Gene codon composition determines differentiation-dependent expression of a viral capsid gene in keratinocytes in vitro and in vivo

Molecular and Cellular Biology

Volumn 25, Issue 19, 2005, Pages 8643-8655

  Zhao, Kong Nan ^a   Gu, WenYi ^a   Fang, Ning Xia ^a   Saunders, Nicholas A ^a   Frazer, Ian H ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CYTOKERATIN 14; INVOLUCRIN; MESSENGER RNA; STRUCTURAL PROTEIN; VIRUS PROTEIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CODON; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; KERATINOCYTE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID;

ANIMALS; BIOLISTICS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CAPSID; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CODON; DACTINOMYCIN; DNA; GENE EXPRESSION REGULATION, VIRAL; KERATIN-14; KERATINOCYTES; KERATINS; MICE; MICE, INBRED BALB C; MICROSCOPY, FLUORESCENCE; NUCLEIC ACID HYBRIDIZATION; PAPILLOMAVIRIDAE; PLASMIDS; PROTEIN BIOSYNTHESIS; PROTEIN PRECURSORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER; RNA, TRANSFER; TIME FACTORS; TRANSFECTION; VIRUSES;

MIRIDAE; PAPILLOMAVIRUS;

EID: 25444502301     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.19.8643-8655.2005     Document Type: Article

References (70)

1. Aho, S., M. Buisson, T. Pajunen, Y. W. Ryoo, J. F. Giot, H. Gruffat, A. Sergeant, and J. Uitto. 2000. Ubinuclein, a novel nuclear protein interacting with cellular and viral transcription factors. J. Cell Biol. 148:1165-1176.
2. Barksdale, S. K., and C. C. Baker. 1993. Differentiation-specific expression from the bovine papillomavirus type 1 P2443 and late promoters. J. Virol. 67:5605-5616.
3. Bennetzen, J. L., and B. D. Hall. 1982. Codon selection in yeast. J. Biol. Chem. 257:3026-3031.
4. Bowden, P. E., C. D. Woodworth, J. Doniger, and J. A. DiPaolo. 1992. Down-regulation of keratin 14 gene expression after v-Ha-ras transfection of human papillomavirus-immortalized human cervical epithelial cells. Cancer Res. 52:5865-5871.
5. Brown, D. R., L. Fan, J. Jones, and J. Bryan. 1994. Colocalization of human papillomavirus type 11 E1E4 and L1 proteins in human foreskin implants grown in athymic mice. Virology 201:46-54.
6. Calkhoven, C. F., C. Muller, and A. Leutz. 2002. Translational control of gene expression and disease. Trends Mol. Med. 8:577-583.
7. Carlini, D. B., Y. Chen, and W. Stephan. 2001. The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes Adh and Adhr. Genetics 159:623-633.
8. Chiba, Y., M. Ishikawa, F. Kijima, R. H. Tyson, J. Kim, A. Yamamoto, E. Nambara, T. Leustek, R. M. Wallsgrove, and S. Naito. 1999. Evidence for autoregulation of cystathionine gamma-synthase mRNA stability in Arabidopsis. Science 286:1371-1374.
9. Cid-Arregui, A., V. Juarez, and H. zur Hausen. 2003. A synthetic E7 gene of human papillomavirus type 16 that yields enhanced expression of the protein in mammalian cells and is useful for DNA immunization studies. J. Virol. 77:4928-4937.
10. Collier, B., L. Goobar-Larsson, M. Sokolowski, and S. Schwartz. 1998. Translational inhibition in vitro of human papillomavirus type 16 L2 mRNA mediated through interaction with heterogenous ribonucleoprotein K and poly(rC)-binding proteins 1 and 2. J. Biol. Chem. 273:22648-22656.
11. Collier, B., D. Oberg, X. Zhao, and S. Schwartz. 2002. Specific inactivation of inhibitory sequences in the 5′ end of the human papillomavirus type 16 L1 open reading frame results in production of high levels of L1 protein in human epithelial cells. J. Virol. 76:2739-2752.
12. Dibbens, J. A., D. L. Miller, A. Damert, W. Risau, M. A. Vadas, and G. J. Goodall. 1999. Hypoxic regulation of vascular endothelial growth factor mRNA stability requires the cooperation of multiple RNA elements. Mol. Biol. Cell 10:907-919.
13. Dover, R., and F. M. Watt. 1987. Measurement of the rate of epidermal terminal differentiation: expression of involucrin by S-phase keratinocytes in culture and in psoriatic plaques. J. Investig. Dermatol. 89:349-352.
14. Duan, J., and M. A. Antezana. 2003. Mammalian mutation pressure, synonymous codon choice, and mRNA degradation. J. Mol. Evol. 57:694-701.
15. Duret, L. 2000. tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet. 16:287-289.
16. Eckert, R. L., and J. F. Welter. 1996. Transcription factor regulation of epidermal keratinocyte gene expression. Mol. Biol. Rep. 23:59-70.
17. Eckert, R. L., J. F. Crish, E. B. Banks, and J. F. Welter. 1997. The epidermis: genes on-genes off. J. Investig. Dermatol. 109:501-509.
18. Elf, J., D. Nilsson, T. Tenson, and M. Ehrenberg. 2003. Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 300:1718-1722.
19. Faus, I., H. J. Hsu, and E. Fuchs. 1994. Oct-6: a regulator of keratinocyte gene expression in stratified squamous epithelia. Mol. Cell. Biol. 14:3263-3275.
20. Frattini, M. G., H. B. Lim, and L. A. Laimins. 1996. In vitro synthesis of oncogenic human papillomaviruses requires episomal genomes for differentiation-dependent late expression. Proc. Natl. Acad. Sci. USA 93:3062-3067.
21. Frattini, M. G., H. B. Lim, J. Doorbar, and L. A. Laimins. 1997. Induction of human papillomavirus type 18 late gene expression and genomic amplification in organotypic cultures from transfected DNA templates. J. Virol. 71:7068-7072.
22. Furth, P. A., and C. C. Baker. 1991. An element in the bovine papillomavirus late 3′ untranslated region reduces polyadenylated cytoplasmic RNA levels. J. Virol. 65:5806-5812.
23. Gouy, M., and C. Gautier. 1982. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 10:7055-7074.
24. Gu, W., M. Li, W. M. Zhao, N. X. Fang, S. Bu, I. H. Frazer, and K. N. Zhao. 2004. tRNASer(CGA) differentially regulates expression of wild-type and codon-modified papillomavirus L1 genes. Nucleic Acids Res. 32:4448-4461.
25. Haas, J., E. C. Park, and B. Seed. 1996. Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr. Biol. 6:315-324.
26. Heim, R., A. B. Cubitt, and R. Y. Tsien. 1995. Improved green fluorescence. Nature 373:663-664.
27. Hopper, A. K., and E. M. Phizicky. 2003. tRNA transfers to the limelight. Genes Dev. 17:162-180.
28. Ibba, M., H. D. Becker, C. Stathopoulos, D. L. Tumbula, and D. Soll. 2000. The adaptor hypothesis revisited. Trends Biochem. Sci. 25:311-316.
29. Janzen, D. M., and A. P. Geballe. 2004. The effect of eukaryotic release factor depletion on translation termination in human cell lines. Nucleic Acids Res. 32:4491-4502.
30. Jimenez-Garcia, L. F., and D. L. Spector. 1993. In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell 73:47-59.
31. Karlin, S., B. E. Blaisdell, and G. A. Schachtel. 1990. Contrasts in codon usage of latent versus productive genes of Epstein-Barr virus: data and hypotheses. J. Virol. 64:4264-4273.
32. Kennedy, I. M., J. K. Haddow, and J. B. Clements. 1991. A negative regulatory element in the human papillomavirus type 16 genome acts at the level of late mRNA stability. J. Virol. 65:2093-2097.
33. Klumpp, D. J., and L. A. Laimins. 1999. Differentiation-induced changes in promoter usage for transcripts encoding the human papillomavirus type 31 replication protein E1. Virology 257:239-246.
34. Kuchino, Y., and E. Borek. 1978. Tumour-specific phenylalanine tRNA contains two supernumerary methylated bases. Nature 271:126-129.
35. Leask, A., M. Rosenberg, R. Vassar, and E. Fuchs. 1990. Regulation of a human epidermal keratin gene: sequences and nuclear factors involved in keratinocyte-specific transcription. Genes Dev. 4:1985-1998.
36. Leder, C., J. A. Kleinschmidt, C. Wiethe, and M. Muller. 2001. Enhancement of capsid gene expression: preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J. Virol. 75:9201-9209.
37. Lemm, I., and J. Ross. 2002. Regulation of c-myc mRNA decay by translational pausing in a coding region instability determinant. Mol. Cell. Biol. 22:3959-3969.
38. Levine, M., and R. Tjian. 2003. Transcription regulation and animal diversity. Nature 424:147-151.
39. Levy, J. P., R. R. Muldoon, S. Zolotukhin, and C. J. Link, Jr. 1996. Retroviral transfer and expression of a humanized, red-shifted green fluorescent protein gene into human tumor cells. Nat. Biotechnol. 14:610-614.
40. Li, E. R., D. M. Owens, P. Djian, and F. M. Watt. 2000. Expression of involucrin in normal, hyperproliferative and neoplastic mouse keratinocytes. Exp. Dermatol. 9:431-438.
41. Liu, W. J., K. N. Zhao, F. G. Gao, G. R. Leggatt, G. J. Fernando, and I. H. Frazer. 2001. Polynucleotide viral vaccines: codon optimisation and ubiquitin conjugation enhances prophylactic and therapeutic efficacy. Vaccine 20:862-869.
42. Liu, W. J., F. Gao, K. N. Zhao, W. Zhao, G. J. Fernando, R. Thomas, and I. H. Frazer. 2002. Codon modified human papillomavirus type 16 E7 DNA vaccine enhances cytotoxic T-lymphocyte induction and anti-tumour activity. Virology 301:43-52.
43. Mellors, R. C., J. F. Keane, Jr., and G. N. Papanicolaou. 1952. Nucleic acid content of the squamous cancer cell. Science 116:265-269.
44. Merritt, A. J., M. Y. Berika, W. Zhai, S. E. Kirk, B. Ji, M. J. Hardman, and D. R. Garrod. 2002. Suprabasal desmoglein 3 expression in the epidermis of transgenic mice results in hyperproliferation and abnormal differentiation. Mol. Cell. Biol. 22:5846-5858.
45. Moriyama, E. N., and J. R. Powell. 1997. Codon usage bias and tRNA abundance in Drosophila. J. Mol. Evol. 45:514-523.
46. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-rime RT-PCR. Nucleic Acids Res. 29:e45.
47. Plotkin, J. B., H. Robins, and A. J. Levine. 2004. Tissue-specific codon usage and the expression of human genes. Proc. Natl. Acad. Sci. USA 101:12588-12591.
48. Reiners, J. J., Jr., and T. Rupp. 1989. Conversion of xanthine dehydrogenase to xanthine oxidase occurs during keratinocyte differentiation: modulation by 12-O-tetradecanoylphorbol-13-acetate. J. Investig. Dermatol. 93:132-135.
49. Ruesch, M. N., F. Stubenrauch, and L. A. Laimins. 1998. Activation of papillomavirus late gene transcription and genome amplification upon differentiation in semisolid medium is coincident with expression of involucrin and transglutaminase but not keratin-10. J. Virol. 72:5016-5024.
50. Sasagawa, T., P. Pushko, G. Steers, S. E. Gschmeissner, M. A. Hajibagheri, J. Finch, L. Crawford, and M. Tommasino. 1995. Synthesis and assembly of virus-like particles of human papillomaviruses type 6 and type 16 in fission yeast Schizosaccharomyces pombe. Virology 206:126-135.
51. Saunders, N., A. Dicker, C. Popa, S. Jones, and A. Dahler. 1999. Histone deacetylase inhibitors as potential anti-skin cancer agents. Cancer Res. 59:399-404.
52. Schwartz, D. C., and R. Parker. 1999. Mutations in translation initiation factors lead to increased rates of deadenylation and decapping of mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:5247-5256.
53. Schwartz, S. 2000. Regulation of human papillomavirus late gene expression. Upsala J. Med. Sci. 105:171-192.
54. Sokolowski, M., C. Zhao, W. Tan, and S. Schwartz. 1997. AU-rich mRNA instability elements on human papillomavirus type 1 late mRNAs and c-fos mRNAs interact with the same cellular factors. Oncogene 15:2303-2319.
55. Sokolowski, M., W. Tan, M. Jellne, and S. Schwartz. 1998. mRNA instability elements in the human papillomavirus type 16 L2 coding region. J. Virol. 72:1504-1515.
56. Spector, D. L. 1993. Nuclear organization of pre-mRNA processing. Curr. Opin. Cell Biol. 5:442-447.
57. Surosky, R. T., and R. E. Esposito. 1992. Early meiotic transcripts are highly unstable in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:3948-3958.
58. Tierney, M. J., and R. L. Medcalf. 2001. Plasminogen activator inhibitor type 2 contains mRNA instability elements within exon 4 of the coding region. Sequence homology to coding region instability determinants in other mRNAs. J. Biol. Chem. 276:13675-13684.
59. Tumbula, D. L., H. D. Becker, W. Z. Chang, and D. Soll. 2000. Domain-specific recruitment of amide amino acids for protein synthesis. Nature 407:106-110.
60. Varenne, S., D. Baty, H. Verheij, D. Shire, and C. Lazdunski. 1989. The maximum rate of gene expression is dependent on the downstream context of unfavourable codons. Biochimic 71:1221-1229.
61. Wells, K. D., J. A. Foster, K. Moore, V. G. Pursel, and R. J. Wall. 1999. Codon optimization, genetic insulation, and an rtTA reporter improve performance of the tetracycline switch. Transgenic Res. 8:371-381.
62. Wiklund, L., M. Sokolowski, A. Carlsson, M. Rush, and S. Schwartz. 2002. Inhibition of translation by UAUUUAU and UAUUUUUAU motifs of the AU-rich RNA instability element in the HPV-1 late 3′ untranslated region. J. Biol. Chem. 277:40462-40471.
63. Wilusz, C. J., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell. Biol. 2:237-246.
64. Wisdom, R., and W. Lee. 1991. The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev. 5:232-243.
65. Yeilding, N. M., and W. M. Lee. 1997. Coding elements in exons 2 and 3 target c-myc mRNA downregulation during myogenic differentiation. Mol. Cell. Biol. 17:2698-2707.
66. Youngman, E. M., J. L. Brunelle, A. B. Kochaniak, and R. Green. 2004. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117:589-599.
67. Zhao, K. N., and I. H. Frazer. 2002. Saccharomyces cerevisiae is permissive for replication of bovine papillomavirus type 1. J. Virol. 76:12265-12273.
68. Zhao, K. N., W. J. Liu, and I. H. Frazer. 2003. Codon usage bias and A + T content variation in human papillomavirus genomes. Virus Res. 98:95-104.
69. Zhou, J., W. J. Liu, S. W. Peng, X. Y. Sun, and I. Frazer. 1999. Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J. Virol. 73:4972-4982.
70. Zolotukhin, S., M. Potter, W. W. Hauswirth, J. Guy, and N. Muzyczka. 1996. A "humanized" green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J. Virol. 70:4646-4654.