amiri, A., et al. 2007. eEF1A2 activates Akt and stimulates Akt-dependent actin remodeling, invasion and migration. Oncogene 26:3027-3040.
5. Barbosa, M. S., et al. 1990. The region of the HPV E7 oncoprotein homologous to adenovirus E1a and Sv40 large T antigen contains separate domains for Rb binding and casein kinase II phosphorylation. EMBO J. 9:153-160.
6. Bishop, A. L., and A. Hall. 2000. Rho GTPases and their effector proteins. Biochem. J. 348(Pt. 2):241-255.
7. Bouvard, V., A. S. Gabet, R. Accardi, B. S. Sylla, and M. Tommasino. 2006. The cutaneous human papillomavirus types and non-melanoma skin cancer, p. 269-277. In S. Campo (ed.), Papillomavirus research: from natural history to vaccines and beyond. Caister Academic Press, Hethersett, Norwich, United Kingdom.
8. Cain, R. J., and A. J. Ridley. 2009. Phosphoinositide 3-kinases in cell migration. Biol. Cell 101:13-29.
9. Caldeira, S., et al. 2003. The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J. Virol. 77:2195-2206.
10. Chapman, S., X. Liu, C. Meyers, R. Schlegel, and A. A. McBride. 2010. Human keratinocytes are efficiently immortalized by a Rho kinase inhibitor. J. Clin. Invest. 120:2619-2626.
11. Charette, S. T., and D. J. McCance. 2007. The E7 protein from human papillomavirus type 16 enhances keratinocyte migration in an Akt-dependent manner. Oncogene 26:7386-7390.
12. Chien, W. M., J. N. Parker, D. C. Schmidt-Grimminger, T. R. Broker, and L. T. Chow. 2000. Casein kinase II phosphorylation of the human papillomavirus-18 E7 protein is critical for promoting S-phase entry. Cell Growth Differ. 11:425-435.
13. Cimarelli, A., and J. Luban. 1999. Translation elongation factor 1-alpha interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 73:5388-5401.
14. Clegg, R. M. 1992. Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211:353-388.
15. Dong, W., et al. 2005. Skin hyperproliferation and susceptibility to chemical carcinogenesis in transgenic mice expressing E6 and E7 of human papillomavirus type 38. J. Virol. 79:14899-14908.
16. Ejiri, S. 2002. Moonlighting functions of polypeptide elongation factor 1: from actin bundling to zinc finger protein R1-associated nuclear localization. Biosci. Biotechnol. Biochem. 66:1-21.
17. Firzlaff, J. M., B. Luscher, and R. N. Eisenman. 1991. Negative charge at the casein kinase II phosphorylation site is important for transformation but not for Rb protein binding by the E7 protein of human papillomavirus type 16. Proc. Natl. Acad. Sci. U. S. A. 88:5187-5191.
18. Gallagher, S. R. 2006. One-dimensional SDS gel electrophoresis of proteins, unit 10 2A, p. 1-37. In F. M. Ausubel et al. (ed.), Current protocols in molecular biology. Wiley Interscience, New York, NY.
19. Genovese, N. J., N. S. Banerjee, T. R. Broker, and L. T. Chow. 2008. Casein kinase II motif-dependent phosphorylation of human papillomavirus E7 protein promotes p130 degradation and S-phase induction in differentiated human keratinocytes. J. Virol. 82:4862-4873.
20. Ghittoni, R., et al. 2010. The biological properties of E6 and E7 oncoproteins from human papillomaviruses. Virus Genes 40:1-13.
21. Grammatikakis, N., et al. 2001. Simian virus 40 large tumor antigen modulates the Raf signaling pathway. J. Biol. Chem. 276:27840-27845.
22. Gross, S. R., and T. G. Kinzy. 2005. Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol. 12:772-778.
23. Gyenis, L., and D. W. Litchfield. 2008. The emerging CK2 interactome: insights into the regulation and functions of CK2. Mol. Cell. Biochem. 316:5-14.
24. Hall, A. 2005. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33:891-895.
25. Howley, P. M., and D. R. Lowy. 2007. Polyomaviruses, p. 229-2354. In D. M. Knipe et al. (ed.), Fields virology, 5th ed. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, PA.
26. Iyer, S. S., and D. J. Kusner. 2009. Coordinate regulation of sphingosine kinase and actin dynamics. Methods Mol. Biol. 531:347-361.
27. Jewers, R. J., P. Hildebrandt, J. W. Ludlow, B. Kell, and D. J. McCance. 1992. Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. J. Virol. 66:1329-1335.
28. Johnson, H. W., and M. J. Schell. 2009. Neuronal IP3 3-kinase is an F-actinbundling protein: role in dendritic targeting and regulation of spine morphology. Mol. Biol. Cell 20:5166-5180.
29. Kahns, S., et al. 1998. The elongation factor 1 A-2 isoform from rabbit: cloning of the cDNA and characterization of the protein. Nucleic Acids Res. 26:1884-1890.
30. Khacho, M., et al. 2008. eEF1A is a novel component of the mammalian nuclear protein export machinery. Mol. Biol. Cell 19:5296-5308.
31. Klein, R. M., L. S. Spofford, E. V. Abel, A. Ortiz, and A. E. Aplin. 2008. B-RAF regulation of Rnd3 participates in actin cytoskeletal and focal adhesion organization. Mol. Biol. Cell 19:498-508.
32. Knudsen, S. M., J. Frydenberg, B. F. Clark, and H. Leffers. 1993. Tissuedependent variation in the expression of elongation factor-1 alpha isoforms: isolation and characterisation of a cDNA encoding a novel variant of human elongation-factor 1 alpha. Eur. J. Biochem. 215:549-554.
33. Leclercq, T. M., P. A. Moretti, M. A. Vadas, and S. M. Pitson. 2008. Eukaryotic elongation factor 1A interacts with sphingosine kinase and directly enhances its catalytic activity. J. Biol. Chem. 283:9606-9614.
34. Lee, J. M. 2003. The role of protein elongation factor eEF1A2 in ovarian cancer. Reprod. Biol. Endocrinol. 1:69.
35. Lee, S., et al. 2004. Frameshift mutation in the Dok1 gene in chronic lymphocytic leukemia. Oncogene 23:2287-2297.
36. Liu, G., et al. 1996. F-actin sequesters elongation factor 1alpha from interaction with aminoacyl-tRNA in a pH-dependent reaction. J. Cell Biol. 135:953-963.
37. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
38. Mantovani, F., and L. Banks. 2001. The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20:7874-7887.
39. McLaughlin-Drubin, M. E., and K. Munger. 2009. The human papillomavirus E7 oncoprotein. Virology 384:335-344.
40. Meggio, F., and L. A. Pinna. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17:349-368.
41. Moody, C. A., and L. A. Laimins. 2010. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 10:550-560.
42. Morita, K., F. Bunai, and O. Numata. 2008. Roles of three domains of Tetrahymena eEF1A in bundling F-actin. Zoolog. Sci. 25:22-29.
43. Naumanen, P., P. Lappalainen, and P. Hotulainen. 2008. Mechanisms of actin stress fibre assembly. J. Microsc. 231:446-454.
44. Nieminen, J., A. Kuno, J. Hirabayashi, and S. Sato. 2007. Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer. J. Biol. Chem. 282:1374-1383.
45. Nissen, P., et al. 1995. Crystal structure of the ternary complex of PhetRNAPhe, EF-Tu, and a GTP analog. Science 270:1464-1472.
46. Niu, Y., et al. 2006. A nuclear export signal and phosphorylation regulate Dok1 subcellular localization and functions. Mol. Cell. Biol. 26:4288-4301.
47. Papakonstanti, E. A., and C. Stournaras. 2007. Actin cytoskeleton architecture and signaling in osmosensing. Methods Enzymol. 428:227-240.
48. Pawlak, G., and D. M. Helfman. 2001. Cytoskeletal changes in cell transformation and tumorigenesis. Curr. Opin. Genet. Dev. 11:41-47.
49. Pawlak, G., and D. M. Helfman. 2002. MEK mediates v-Src-induced disruption of the actin cytoskeleton via inactivation of the Rho-ROCK-LIM kinase pathway. J. Biol. Chem. 277:26927-26933.
50. Pawlak, G., and D. M. Helfman. 2002. Post-transcriptional down-regulation of ROCKI/Rho-kinase through an MEK-dependent pathway leads to cytoskeleton disruption in Ras-transformed fibroblasts. Mol. Biol. Cell 13:336-347.
51. Pfister, H. 2003. Human papillomavirus and skin cancer. J. Natl. Cancer Inst. Monogr. 2003:52-56.
52. Pittman, Y. R., K. Kandl, M. Lewis, L. Valente, and T. G. Kinzy. 2009. Coordination of eukaryotic translation elongation factor 1A (eEF1A) function in actin organization and translation elongation by the guanine nucleotide exchange factor eEF1Balpha. J. Biol. Chem. 284:4739-4747.
53. Pleschka, S. 2008. RNA viruses and the mitogenic Raf/MEK/ERK signal transduction cascade. Biol. Chem. 389:1273-1282.
54. Pollard, T. D., and J. A. Cooper. 2009. Actin, a central player in cell shape and movement. Science 326:1208-1212.
55. Rao, J., and N. Li. 2004. Microfilament actin remodeling as a potential target for cancer drug development. Curr. Cancer Drug Targets 4:345-354.
56. Riedl, J., et al. 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5:605-607.
57. Riis, B., S. I. Rattan, B. F. Clark, and W. C. Merrick. 1990. Eukaryotic protein elongation factors. Trends Biochem. Sci. 15:420-424.
58. Ritt, D. A., et al. 2007. CK2 is a component of the KSR1 scaffold complex that contributes to Raf kinase activation. Curr. Biol. 17:179-184.
59. Soares, D. C., P. N. Barlow, H. J. Newbery, D. J. Porteous, and C. M. Abbott. 2009. Structural models of human eEF1A1 and eEF1A2 reveal two distinct surface clusters of sequence variation and potential differences in phosphorylation. PLoS One 4:e6315.
60. Stark, H., et al. 1997. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389:403-406.
61. Sylla, B. S., et al. 2000. The X-linked lymphoproliferative syndrome gene product SH2D1A associates with p62dok (Dok1) and activates NF-kappa B. Proc. Natl. Acad. Sci. U. S. A. 97:7470-7475.
62. Vasiliev, J. M. 2004. Cytoskeletal mechanisms responsible for invasive migration of neoplastic cells. Int. J. Dev. Biol. 48:425-439.
63. Wang, Y., Y. Jiang, M. Meyering-Voss, M. Sprinzl, and P. B. Sigler. 1997. Crystal structure of the EF-Tu.EF-Ts complex from Thermus thermophilus. Nat. Struct. Biol. 4:650-656.
64. Watanabe, N., T. Kato, A. Fujita, T. Ishizaki, and S. Narumiya. 1999. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat. Cell Biol. 1:136-143.
65. Yamaji, Y., et al. 2006. In vivo interaction between Tobacco mosaic virus RNA-dependent RNA polymerase and host translation elongation factor 1A. Virology 347:100-108.
66. Yuan, H., et al. 2009. Human papillomavirus type 16 oncoprotein E7 suppresses cadherin-mediated cell adhesion via ERK and AP-1 signaling. Int. J. Oncol. 35:309-314.