Cloning and characterization of the gene encoding the highly expressed ribosomal protein L3 of the ciliated protozoan Tetrahymena thermophila. Evidence for differential codon usage in highly expressed genes

Cell Biology International

Volumn 23, Issue 8, 1999, Pages 551-560

  Larsen, Leif K ^a   Andreasen, Per H ^a   Dreisig, Hanne ^a   Palm, Lisbeth ^a   Nielsen, Henrik ^b   Engberg, Jan ^c   Kristiansen, Karsten ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Codon bias; Database analysis; Gene expression; Ribosomal protein

Indexed keywords

ADENINE; COMPLEMENTARY DNA; MEMBRANE ANTIGEN; RIBOSOME PROTEIN; THYMINE;

ARTICLE; CODON; CODON USAGE; DATA ANALYSIS; GENE; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; INTRON; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; TETRAHYMENA THERMOPHILA;

TETRAHYMENA THERMOPHILA;

EID: 0033500379     PISSN: 10656995     EISSN: None     Source Type: Journal    
DOI: 10.1006/cbir.1999.0419     Document Type: Article

References (50)

1. Andreasen PH, Dreisig H, Kristiansen K. Regulation of ribosome synthesis in Tetrahymena pyriformis. 3. Analysis by translation in vitro of RNA isolated during nutritional shift-down and nutritional shift-up. Eur J Biochem. 140:1984;485-492.
2. Andreasen PH, Dreisig H, Kristiansen K. Unusual ciliate-specific codons in Tetrahymena mRNAs are translated correctly in a rabbit reticulocyte lysate supplemented with a subcellular fraction from Tetrahymena. Biochem J. 244:1987;331-335.
3. Aota S, Ikemura T. Diversity in G+C content at the third position of codons in vertebrate genes and its cause. Nucleic Acids Res. 14:1986;6345-6355.
4. Bernardi G, Bernardi G. Compositional constraints and genome evolution. J Mol Evol. 24:1986;1-11.
5. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F. The mosaic genome of warm-blooded vertebrates. Science. 228:1985;953-958.
6. Chiapello H, Lisacek F, Caboche M, Henaut A. Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene. 209:1998;GC1-GC38.
7. Csank C, Taylor FM, Martindale DW. Nuclear pre-mRNA introns: Analysis and comparison of intron sequences from Tetrahymena thermophila and other eukaryotes. Nucleic Acids Res. 18:1990;5133-5141.
8. Deak JC, Doerder FP. Sequence, codon usage and cysteine periodicity of the SerH1 gene and in the encoded surface protein of Tetrahymena thermophila. Gene. 164:1995;163-166.
9. Deschavanne P, Filipski J. Correlation of GC content with replication timing and repair mechanisms in weakly expressed E. coli genes. Nucleic Acids Res. 23:1995;1350-1353.
10. Dreisig H, Andreasen PH, Kristiansen K. Regulation of ribosome synthesis in Tetrahymena pyriformis. 1. Coordination of synthesis of ribosomal proteins and ribosomal RNA during nutritional shift-down. Eur J Biochem. 140:1984;469-475.
11. Dreisig H, Andreasen PH, Kristiansen K. Regulation of ribosome synthesis in Tetrahymena pyriformis. 2. Coordination of synthesis of ribosomal proteins and ribosomal RNA during nutritional shift-up. Eur J Biochem. 140:1984;477-483.
12. Engberg J, Bojsen K, Nielsen H. Structural characterization of the intron containing S25 ribosomal protein genes from two Tetrahymena species. Molecular Biology of RNA. 1989;Alan R. Liss, Inc. p. 145-154.
13. Eyre-Walker A. Synonymous codon bias is related to gene length in Escherichia coli: Selection for translational accuracy? Mol Biol Evol. 13:1996;864-872.
14. Filipski J. Correlation between molecular clock ticking, codon usage fidelity of DNA repair, chromosome banding and chromatin compactness in germline cells. FEBS Lett. 217:1987;184-186.
15. Flinta C, Persson B, Jornwall H, Von Heijne G. Sequence determinants of cytosolic N-terminal protein processing. Eur J Biochem. 154:1986;193-196.
16. Gniadkowski M, Hemmings-Mieszczak M, Klahre U, Liu H-X, Filipowicz W. Characterization of intronic uridine-rich sequence elements acting as possible targets for nuclear proteins during pre-mRNA splicing in Nicotiana plumbaginifolia. Nucleic Acids Res. 24:1996;619-627.
17. Gorovsky MA. Genome organization and reorganization in Tetrahymena. Annu Rev Genet. 14:1980;203-239.
18. Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 9:1981;R43-R73.
19. Grosjean H, Fiers W. Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene. 18:1982;199-209.
20. Hansen TS, Andreasen PH, Dreisig H, Højrup P, Nielsen H, Engberg J, Kristiansen K. Tetrahymena thermophila acidic ribosomal protein L37 contains an archaebacterial type of C-terminus. Gene. 105:1991;143-150.
21. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 2:1985;13-34.
22. Karlin S, Burge C. Dinucleotide relative abundance extremes: A genomic signature. Trends Genet. 11:1995;283-290.
23. Kurland CG. Codon bias and gene expression. FEBS Lett. 285:1991;165-169.
24. Larsen, LK, 1998, Structure and expression of class II genes in Tetrahymena thermophila, Odense University.
25. Lee C, Levin A, Branton D. Copper staining: A five-minute protein stain for sodium dodecyl sulfate-polyacrylamide gels. Anal Biochem. 166:1987;308-312.
26. Mager WH, Planta RJ, Ballesta J-PG, Lee JC, Mizuta K, Suzuki K, Warner JR, Woolford J. A new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Nucleic Acids Res. 25:1997;4872-4875.
27. Maniatis T, Fritsch EF, Sambrook J. Molecular Cloning: A Laboratory Manual. 1982;Cold Spring Harbor Laboratory Press, NY.
28. Martindale DW. A conjugation-specific gene (cnjC) from Tetrahymena encodes a protein homologous to yeast RNA polymerase subunits (RPB3, RPC40) and similar to a portion of the prokaryotic RNA polymerase alpha subunit (rpoA). Nucleic Acids Res. 18:1990;2953-2960.
29. Médigue C, Rouxel T, Vigier P, Hénaut A, Danchin A. Evidence for horizontal gene transfer in Escherichia coli speciation. J Mol Biol. 222:1991;851-856.
30. Montero LM, Salinas J, Matassi G, Bernardi G. Gene distribution and isochore organization in the nuclear genome of plants. Nucleic Acids Res. 18:1990;1859-1867.
31. Moreland RB, Nam HG, Hereford LM, Fried HM. Identification of a nuclear localization signal of a yeast ribosomal protein. Proc Natl Acad Sci U S A. 82:1985;6561-6565.
32. Moriyama EN. Codon usage bias and tRNA abundance in Drosophila. J Mol Evol. 45:1997;514-523.
33. Nakamura Y, Tabata S. Codon-anticodon assignment and detection of codon usage trends in seven microbial genomes. Microb Comp Genomics. 2:1997;299-312.
34. Nielsen H, Andreasen PH, Dreisig H, Kristiansen K, Engberg J. An intron in a ribosomal protein gene from Tetrahymena. EMBO J. 5:1986;2711-2717.
35. Nilsson B, Uhlén M, Josephson S, Gatenbeck S, Philipson L. An improved positive selection vector constructed by oligonucleotide mediated mutagenesis. Nucleic Acids Res. 11:1983;8019-8030.
36. Planta RJ, Mager WH. The list of cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Yeast. 14:1998;471-477.
37. Prescott DM. The DNA of ciliated protozoa. Microbiol Rev. 58:1994;233-267.
38. Rosendahl G, Andreasen PH, Kristiansen K. Structure and evolution of the Tetrahymena thermophila gene encoding ribosomal protein L21. Gene. 98:1991;161-167.
39. Sharp PM, Devine KM. Codon usage and gene expression level in Dictyostelium discoideum: Highly expressed genes do 'prefer' optimal codons. Nucleic Acids Res. 17:1989;5029-5039.
40. Simoneau P, Li CM, Loechel S, Wenzel R, Herrmann R, Hu PC. Codon reading scheme in Mycoplasma pneumoniae revealed by the analysis of the complete set of tRNA genes. Nucleic Acids Res. 21:1993;4967-4974.
41. Sogin ML, Elwood HJ, Gunderson JH. Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci U S A. 83:1986;1383-1387.
42. Tannich E, Horstmann RD. Codon usage in pathogenic Entamoeba histolytica. J Mol Evol. 34:1992;272-273.
43. Taylor FM, Martindale DW. Retroviral-type zinc fingers and glycine-rich repeats in a protein encoded by cnjB, a Tetrahymena gene active during meiosis. Nucleic Acids Res. 21:1993;4610-4614.
44. Thomas LK, Dix DB, Thompson RC. Codon choice and gene expression: synonymous codons differ in their ability to direct aminoacylated-transfer RNA binding to ribosomes in vitro. Proc Natl Acad Sci U S A. 85:1988;4242-4246.
45. Tondravi MM, Willis RL, Love JR, Bannon GA. Molecular characterization of SerH3, a Tetrahymena thermophila gene encoding a temperature-regulated surface antigen. Mol Cell Biol. 10:1990;6091-6096.
46. Winkler HH, Wood DO. Codon usage in selected AT-rich bacteria. Biochimie. 70:1988;977-986.
47. Wolfe KH, Sharp PM, Li W-H. Mutation rates differ among regions of the mammalian genome. Nature. 337:1989;283-285.
48. Wool IG, Chan YL, Glück A. Structure and evolution of mammalian ribosomal proteins. Biochem Cell Biol. 73:1995;933-947.
49. Wright F. The 'effective number of codons' used in a gene. Gene. 87:1990;23-29.
50. Yao MC, Yao CH. Transformation of Tetrahymena to cycloheximide resistance with a ribosomal protein gene through sequence replacement. Proc Natl Acad Sci U S A. 88:1991;9493-9497.