Measures of Compositional Strand Bias Related to Replication Machinery and its Applications

Current Genomics

Volumn 13, Issue 1, 2012, Pages 4-15

  Arakawa, Kazuharu ^a   Tomita, Masaru ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Bacterial replication; GC skew; Nucleotide composition bias; Replication related mutations

Indexed keywords

DOUBLE STRANDED DNA; OLIGONUCLEOTIDE;

COMPUTER PREDICTION; DISCRIMINANT ANALYSIS; DNA REPLICATION; DNA STRAND; DNA TRANSCRIPTION; DROSOPHILA; EUBACTERIACEAE; EUKARYOTE; GENE MUTATION; GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; ORIENTATION; PROKARYOTE; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL NOISE RATIO; XENOPUS;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 84856413643     PISSN: 13892029     EISSN: 18755488     Source Type: Journal    
DOI: 10.2174/138920212799034749     Document Type: Review

References (124)

1. Nakabachi, A.; Yamashita, A.; Toh, H.; Ishikawa, H.; Dunbar, H. E.; Moran, N. A.; Hattori, M. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science, 2006, 314(5797), 267.
2. Hildebrand, F.; Meyer, A.; Eyre-Walker, A. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet., 2010, 6(9), e1001107.
3. Rocha, E. P.; Danchin, A. Base composition bias might result from competition for metabolic resources. Trends Genet., 2002, 18(6), 291-294.
4. Akashi, H.; Gojobori, T. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. U S A, 2002, 99(6), 3695-3700.
5. Mitchell, D. GC content and genome length in Chargaff compliant genomes. Biochem. Biophys. Res. Commun., 2007, 353(1), 207-210.
6. McEwan, C. E.; Gatherer, D.; McEwan, N. R. Nitrogen-fixing aerobic bacteria have higher genomic GC content than non-fixing species within the same genus. Hereditas, 1998, 128(2), 173-178.
7. Naya, H.; Romero, H.; Zavala, A.; Alvarez, B.; Musto, H. Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J. Mol. Evol., 2002, 55(3), 260-264.
8. Wang, H. C.; Susko, E.; Roger, A. J. On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: data quality and confounding factors. Biochem. Biophys. Res. Commun., 2006, 342(3), 681-684.
9. Forsdyke, D. R.; Mortimer, J. R. Chargaff's legacy. Gene, 2000, 261(1), 127-137.
10. Chargaff, E. Structure and function of nucleic acids as cell constituents. Fed. Proc., 1951, 10(3), 654-659.
11. Watson, J. D.; Crick, F. H. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature, 1953, 171(4356), 737-738.
12. Rudner, R.; Karkas, J. D.; Chargaff, E. Separation of B. subtilis DNA into complementary strands. 3. Direct analysis. Proc. Natl. Acad. Sci. U S A, 1968, 60(3), 921-922.
13. Mitchell, D.; Bridge, R. A test of Chargaff's second rule. Biochem. Biophys. Res. Commun., 2006, 340(1), 90-94.
14. Sueoka, N. Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. J. Mol. Evol., 1995, 40(3), 318-325.
15. Nikolaou, C.; Almirantis, Y. Deviations from Chargaff's second parity rule in organellar DNA Insights into the evolution of organellar genomes. Gene, 2006, 381, 34-41.
16. Szybalski, W.; Kubinski, H.; Sheldrick, P. Pyrimidine clusters on the transcribing strand of DNA and their possible role in the initiation of RNA synthesis. Cold Spring Harb Symp. Quant. Biol., 1966, 31, 123-127.
17. Bell, S. J.; Forsdyke, D. R. Deviations from Chargaff's second parity rule correlate with direction of transcription. J. Theor. Biol., 1999, 197(1), 63-76.
18. Lao, P. J.; Forsdyke, D. R. Thermophilic bacteria strictly obey Szybalski's transcription direction rule and politely purine-load RNAs with both adenine and guanine. Genome Res., 2000, 10(2), 228-236.
19. Touchon, M.; Arneodo, A.; d'Aubenton-Carafa, Y.; Thermes, C. Transcription-coupled and splicing-coupled strand asymmetries in eukaryotic genomes. Nucleic Acids Res., 2004, 32(17), 4969-4978.
20. Rocha, E. P. Order and disorder in bacterial genomes. Curr. Opin. Microbiol., 2004, 7(5), 519-527.
21. Lobry, J. R.; Louarn, J. M. Polarisation of prokaryotic chromosomes. Curr. Opin. Microbiol., 2003, 6(2), 101-108.
22. Lobry, J. R. Asymmetric substitution patterns in the two DNA strands of bacteria. Mol. Biol. Evol., 1996, 13(5), 660-665.
23. Rocha, E. P. The replication-related organization of bacterial genomes. Microbiology 2004, 150(Pt 6), 1609-1627.
24. Rocha, E. P. The organization of the bacterial genome. Annu. Rev. Genet., 2008, 42, 211-233.
25. McLean, M. J.; Wolfe, K. H.; Devine, K. M. Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. J. Mol. Evol., 1998, 47(6), 691-696.
26. Mrazek, J.; Karlin, S. Strand compositional asymmetry in bacterial and large viral genomes. Proc. Natl. Acad. Sci. USA, 1998, 95(7), 3720-3725.
27. Rocha, E. Is there a role for replication fork asymmetry in the distribution of genes in bacterial genomes? Trends Microbiol., 2002, 10(9), 393-395.
28. Guo, F. B.; Ning, L. W. Strand-specific Composition Bias in Bacterial Genomes. In DNA Replication-Current Advances, Seligmann, H., Ed. InTech: 2011.
29. Guo, F. B.; Yu, X. J. Separate base usages of genes located on the leading and lagging strands in Chlamydia muridarum revealed by the Z curve method. BMC Genomics, 2007, 8, 366.
30. Guo, F. B.; Yuan, J. B. Codon usages of genes on chromosome, and surprisingly, genes in plasmid are primarily affected by strandspecific mutational biases in Lawsonia intracellularis. DNA Res., 2009, 16(2), 91-104.
31. Rocha, E. P.; Danchin, A.; Viari, A. Universal replication biases in bacteria. Mol. Microbiol., 1999, 32(1), 11-16.
32. Wei, W.; Guo, F. B. Strong Strand Composition Bias in the Genome of Ehrlichia canis Revealed by Multiple Methods. Open Microbiol. J., 2010, 4, 98-102.
33. Salzberg, S. L.; Salzberg, A. J.; Kerlavage, A. R.; Tomb, J. F. Skewed oligomers and origins of replication. Gene, 1998, 217(1-2), 57-67.
34. Arakawa, K.; Uno, R.; Nakayama, Y.; Tomita, M. Validating the significance of genomic properties of Chi sites from the distribution of all octamers in Escherichia coli. Gene, 2007, 392(1-2), 239-246.
35. Kowalczykowski, S. C.; Dixon, D. A.; Eggleston, A. K.; Lauder, S. D.; Rehrauer, W. M. Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev., 1994, 58(3), 401-465.
36. Uno, R.; Nakayama, Y.; Arakawa, K.; Tomita, M. The orientation bias of Chi sequences is a general tendency of G-rich oligomers. Gene, 2000, 259(1-2), 207-215.
37. Bigot, S.; Saleh, O. A.; Cornet, F.; Allemand, J. F.; Barre, F. X. Oriented loading of FtsK on KOPS. Nat. Struct. Mol. Biol., 2006, 13(11), 1026-1028.
38. Bigot, S.; Saleh, O. A.; Lesterlin, C.; Pages, C.; El Karoui, M.; Dennis, C.; Grigoriev, M.; Allemand, J. F.; Barre, F. X.; Cornet, F. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J., 2005, 24, (21), 3770-3780.
39. Saleh, O. A.; Perals, C.; Barre, F. X.; Allemand, J. F. Fast, DNAsequence independent translocation by FtsK in a single-molecule experiment. EMBO J., 2004, 23(12), 2430-2439.
40. Chedin, F.; Kowalczykowski, S. C. A novel family of regulated helicases/nucleases from Gram-positive bacteria: insights into the initiation of DNA recombination. Mol. Microbiol., 2002, 43(4), 823-834.
41. Hendrickson, H.; Lawrence, J. G. Selection for chromosome architecture in bacteria. J. Mol. Evol., 2006, 62(5), 615-629.
42. Rocha, E. P.; Danchin, A. Gene essentiality determines chromosome organisation in bacteria. Nucleic Acids Res., 2003, 31(22), 6570-6577.
43. Omont, N.; Kepes, F. Transcription/replication collisions cause bacterial transcription units to be longer on the leading strand of replication. Bioinformatics, 2004, 20(16), 2719-2725.
44. Price, M. N.; Alm, E. J.; Arkin, A. P. Interruptions in gene expression drive highly expressed operons to the leading strand of DNA replication. Nucleic Acids Res., 2005, 33(10), 3224-3234.
45. Arakawa, K.; Tomita, M. Selection effects on the positioning of genes and gene structures from the interplay of replication and transcription in bacterial genomes. Evol. Bioinform. Online, 2007, 3, 279-286.
46. Valens, M.; Penaud, S.; Rossignol, M.; Cornet, F.; Boccard, F. Macrodomain organization of the Escherichia coli chromosome. EMBO J. 2004, 23(21), 4330-4341.
47. Gierlik, A.; Kowalczuk, M.; Mackiewicz, P.; Dudek, M. R.; Cebrat, S. Is there replication-associated mutational pressure in the Saccharomyces cerevisiae genome? J. Theor. Biol., 2000, 202(4), 305-314.
48. Huvet, M.; Nicolay, S.; Touchon, M.; Audit, B.; d'Aubenton-Carafa, Y.; Arneodo, A.; Thermes, C. Human gene organization driven by the coordination of replication and transcription. Genome Res., 2007, 17(9), 1278-1285.
49. Necsulea, A.; Guillet, C.; Cadoret, J. C.; Prioleau, M. N.; Duret, L. The relationship between DNA replication and human genome organization. Mol. Biol. Evol., 2009, 26(4), 729-741.
50. Touchon, M.; Nicolay, S.; Audit, B.; Brodie of Brodie, E. B.; d'Aubenton-Carafa, Y.; Arneodo, A.; Thermes, C. Replicationassociated strand asymmetries in mammalian genomes: toward detection of replication origins. Proc. Natl. Acad. Sci. USA, 2005, 102(28), 9836-9841.
51. Calistri, E.; Livi, R.; Buiatti, M. Evolutionary trends of GC/AT distribution patterns in promoters. Mol. Phylogenet. Evol., 2011, 60(2), 228-235.
52. Fujimori, S.; Washio, T.; Tomita, M. GC-compositional strand bias around transcription start sites in plants and fungi. BMC Genomics, 2005, 6, 26.
53. Tatarinova, T.; Brover, V.; Troukhan, M.; Alexandrov, N. Skew in CG content near the transcription start site in Arabidopsis thaliana. Bioinformatics, 2003, 19 Suppl 1, i313-4.
54. Arakawa, K.; Suzuki, H.; Tomita, M. Computational Genome Analysis Using The G-language System. Genes, Genomes and Genomics, 2008, 2(1), 1-13.
55. Frank, A. C.; Lobry, J. R. Oriloc: prediction of replication boundaries in unannotated bacterial chromosomes. Bioinformatics, 2000, 16(6), 560-561.
56. Mackiewicz, P.; Zakrzewska-Czerwinska, J.; Zawilak, A.; Dudek, M. R.; Cebrat, S. Where does bacterial replication start? Rules for predicting the oriC region. Nucleic Acids Res., 2004, 32(13), 3781-3791.
57. Perna, N. T.; Kocher, T. D. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J. Mol. Evol., 1995, 41(3), 353-358.
58. Freeman, J. M.; Plasterer, T. N.; Smith, T. F.; Mohr, S. C. Patterns of Genome Organization in Bacteria. Science 1998, 279(5358), 1827.
59. Bell, S. J.; Forsdyke, D. R. Accounting units in DNA. J. Theor. Biol., 1999, 197(1), 51-61.
60. Palleja, A.; Guzman, E.; Garcia-Vallve, S.; Romeu, A. In silico prediction of the origin of replication among bacteria: a case study of Bacteroides thetaiotaomicron. OMICS, 2008, 12(3), 201-210.
61. Touchon, M.; Rocha, E. P. From GC skews to wavelets: a gentle guide to the analysis of compositional asymmetries in genomic data. Biochimie, 2008, 90(4), 648-659.
62. Lobry, J. R. A simple vectorial representation of DNA sequences for the detection of replication origins in bacteria. Biochimie, 1996, 78(5), 323-326.
63. Peng, C. K.; Buldyrev, S. V.; Goldberger, A. L.; Havlin, S.; Sciortino, F.; Simons, M.; Stanley, H. E. Long-range correlations in nucleotide sequences. Nature, 1992, 356(6365), 168-170.
64. Zhang, C. T.; Zhang, R.; Ou, H. Y. The Z curve database: a graphic representation of genome sequences. Bioinformatics, 2003, 19(5), 593-599.
65. Zhang, R.; Zhang, C. T. Z curves, an intutive tool for visualizing and analyzing the DNA sequences. J. Biomol. Struct. Dyn., 1994, 11(4), 767-782.
66. Grigoriev, A. Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res., 1998, 26(10), 2286-2290.
67. Tillier, E. R.; Collins, R. A. The contributions of replication orientation, gene direction, and signal sequences to basecomposition asymmetries in bacterial genomes. J. Mol. Evol., 2000, 50(3), 249-257.
68. Arakawa, K.; Saito, R.; Tomita, M. Noise-reduction filtering for accurate detection of replication termini in bacterial genomes. FEBS Lett., 2007, 581(2), 253-258.
69. Song, J.; Ware, A.; Liu, S. L. Wavelet to predict bacterial ori and ter: a tendency towards a physical balance. BMC Genomics, 2003, 4(1), 17.
70. Nicolay, S.; Brodie Of Brodie, E. B.; Touchon, M.; Audit, B.; d'Aubenton-Carafa, Y.; Thermes, C.; Arneodo, A. Bifractality of human DNA strand-asymmetry profiles results from transcription. Phys. Rev. E Stat. Nonlin Soft Matter Phys., 2007, 75(3 Pt 1), 032902.
71. Kowalczuk, M.; Mackiewicz, P.; Mackiewicz, D.; Nowicka, A.; Dudkiewicz, M.; Dudek, M. R.; Cebrat, S. DNA asymmetry and the replicational mutational pressure. J. Appl. Genet., 2001, 42(4), 553-577.
72. Rocha, E. P.; Danchin, A. Ongoing evolution of strand composition in bacterial genomes. Mol. Biol. Evol., 2001, 18(9), 1789-1799.
73. Rocha, E. P.; Touchon, M.; Feil, E. J. Similar compositional biases are caused by very different mutational effects. Genome Res., 2006, 16(12), 1537-1547.
74. Lobry, J. R.; Sueoka, N. Asymmetric directional mutation pressures in bacteria. Genome Biol., 2002, 3(10), RESEARCH0058.
75. Arakawa, K.; Suzuki, H.; Tomita, M. Quantitative analysis of replication-related mutation and selection pressures in bacterial chromosomes and plasmids using generalised GC skew index. BMC Genomics, 2009, 10, 640.
76. Arakawa, K.; Tomita, M. The GC Skew Index: A Measure of Genomic Compositional Asymmetry and the Degree of Replicational Selection. Evol. Bioinform. Online, 2007, 3, 159-168.
77. Chen, C.; Chen, C. W. Quantitative analysis of mutation and selection pressures on base composition skews in bacterial chromosomes. BMC Genomics, 2007, 8, 286.
78. Marin, A.; Xia, X. GC skew in protein-coding genes between the leading and lagging strands in bacterial genomes: new substitution models incorporating strand bias. J. Theor. Biol., 2008, 253(3), 508-513.
79. Morton, R. A.; Morton, B. R. Separating the effects of mutation and selection in producing DNA skew in bacterial chromosomes. BMC Genomics, 2007, 8, 369.
80. Frank, A. C.; Lobry, J. R. Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene, 1999, 238(1), 65-77.
81. Reyes, A.; Gissi, C.; Pesole, G.; Saccone, C. Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol. Biol. Evol., 1998, 15(8), 957-966.
82. Coulondre, C.; Miller, J. H.; Farabaugh, P. J.; Gilbert, W. Molecular basis of base substitution hotspots in Escherichia coli. Nature, 1978, 274(5673), 775-780.
83. Frederico, L. A.; Kunkel, T. A.; Shaw, B. R. A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry, 1990, 29(10), 2532-2537.
84. Lindahl, T.; Nyberg, B. Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry, 1974, 13(16), 3405-3410.
85. Francino, M. P.; Ochman, H. Strand asymmetries in DNA evolution. Trends Genet., 1997, 13(6), 240-245.
86. Karlin, S. Bacterial DNA strand compositional asymmetry. Trends Microbiol., 1999, 7(8), 305-308.
87. Worning, P.; Jensen, L. J.; Hallin, P. F.; Staerfeldt, H. H.; Ussery, D. W. Origin of replication in circular prokaryotic chromosomes. Environ. Microbiol., 2006, 8(2), 353-361.
88. Campbell, A.; Mrazek, J.; Karlin, S. Genome signature comparisons among prokaryote, plasmid, and mitochondrial DNA. Proc. Natl. Acad. Sci. U S A, 1999, 96(16), 9184-9189.
89. Lawrence, J. G.; Ochman, H. Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol., 1997, 44(4), 383-397.
90. Ochman, H.; Lawrence, J. G.; Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature, 2000, 405(6784), 299-304.
91. Suzuki, H.; Sota, M.; Brown, C. J.; Top, E. M. Using Mahalanobis distance to compare genomic signatures between bacterial plasmids and chromosomes. Nucleic Acids Res., 2008, 36(22), e147.
92. Vieira-Silva, S.; Rocha, E. P. The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS Genet., 2010, 6(1), e1000808.
93. Sharp, P. M.; Bailes, E.; Grocock, R. J.; Peden, J. F.; Sockett, R. E. Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res., 2005, 33(4), 1141-1153.
94. Deshpande, A. M.; Newlon, C. S. DNA replication fork pause sites dependent on transcription. Science, 1996, 272(5264), 1030-1033.
95. French, S. Consequences of replication fork movement through transcription units in vivo. Science, 1992, 258(5086), 1362-1365.
96. Nikolaou, C.; Almirantis, Y. A study on the correlation of nucleotide skews and the positioning of the origin of replication: different modes of replication in bacterial species. Nucleic Acids Res., 2005, 33(21), 6816-6822.
97. Bell, S. P.; Dutta, A. DNA replication in eukaryotic cells. Annu. Rev. Biochem., 2002, 71, 333-374.
98. Coverley, D.; Laskey, R. A. Regulation of eukaryotic DNA replication. Annu. Rev. Biochem., 1994, 63, 745-776.
99. Hyrien, O.; Mechali, M. Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos. EMBO J., 1993, 12(12), 4511-4520.
100. Sasaki, T.; Sawado, T.; Yamaguchi, M.; Shinomiya, T. Specification of regions of DNA replication initiation during embryogenesis in the 65-kilobase DNApolalpha-dE2F locus of Drosophila melanogaster. Mol. Cell Biol., 1999, 19(1), 547-555.
101. Gilbert, D. M. Making sense of eukaryotic DNA replication origins. Science, 2001, 294(5540), 96-100.
102. Demeret, C.; Vassetzky, Y.; Mechali, M. Chromatin remodelling and DNA replication: from nucleosomes to loop domains. Oncogene, 2001, 20(24), 3086-3093.
103. McNairn, A. J.; Gilbert, D. M. Epigenomic replication: linking epigenetics to DNA replication. Bioessays, 2003, 25(7), 647-656.
104. Mechali, M. DNA replication origins: from sequence specificity to epigenetics. Nat. Rev. Genet., 2001, 2(8), 640-645.
105. The ENCODE consortium, Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature, 2007, 447(7146), 799-816.
106. Cadoret, J. C.; Meisch, F.; Hassan-Zadeh, V.; Luyten, I.; Guillet, C.; Duret, L.; Quesneville, H.; Prioleau, M. N. Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc. Natl. Acad. Sci. USA, 2008, 105(41), 15837-15842.
107. Cayrou, C.; Coulombe, P.; Vigneron, A.; Stanojcic, S.; Ganier, O.; Peiffer, I.; Rivals, E.; Puy, A.; Laurent-Chabalier, S.; Desprat, R.; Mechali, M., Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res., 2011, 21(9), 1438-1449.
108. Hansen, R. S.; Thomas, S.; Sandstrom, R.; Canfield, T. K.; Thurman, R. E.; Weaver, M.; Dorschner, M. O.; Gartler, S. M.; Stamatoyannopoulos, J. A. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. U S A, 2010, 107(1), 139-144.
109. Lucas, I.; Palakodeti, A.; Jiang, Y.; Young, D. J.; Jiang, N.; Fernald, A. A.; Le Beau, M. M. High-throughput mapping of origins of replication in human cells. EMBO Rep., 2007, 8(8), 770-777.
110. Chen, C. L.; Duquenne, L.; Audit, B.; Guilbaud, G.; Rappailles, A.; Baker, A.; Huvet, M.; d'Aubenton-Carafa, Y.; Hyrien, O.; Arneodo, A.; Thermes, C. Replication-associated mutational asymmetry in the human genome. Mol. Biol. Evol., 2011, 28(8), 2327-2337.
111. Polak, P.; Arndt, P. F. Long-range bidirectional strand asymmetries originate at CpG islands in the human genome. Genome Biol. Evol., 2009, 1, 189-197.
112. Audit, B.; Nicolay, S.; Huvet, M.; Touchon, M.; d'Aubenton-Carafa, Y.; Thermes, C.; Arneodo, A. DNA replication timing data corroborate in silico human replication origin predictions. Phys. Rev. Lett., 2007, 99(24), 248102.
113. Audit, B.; Zaghloul, L.; Vaillant, C.; Chevereau, G.; d'Aubenton-Carafa, Y.; Thermes, C.; Arneodo, A. Open chromatin encoded in DNA sequence is the signature of 'master' replication origins in human cells. Nucleic Acids Res., 2009, 37(18), 6064-6075.
114. Baker, A.; Nicolay, S.; Zaghloul, L.; d'Aubenton-Carafa, Y.; Thermes, C.; Audit, B.; Arneodo, A. Wavelet-based method to disentangle transcription- and replication-associated strand asymmetries in mammalian genomes. Appl. Comput. Harmon. Anal., 2010, 28(2), 150-170.
115. Touchon, M.; Nicolay, S.; Arneodo, A.; d'Aubenton-Carafa, Y.; Thermes, C. Transcription-coupled TA and GC strand asymmetries in the human genome. FEBS Lett., 2003, 555(3), 579-582.
116. Lundgren, M.; Andersson, A.; Chen, L.; Nilsson, P.; Bernander, R. Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc. Natl. Acad. Sci. U S A, 2004, 101(18), 7046-7051.
117. Robinson, N. P.; Dionne, I.; Lundgren, M.; Marsh, V. L.; Bernander, R.; Bell, S. D. Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell, 2004, 116(1), 25-38.
118. Markowitz, V. M.; Chen, I. M.; Palaniappan, K.; Chu, K.; Szeto, E.; Grechkin, Y.; Ratner, A.; Anderson, I.; Lykidis, A.; Mavromatis, K.; Ivanova, N. N.; Kyrpides, N. C. The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Res., 2010, 38(Database issue), D382-D390.
119. Charif, D.; Lobry, J. R. SeqinR 1.0-2: a contributed package to the R-project for statistical computing devoted to biological sequences retrieval and analysis. In Structural approaches to sequence evolution: Molecules, networks, populations, Bastolla, U.; Porto, M.; H.E., R.; Vendruscolo, M., Eds. Springer Verlag: New York, 2007; pp 207-232.
120. Arakawa, K.; Mori, K.; Ikeda, K.; Matsuzaki, T.; Kobayashi, Y.; Tomita, M. G-language Genome Analysis Environment: a workbench for nucleotide sequence data mining. Bioinformatics, 2003, 19(2), 305-306.
121. Arakawa, K.; Tomita, M. G-language System as a platform for large-scale analysis of high-throughput omics data. Journal of Pesticide Science, 2006, 31(3), 282-288.
122. Arakawa, K.; Kido, N.; Oshita, K.; Tomita, M. G-language genome analysis environment with REST and SOAP web service interfaces. Nucleic Acids Res., 2010, 38(Web Server issue), W700-W705.
123. Gao, F.; Zhang, C. T. DoriC: a database of oriC regions in bacterial genomes. Bioinformatics, 2007, 23(14), 1866-1867.
124. Kono, N.; Arakawa, K.; Tomita, M. Comprehensive prediction of chromosome dimer resolution sites in bacterial genomes. BMC Genomics, 2011, 12, 19.