Expression of papillomavirus L1 proteins regulated by authentic gene codon usage is favoured in G2/M-like cells in differentiating keratinocytes

Virology

Volumn 399, Issue 1, 2010, Pages 46-58

  Ding, Jianmin ^a   Doorbar, John ^b   Li, Bo ^a   Zhou, Fang ^a   Gu, Wenyi ^a   Zhao, Liang ^a   Saunders, Nicholas A ^a   Frazer, Ian H ^a   Zhao, Kong Nan ^a,c,d  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Cell cycle; Gene codon usage; Keratinocyte; L1 protein; Papillomavirus

Indexed keywords

COLCHICINE; CYCLIN B1; CYCLIN D2; INVOLUCRIN; PROTEIN E4; PROTEIN L1; RETINOIC ACID; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIFFERENTIATION; CODON USAGE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENE FREQUENCY; IMMUNOFLUORESCENCE MICROSCOPY; KERATINOCYTE; MOUSE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS REPLICATION;

ANIMALS; CAPSID PROTEINS; CELL CYCLE; CELL DIFFERENTIATION; CELLS, CULTURED; CODON; COLCHICINE; CYCLIN B1; CYCLIN D2; G2 PHASE; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; KERATINOCYTES; MICE; MITOSIS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PROTEIN PRECURSORS; TUBULIN MODULATORS;

PAPILLOMAVIRIDAE;

EID: 77049121449     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.12.021     Document Type: Article

References (65)

1. Aho S., Buisson M., Pajunen T., Ryoo Y.W., Giot J.F., Gruffat H., Sergeant A., and Uitto J. Ubinuclein, a novel nuclear protein interacting with cellular and viral transcription factors. J. Cell Biol. 148 6 (2000) 1165-1176
2. Antúnez de Mayolo A., L. M., Erdeniz N., Thybo T., Mortensen U.H., and Rothstein R. Multiple start codons and phosphorylation result in discrete Rad52 protein species. Nucleic Acids Res. 34 9 (2006) 2587-2597
3. Balazs I., and Caldarella J. Retrovirus gene expression during the cell cycle. I. Virus production, synthesis, and expression of viral proteins in Rauscher murine leukemia virus-infected mouse cells. J. Virol. 39 3 (1981) 792-799
4. Bennetzen J.L., and Hall B.D. Codon selection in yeast. J. Biol. Chem. 257 6 (1982) 3026-3031
5. Blain S.W. Switching cyclin D-Cdk4 kinase activity on and off. Cell Cycle 7 7 (2008) 892-898
6. Chaturvedi V., Bacon P., Bodner B., and Nickoloff B.J. Proliferating cultured human keratinocytes are more susceptible to apoptosis compared with mouse keratinocytes. J. Invest. Dermatol. 123 6 (2004) 1200-1203
7. Chen H.H., and Fluck M.M. Cell cycle control of polyomavirus-induced transformation. J. Virol. 67 4 (1993) 1996-2005
8. Chow L.T., Duffy A.A., Wang H.K., and Broker T.R. A highly efficient system to produce infectious human papillomavirus: elucidation of natural virus-host interactions. Cell Cycle 8 9 (2009) 1319-1323
9. Danilenko M., Wang X., and Studzinski G.P. Carnosic acid and promotion of monocytic differentiation of HL60-G cells initiated by other agents. J. Natl. Cancer Inst. 93 16 (2001) 1224-1233
10. Davy C., and Doorbar J. G2/M cell cycle arrest in the life cycle of viruses. Virology 368 2 (2007) 219-226
11. Davy C.E., Jackson D.J., Wang Q., Raj K., Masterson P.J., Fenner N.F., Southern S., Cuthill S., Millar J.B., and Doorbar J. Identification of a G(2) arrest domain in the E1 wedge E4 protein of human papillomavirus type 16. J. Virol. 76 19 (2002) 9806-9818
12. Davy C.E., Jackson D.J., Raj K., Peh W.L., Southern S.A., Das P., Sorathia R., Laskey P., Middleton K., Nakahara T., Wang Q., Masterson P.J., Lambert P.F., Cuthill S., Millar J.B., and Doorbar J. Human papillomavirus type 16 E1 E4-induced G2 arrest is associated with cytoplasmic retention of active Cdk1/cyclin B1 complexes. J. Virol. 79 7 (2005) 3998-4011
13. Devgan V., Nguyen B.C., Oh H., and Dotto G.P. p21WAF1/Cip1 suppresses keratinocyte differentiation independently of the cell cycle through transcriptional up-regulation of the IGF-I gene. J. Biol. Chem. 281 41 (2006) 30463-30470
14. Di Marzio P., Choe S., Ebright M., Knoblauch R., and Landau N.R. Mutational analysis of cell cycle arrest, nuclear localization and virion packaging of human immunodeficiency virus type 1 Vpr. J. Virol. 69 12 (1995) 7909-7916
15. Doorbar J. The papillomavirus life cycle. J. Clin. Virol. 32 Suppl. 1 (2005) S7-S15
16. Dunnwald M., Zuberi A.R., Stephens K., Le R., Sundberg J.P., Fleckman P., and Dale B.A. The ichq mutant mouse, a model for the human skin disorder harlequin ichthyosis: mapping, keratinocyte culture, and consideration of candidate genes involved in epidermal growth regulation. Exp. Dermatol. 12 3 (2003) 245-254
17. Fang N.X., Gu W., Ding J., Saunders N.A., Frazer I.H., and Zhao K.N. Calcium enhances mouse keratinocyte differentiation in vitro to differentially regulate expression of papillomavirus authentic and codon modified L1 genes. Virology 365 1 (2007) 187-197
18. Felton-Edkins Z.A., Kenneth N.S., Brown T.R., Daly N.L., Gomez-Roman N., Grandori C., Eisenman R.N., and White R.J. Direct regulation of RNA polymerase III transcription by RB, p53 and c-Myc. Cell Cycle 2 3 (2003) 181-184
19. Goh W.C., Rogel M.E., Kinsey C.M., Michael S.F., Fultz P.N., Nowak M.A., Hahn B.H., and Emerman M. HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo. Nat. Med. 4 1 (1998) 65-71
20. Gouy M., and Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 10 22 (1982) 7055-7074
21. Gu W., Li M., Zhao W.M., Fang N.X., Bu S., Frazer I.H., and Zhao K.N. tRNASer(CGA) differentially regulates expression of wild-type and codon-modified papillomavirus L1 genes. Nucleic Acids Res. 32 15 (2004) 4448-4461
22. Gu W., Ding J., Wang X., de Kluyver R.L., Saunders N.A., Frazer I.H., and Zhao K.N. Generalized substitution of isoencoding codons shortens the duration of papillomavirus L1 protein expression in transiently gene-transfected keratinocytes due to cell differentiation. Nucleic Acids Res. 35 14 (2007) 4820-4832
23. Guccione E., Pim D., and Banks L. HPV-18 E6*I modulates HPV-18 full-length E6 functions in a cell cycle dependent manner. Int. J. Cancer 110 6 (2004) 928-933
24. Hager B., Bickenbach J.R., and Fleckman P. Long-term culture of murine epidermal keratinocytes. J. Invest. Dermatol. 112 6 (1999) 971-976
25. Hashida T., and Yasumoto S. Induction of chromosome abnormalities in mouse and human epidermal keratinocytes by the human papillomavirus type 16 E7 oncogene. J. Gen. Virol. 72 Pt 7 (1991) 1569-1577
26. Haugwitz U., Wasner M., Wiedmann M., Spiesbach K., Rother K., Mossner J., and Engeland K. A single cell cycle genes homology region (CHR) controls cell cycle-dependent transcription of the cdc25C phosphatase gene and is able to cooperate with E2F or Sp1/3 sites. Nucleic Acids Res. 30 9 (2002) 1967-1976
27. He J., Choe S., Walker R., Di Marzio P., Morgan D.O., and Landau N.R. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69 11 (1995) 6705-6711
28. Heinrich M.C., Silvey K.V., Stone S., Zigler A.J., Griffith D.J., Montalto M., Chai L., Zhi Y., and Hoatlin M.E. Posttranscriptional cell cycle-dependent regulation of human FANCC expression. Blood 95 12 (2000) 3970-3977
29. Imaki H., Nakayama K., Delehouzee S., Handa H., Kitagawa M., Kamura T., and Nakayama K.I. Cell cycle-dependent regulation of the Skp2 promoter by GA-binding protein. Cancer Res. 63 15 (2003) 4607-4613
30. Kashanchi F., Agbottah E.T., Pise-Masison C.A., Mahieux R., Duvall J., Kumar A., and Brady J.N. Cell cycle-regulated transcription by the human immunodeficiency virus type 1 Tat transactivator. J. Virol. 74 2 (2000) 652-660
31. Kim J.H., Polish J., and Johnston M. Specificity and regulation of DNA binding by the yeast glucose transporter gene repressor Rgt1. Mol. Cell. Biol. 23 15 (2003) 5208-5216
32. Kuo H.C., Kuo W.H., Lee Y.J., Wang C.J., and Tseng T.H. Enhancement of caffeic acid phenethyl ester on all-trans retinoic acid-induced differentiation in human leukemia HL-60 cells. Toxicol. Appl. Pharmacol. 216 1 (2006) 80-88
33. Lake R.J., and Jelinek W.R. Cell cycle- and terminal differentiation-associated regulation of the mouse mRNA encoding a conserved mitotic protein kinase. Mol. Cell. Biol. 13 12 (1993) 7793-7801
34. Leask A., Rosenberg M., Vassar R., and Fuchs E. Regulation of a human epidermal keratin gene: sequences and nuclear factors involved in keratinocyte-specific transcription. Genes Dev. 4 11 (1990) 1985-1998
35. Lindqvist A., Rodriguez-Bravo V., and Medema R.H. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J. Cell. Biol. 185 2 (2009) 193-202
36. Macurek L., Lindqvist A., and Medema R.H. Aurora-A and hBora join the game of Polo. Cancer Res. 69 11 (2009) 4555-4558
37. Mannik J., Alzayady K., and Ghazizadeh S. Regeneration of multilineage skin epithelia by differentiated keratinocytes. J. Invest. Dermatol. (2009) doi:10.1038/jid.2009.244
38. Marcelo C.L., Kim Y.G., Kaine J.L., and Voorhees J.J. Stratification, specialization, and proliferation of primary keratinocyte cultures. Evidence of a functioning in vitro epidermal cell system. J. Cell Biol. 79 2 Pt 1 (1978) 356-370
39. Maruvada P., Dmitrieva N.I., East-Palmer J., and Yen P.M. Cell cycle-dependent expression of thyroid hormone receptor-beta is a mechanism for variable hormone sensitivity. Mol. Biol. Cell 15 4 (2004) 1895-1903
40. McIntosh P.B., Martin S.R., Jackson D.J., Khan J., Isaacson E.R., Calder L., Raj K., Griffin H.M., Wang Q., Laskey P., Eccleston J.F., and Doorbar J. Structural analysis reveals an amyloid form of the human papillomavirus type 16 E1-E4 protein and provides a molecular basis for its accumulation. J. Virol. 82 16 (2008) 8196-8203
41. Millard S.S., Vidal A., Markus M., and Koff A. A U-rich element in the 5′ untranslated region is necessary for the translation of p27 mRNA. Mol. Cell. Biol. 20 16 (2000) 5947-5959
42. Miura K., Koide N., Himeno S., Nakagawa I., and Imura N. The involvement of microtubular disruption in methylmercury-induced apoptosis in neuronal and nonneuronal cell lines. Toxicol. Appl. Pharmacol. 160 3 (1999) 279-288
43. Moon R.C., Mehta R.G., and Detrisac C.J. Retinoids as chemopreventive agents for breast cancer. Cancer Detect. Prev. 16 1 (1992) 73-79
44. Park F., Ohashi K., Chiu W., Naldini L., and Kay M.A. Efficient lentiviral transduction of liver requires cell cycling in vivo. Nat. Genet. 24 1 (2000) 49-52
45. Peh W.L., Middleton K., Christensen N., Nicholls P., Egawa K., Sotlar K., Brandsma J., Percival A., Lewis J., Liu W.J., and Doorbar J. Life cycle heterogeneity in animal models of human papillomavirus-associated disease. J. Virol. 76 20 (2002) 10401-10416
46. Peh W.L., Brandsma J.L., Christensen N.D., Cladel N.M., Wu X., and Doorbar J. The viral E4 protein is required for the completion of the cottontail rabbit papillomavirus productive cycle in vivo. J. Virol. 78 4 (2004) 2142-2151
47. Plotkin J.B., Robins H., and Levine A.J. Tissue-specific codon usage and the expression of human genes. Proc. Natl. Acad. Sci. U. S. A. 101 34 (2004) 12588-12591
48. Ray P.S., Grover R., and Das S. Two internal ribosome entry sites mediate the translation of p53 isoforms. EMBO Rep. 7 4 (2006) 404-410
49. Roberts B.D., Fang G., and Butera S.T. Influence of cell cycle on HIV-1 expression differs among various models of chronic infection. Arch. Virol. 142 6 (1997) 1087-1099
50. Saunders N., Dicker A., Popa C., Jones S., and Dahler A. Histone deacetylase inhibitors as potential anti-skin cancer agents. Cancer Res. 59 2 (1999) 399-404
51. Simon M., and Green H. Enzymatic cross-linking of involucrin and other proteins by keratinocyte particulates in vitro. Cell 40 3 (1985) 677-683
52. Southern S.A., McDicken I.W., and Herrington C.S. Loss of cytokeratin 14 expression is related to human papillomavirus type and lesion grade in squamous intraepithelial lesions of the cervix. Hum. Pathol. 32 12 (2001) 1351-1355
53. Stoler M.H., and Ratliff N.B. Potential and problems of the in situ molecular detection of viral genomes. Am. J. Clin. Pathol. 93 5 (1990) 714-716
54. Stoldt V.R., Schnorr O., Schulze-Osthoff K., and Scharf R.E. Transforming growth factor-beta1 enhances the antifibrinolytic and prothrombotic state of growing endothelial cells in a cell cycle-specific manner. FASEB J. 20 7 (2006) 965-966
55. Sutton R.E., Reitsma M.J., Uchida N., and Brown P.O. Transduction of human progenitor hematopoietic stem cells by human immunodeficiency virus type 1-based vectors is cell cycle dependent. J. Virol. 73 5 (1999) 3649-3660
56. Syrjanen S.M., and Syrjanen K.J. New concepts on the role of human papillomavirus in cell cycle regulation. Ann. Med. 31 3 (1999) 175-187
57. Tan N.S., Michalik L., Noy N., Yasmin R., Pacot C., Heim M., Fluhmann B., Desvergne B., and Wahli W. Critical roles of PPAR beta/delta in keratinocyte response to inflammation. Genes Dev. 15 24 (2001) 3263-3277
58. Tobiume M., Fujinaga K., Kameoka M., Kimura T., Nakaya T., Yamada T., and Ikuta K. Dependence on host cell cycle for activation of human immunodeficiency virus type 1 gene expression from latency. J. Gen. Virol. 79 Pt 6 (1998) 1363-1371
59. Wang H.K., Duffy A.A., Broker T.R., and Chow L.T. Robust production and passaging of infectious HPV in squamous epithelium of primary human keratinocytes. Genes Dev. 23 2 (2009) 181-194
60. Wang Q., Kennedy A., Das P., McIntosh P.B., Howell S.A., Isaacson E.R., Hinz S.A., Davy C., and Doorbar J. Phosphorylation of the human papillomavirus type 16 E1-E4 protein at T57 by ERK triggers a structural change that enhances keratin binding and protein stability. J. Virol. 83 8 (2009) 3668-3683
61. Wasner M., Tschop K., Spiesbach K., Haugwitz U., Johne C., Mossner J., Mantovani R., and Engeland K. Cyclin B1 transcription is enhanced by the p300 coactivator and regulated during the cell cycle by a CHR-dependent repression mechanism. FEBS Lett. 536 1-3 (2003) 66-70
62. White A.E., Livanos E.M., and Tlsty T.D. Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev. 8 6 (1994) 666-677
63. White R.J., Trouche D., Martin K., Jackson S.P., and Kouzarides T. Repression of RNA polymerase III transcription by the retinoblastoma protein. Nature 382 6586 (1996) 88-90
64. Zeltner R., Borenstein L.A., Wettstein F.O., and Iftner T. Changes in RNA expression pattern during the malignant progression of cottontail rabbit papillomavirus-induced tumors in rabbits. J. Virol. 68 6 (1994) 3620-3630
65. Zhao K.N., Gu W., Fang N.X., Saunders N.A., and Frazer I.H. Gene codon composition determines differentiation-dependent expression of a viral capsid gene in keratinocytes in vitro and in vivo. Mol. Cell. Biol. 25 19 (2005) 8643-8655