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Volume 2015, Article ID 267570, 20 pages
http://dx.doi.org/10.1155/2015/267570
Review Article

From Structure-Function Analyses to Protein Engineering for Practical Applications of DNA Ligase

1Central Research Laboratory, Hitachi Ltd., 1-280 Higashi-koigakubo, Kokubunji, Tokyo 185-8601, Japan
2Department of Bioscience and Biotechnology, Graduate School of Bioresource and Bioenvironmental Sciences, Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka-shi, Fukuoka 812-8581, Japan

Received 20 February 2015; Accepted 18 May 2015

Academic Editor: Frédéric Pecorari

Copyright © 2015 Maiko Tanabe et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Weiss and C. C. Richardson, “Enzymatic breakage and joining of deoxyribonucleic acid, I. Repair of single-strand breaks in DNA by an enzyme system from Escherichia coli infected with T4 bacteriophage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 57, no. 4, pp. 1021–1028, 1967. View at Publisher · View at Google Scholar · View at Scopus
  2. H.-M. Eun, “DNA ligases,” in Enzymology Primer for Recombinant DNA Technology, pp. 109–133, Academic Press, San Diego, Calif, USA, 1996. View at Google Scholar
  3. J. M. Pascal, “DNA and RNA ligases: structural variations and shared mechanisms,” Current Opinion in Structural Biology, vol. 18, no. 1, pp. 96–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Shuman and B. Schwer, “RNA capping enzyme and DNA ligase: a superfamily of covalent nucleotidyl transferases,” Molecular Microbiology, vol. 17, no. 3, pp. 405–410, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Shuman, “Closing the gap on DNA ligase,” Structure, vol. 4, no. 6, pp. 653–656, 1996. View at Google Scholar · View at Scopus
  6. U. Landegren, R. Kaiser, J. Sanders, and L. Hood, “A ligase-mediated gene detection technique,” Science, vol. 241, no. 4869, pp. 1077–1080, 1988. View at Publisher · View at Google Scholar · View at Scopus
  7. O. Söderberg, M. Gullberg, M. Jarvius et al., “Direct observation of individual endogenous protein complexes in situ by proximity ligation,” Nature Methods, vol. 3, no. 12, pp. 995–1000, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. H. S. Subramanya, A. J. Doherty, S. R. Ashford, and D. B. Wigley, “Crystal structure of an ATP-dependent DNA ligase from bacteriophage T7,” Cell, vol. 85, no. 4, pp. 607–615, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. J. M. Pascal, P. J. O'Brien, A. E. Tomkinson, and T. Ellenberger, “Human DNA ligase I completely encircles and partially unwinds nicked DNA,” Nature, vol. 432, no. 7016, pp. 473–478, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. J. M. Pascal, O. V. Tsodikov, G. L. Hura et al., “A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA,” Molecular Cell, vol. 24, no. 2, pp. 279–291, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. H. Nishida, S. Kiyonari, Y. Ishino, and K. Morikawa, “The closed structure of an archaeal DNA ligase from Pyrococcus furiosus,” Journal of Molecular Biology, vol. 360, no. 5, pp. 956–967, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. S. B. Zimmerman, J. W. Little, C. K. Oshinsky, and M. Gellert, “Enzymatic joining of DNA strands: a novel reaction of diphosphopyridine nucleotide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 57, no. 6, pp. 1841–1848, 1967. View at Google Scholar · View at Scopus
  13. I. R. Lehman, “DNA ligase: structure, mechanism, and function,” Science, vol. 186, no. 4166, pp. 790–797, 1974. View at Publisher · View at Google Scholar · View at Scopus
  14. M. J. Engler and C. C. Richardson, “DNA ligases,” in The Enzymes, P. D. Boyer, Ed., vol. 15, pp. 3–29, Academic Press, New York, NY, USA, 1982. View at Google Scholar
  15. P. Sadowski, B. Ginsberg, A. Yudelevich, L. Feiner, and J. Hurwitz, “Enzymatic mechanisms of the repair and breakage of DNA,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 33, pp. 165–177, 1968. View at Google Scholar · View at Scopus
  16. T. Lindahl and R. D. Wood, “Quality control by DNA repair,” Science, vol. 286, no. 5446, pp. 1897–1905, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Waga and B. Stillman, “The DNA replication fork in eukaryotic cells,” Annual Review of Biochemistry, vol. 67, pp. 721–751, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Ellenberger and A. E. Tomkinson, “Eukaryotic DNA ligases: structural and functional insights,” Annual Review of Biochemistry, vol. 77, pp. 313–338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Wilkinson, J. Day, and R. Bowater, “Bacterial DNA ligases,” Molecular Microbiology, vol. 40, no. 6, pp. 1241–1248, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Sriskanda, R. W. Moyer, and S. Shuman, “NAD+-dependent DNA ligase encoded by a eukaryotic virus,” The Journal of Biological Chemistry, vol. 276, no. 39, pp. 36100–36109, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. Z. A. Wood, R. S. Sabatini, and S. L. Hajduk, “RNA ligase: picking up the pieces,” Molecular Cell, vol. 13, no. 4, pp. 455–456, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. L. K. Wang and S. Shuman, “Structure-function analysis of yeast tRNA ligase,” RNA, vol. 11, no. 6, pp. 966–975, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Sawaya and S. Shuman, “Mutational analysis of the guanylyltransferase component of mammalian mRNA capping enzyme,” Biochemistry, vol. 42, no. 27, pp. 8240–8249, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Shuman, “DNA ligases: progress and prospects,” The Journal of Biological Chemistry, vol. 284, no. 26, pp. 17365–17369, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Sriskanda and S. Shuman, “Chlorella virus DNA ligase: nick recognition and mutational analysis,” Nucleic Acids Research, vol. 26, no. 2, pp. 525–531, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Sriskanda and S. Shuman, “Role of nucleotidyltransferase motifs I, III and IV in the catalysis of phosphodiester bond formation by Chlorella virus DNA ligase,” Nucleic Acids Research, vol. 30, no. 4, pp. 903–911, 2002. View at Google Scholar · View at Scopus
  27. V. Sriskanda and S. Shuman, “Mutational analysis of Chlorella virus DNA ligase: Catalytic roles of domain I and motif VI,” Nucleic Acids Research, vol. 26, no. 20, pp. 4618–4625, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Samai and S. Shuman, “Kinetic analysis of DNA strand joining by Chlorella virus DNA ligase and the role of nucleotidyltransferase motif VI in ligase adenylylation,” The Journal of Biological Chemistry, vol. 287, no. 34, pp. 28609–28618, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. C. A. Foy and H. C. Parkes, “Emerging homogeneous DNA-based technologies in the clinical laboratory,” Clinical Chemistry, vol. 47, no. 6, pp. 990–1000, 2001. View at Google Scholar · View at Scopus
  30. R. C. Conaway and I. R. Lehman, “A DNA primase activity associated with DNA polymerase alpha from Drosophila melanogaster embryos,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 8, pp. 2523–2527, 1982. View at Publisher · View at Google Scholar · View at Scopus
  31. H. A. Erlich, “Polymerase chain reaction,” Journal of Clinical Immunology, vol. 9, no. 6, pp. 437–447, 1989. View at Publisher · View at Google Scholar · View at Scopus
  32. D. S. Levin, W. Bai, N. Yao, M. O'Donnell, and A. E. Tomkinson, “An interaction between DNA ligase I and proliferating cell nuclear antigen: implications for Okazaki fragment synthesis and joining,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 24, pp. 12863–12868, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. N. G. Copeland, N. A. Jenkins, and D. L. Court, “Recombineering: a powerful new tool for mouse functional genomics,” Nature Reviews Genetics, vol. 2, no. 10, pp. 769–779, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Y. Wu and R. B. Wallace, “Specificity of the nick-closing activity of bacteriophage T4 DNA ligase,” Gene, vol. 76, no. 2, pp. 245–254, 1989. View at Publisher · View at Google Scholar · View at Scopus
  35. A. M. Alves and F. J. Carr, “Dot blot detection of point mutations with adjacently hybridising synthetic oligonucleotide probes,” Nucleic Acids Research, vol. 16, no. 17, article 8723, 1988. View at Publisher · View at Google Scholar · View at Scopus
  36. D. A. Nickerson, R. Kaiser, S. Lappin, J. Stewart, L. Hood, and U. Landegren, “Automated DNA diagnostics using an ELISA-based oligonucleotide ligation assay,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 22, pp. 8923–8927, 1990. View at Publisher · View at Google Scholar · View at Scopus
  37. I. A. Beck, M. Mahalanabis, G. Pepper et al., “Rapid and sensitive oligonucleotide ligation assay for detection of mutations in human immunodeficiency virus type 1 associated with high-level resistance to protease inhibitors,” Journal of Clinical Microbiology, vol. 40, no. 4, pp. 1413–1419, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Barany, “The ligase chain reaction in a PCR world,” Genome Research, vol. 1, no. 1, pp. 5–16, 1991. View at Google Scholar · View at Scopus
  39. F. Barany, “Genetic disease detection and DNA amplification using cloned thermostable ligase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 1, pp. 189–193, 1991. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Khanna, W. Cao, M. Zirvi, P. Paty, and F. Barany, “Ligase detection reaction for identification of low abundance mutations,” Clinical Biochemistry, vol. 32, no. 4, pp. 287–290, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. H. H. Lee, “Ligase chain reaction,” Biologicals, vol. 24, no. 3, pp. 197–199, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Y. Wu and R. B. Wallace, “The ligation amplification reaction (LAR)-amplification of specific DNA sequences using sequential rounds of template-dependent ligation,” Genomics, vol. 4, no. 4, pp. 560–569, 1989. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Minamitani, S. Nishiguchi, T. Kuroki, S. Otani, and T. Monna, “Detection by ligase chain reaction of precore mutant of hepatitis B virus,” Hepatology, vol. 25, no. 1, pp. 216–222, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. V. D. Karthigesu, M. Mendy, M. Fortuin, H. C. Whittle, C. R. Howard, and L. M. C. Allison, “The ligase chain reaction distinguishes hepatitis B virus S-gene variants,” FEMS Microbiology Letters, vol. 131, no. 2, pp. 127–132, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Osiowy, “Sensitive detection of HBsAG mutants by a gap ligase chain reaction assay,” Journal of Clinical Microbiology, vol. 40, no. 7, pp. 2566–2571, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Zirvi, T. Nakayama, G. Newman, T. McCaffrey, P. Paty, and F. Barany, “Ligase-based detection of mononucleotide repeat sequences,” Nucleic Acids Research, vol. 27, no. 24, pp. e40i–e40viii, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. C. A. Batt, P. Wagner, M. Wiedmann, and R. Gilbert, “Detection of bovine leukocyte adhesion deficiency by nonisotopic ligase chain reaction,” Animal Genetics, vol. 25, no. 2, pp. 95–98, 1994. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Abravaya, J. J. Carrino, S. Muldoon, and H. H. Lee, “Detection of point mutations with a modified ligase chain reaction (Gap-LCR),” Nucleic Acids Research, vol. 23, no. 4, pp. 675–682, 1995. View at Publisher · View at Google Scholar · View at Scopus
  49. V. L. Wilson, Q. Wei, K. R. Wade et al., “Needle-in-a-haystack detection and identification of base substitution mutations in human tissues,” Mutation Research, vol. 406, no. 2–4, pp. 79–100, 1999. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Niederhauser, L. Kaempf, and I. Heinzer, “Use of the ligase detection reaction-polymerase chain reaction to identify point mutations in extended-spectrum beta-lactamases,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 19, no. 6, pp. 477–480, 2000. View at Google Scholar · View at Scopus
  51. C. Bourgeois, N. Sixt, J. B. Bour, and P. Pothier, “Value of a ligase chain reaction assay for detection of ganciclovir resistance-related mutation 594 in UL97 gene of human cytomegalovirus,” Journal of Virological Methods, vol. 67, no. 2, pp. 167–175, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Szemes, P. Bonants, M. de Weerdt, J. Baner, U. Landegren, and C. D. Schoen, “Diagnostic application of padlock probes-multiplex detection of plant pathogens using universal microarrays,” Nucleic Acids Research, vol. 33, no. 8, article e70, 2005. View at Google Scholar · View at Scopus
  53. M. Nilsson, H. Malmgren, M. Samiotaki, M. Kwiatkowski, B. P. Chowdhary, and U. Landegren, “Padlock probes: circularizing oligonucleotides for localized DNA detection,” Science, vol. 265, no. 5181, pp. 2085–2088, 1994. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Nilsson, K. Krejci, J. Koch, M. Kwiatkowski, P. Gustavsson, and U. Landegren, “Padlock probes reveal single-nucleotide differences, parent of origin and in situ distribution of centromeric sequences in human chromosomes 13 and 21,” Nature Genetics, vol. 16, no. 3, pp. 252–255, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. D.-O. Antson, M. Mendel-Hartvig, U. Landegren, and M. Nilsson, “PCR-generated padlock probes distinguish homologous chromosomes through quantitative fluorescence analysis,” European Journal of Human Genetics, vol. 11, no. 5, pp. 357–363, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Fire and S.-Q. Xu, “Rolling replication of short DNA circles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 10, pp. 4641–4645, 1995. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Liu, S. L. Daubendiek, M. A. Zillman, K. Ryan, and E. T. Kool, “Rolling circle DNA synthesis: small circular oligonucleotides as efficient templates for DNA polymerases,” Journal of the American Chemical Society, vol. 118, no. 7, pp. 1587–1594, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. S. L. Daubendiek and E. T. Kool, “Generation of catalytic RNAs by rolling transcription of synthetic DNA nanocircles,” Nature Biotechnology, vol. 15, no. 3, pp. 273–277, 1997. View at Publisher · View at Google Scholar · View at Scopus
  59. P. M. Lizardi, X. Huang, Z. Zhu, P. Bray-Ward, D. C. Thomas, and D. C. Ward, “Mutation detection and single-molecule counting using isothermal rolling-circle amplification,” Nature Genetics, vol. 19, no. 3, pp. 225–232, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Banér, M. Nilsson, M. Mendel-Hartvig, and U. Landegren, “Signal amplification of padlock probes by rolling circle replication,” Nucleic Acids Research, vol. 26, no. 22, pp. 5073–5078, 1998. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Larsson, J. Koch, A. Nygren et al., “In situ genotyping individual DNA molecules by target-primed rolling-circle amplification of padlock probes,” Nature Methods, vol. 1, no. 3, pp. 227–232, 2004. View at Google Scholar · View at Scopus
  62. X.-B. Zhong, P. M. Lizardi, X.-H. Huang, P. L. Bray-Ward, and D. C. Ward, “Visualization of oligonucleotide probes and point mutations in interphase nuclei and DNA fibers using rolling circle DNA amplification,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 7, pp. 3940–3945, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. O. Söderberg, K.-J. Leuchowius, M. Gullberg et al., “Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay,” Methods, vol. 45, no. 3, pp. 227–232, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Margulies, M. Egholm, W. E. Altman et al., “Genome sequencing in microfabricated high-density picolitre reactors,” Nature, vol. 437, no. 7057, pp. 376–380, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. D. R. Bentley, “Whole-genome re-sequencing,” Current Opinion in Genetics & Development, vol. 16, no. 6, pp. 545–552, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. E. R. Mardis, “Next-generation DNA sequencing methods,” Annual Review of Genomics and Human Genetics, vol. 9, pp. 387–402, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Ronaghi, M. Uhlén, and P. Nyrén, “A sequencing method based on real-time pyrophosphate,” Science, vol. 281, no. 5375, pp. 363–365, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. O. Morozova and M. A. Marra, “Applications of next-generation sequencing technologies in functional genomics,” Genomics, vol. 92, no. 5, pp. 255–264, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Shendure, G. J. Porreca, N. B. Reppas et al., “Accurate multiplex colony sequencing of an evolved bacterial genome,” Science, vol. 309, no. 5741, pp. 1728–1732, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Shendure and H. Ji, “Next-generation DNA sequencing,” Nature Biotechnology, vol. 26, no. 10, pp. 1135–1145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. J. J. Dunn and F. W. Studier, “Nucleotide sequence from the genetic left end of bacteriophage T7 DNA to the beginning of gene 4,” Journal of Molecular Biology, vol. 148, no. 4, pp. 303–330, 1981. View at Publisher · View at Google Scholar · View at Scopus
  72. D. E. Barnes, L. H. Johnston, K. I. Kodama, A. E. Tomkinson, D. D. Lasko, and T. Lindahl, “Human DNA ligase I cDNA: cloning and functional expression in Saccharomyces cerevisiae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 17, pp. 6679–6683, 1990. View at Google Scholar · View at Scopus
  73. A. Kletzin, “Molecular characterisation of a DNA ligase gene of the extremely thermophilic archaeon Desulfurolobus ambivalens shows close phylogenetic relationship to eukaryotic ligases,” Nucleic Acids Research, vol. 20, no. 20, pp. 5389–5396, 1992. View at Publisher · View at Google Scholar · View at Scopus
  74. A. J. Doherty, S. R. Ashford, H. S. Subramanya, and D. B. Wigley, “Bacteriophage T7 DNA ligase: overexpression, purification, crystallization, and characterization,” The Journal of Biological Chemistry, vol. 271, no. 19, pp. 11083–11089, 1996. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Odell, V. Sriskanda, S. Shuman, and D. B. Nikolov, “Crystal structure of eukaryotic DNA ligase-adenylate illuminates the mechanism of nick sensing and strand joining,” Molecular Cell, vol. 6, no. 5, pp. 1183–1193, 2000. View at Publisher · View at Google Scholar · View at Scopus
  76. A. J. Doherty and T. R. Dafforn, “Nick recognition by DNA ligases,” Journal of Molecular Biology, vol. 296, no. 1, pp. 43–56, 2000. View at Publisher · View at Google Scholar · View at Scopus
  77. V. Sriskanda and S. Shuman, “Role of nucleotidyl transferase motif V in strand joining by Chlorella virus DNA ligase,” The Journal of Biological Chemistry, vol. 277, no. 12, pp. 9661–9667, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. D. Suck, “Common fold, common function, common origin?” Nature Structural & Molecular Biology, vol. 4, no. 3, pp. 161–165, 1997. View at Google Scholar · View at Scopus
  79. A. G. Murzin, “OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences,” The EMBO Journal, vol. 12, no. 3, pp. 861–867, 1993. View at Google Scholar · View at Scopus
  80. K. Håkansson, A. J. Doherty, S. Shuman, and D. B. Wigley, “X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes,” Cell, vol. 89, no. 4, pp. 545–553, 1997. View at Google Scholar · View at Scopus
  81. A. V. Cherepanov and S. de Vries, “Dynamic mechanism of nick recognition by DNA ligase,” European Journal of Biochemistry, vol. 269, no. 24, pp. 5993–5999, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. D. J. Kim, O. Kim, H.-W. Kim, H. S. Kim, S. J. Lee, and S. W. Suh, “ATP-dependent DNA ligase from Archaeoglobus fulgidus displays a tightly closed conformation,” Acta Crystallographica Section F: Structural Biology and Crystallization Communications, vol. 65, no. 6, pp. 544–550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. T. Petrova, E. Y. Bezsudnova, K. M. Boyko et al., “ATP-dependent DNA ligase from Thermococcus sp. 1519 displays a new arrangement of the OB-fold domain,” Acta Crystallographica Section F: Structural Biology and Crystallization Communications, vol. 68, no. 12, pp. 1440–1447, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. M. C. Cardoso, C. Joseph, H. P. Rahn, R. Reusch, B. Nadal-Ginard, and H. Leonhardt, “Mapping and use of a sequence that targets DNA ligase I to sites of DNA replication in vivo,” The Journal of Cell Biology, vol. 139, no. 3, pp. 579–587, 1997. View at Publisher · View at Google Scholar · View at Scopus
  85. C. Prigent, D. D. Lasko, K. Kodama, J. R. Woodgett, and T. Lindahl, “Activation of mammalian DNA ligase I through phosphorylation by casein kinase II,” The EMBO Journal, vol. 11, no. 8, pp. 2925–2933, 1992. View at Google Scholar · View at Scopus
  86. N. Keppetipola and S. Shuman, “Characterization of a thermophilic ATP-dependent DNA ligase from the euryarchaeon Pyrococcus horikoshii,” Journal of Bacteriology, vol. 187, no. 20, pp. 6902–6908, 2005. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Echols and M. F. Goodman, “Fidelity mechanisms in DNA replication,” Annual Review of Biochemistry, vol. 60, pp. 477–511, 1991. View at Google Scholar · View at Scopus
  88. Y. Wang, D. E. Prosen, L. Mei, J. C. Sullivan, M. Finney, and P. B. Vander Horn, “A novel strategy to engineer DNA polymerases for enhanced processivity and improved performance in vitro,” Nucleic Acids Research, vol. 32, no. 3, pp. 1197–1207, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Kuroita, H. Matsumura, N. Yokota et al., “Structural mechanism for coordination of proofreading and polymerase activities in archaeal DNA polymerases,” Journal of Molecular Biology, vol. 351, no. 2, pp. 291–298, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. B. H. Pheiffer and S. B. Zimmerman, “Polymer-stimulated ligation: enhanced blunt- or cohesive-end ligation of DNA or deoxyribooligonudcleotides by T4 DNA ugase in polymer solutions,” Nucleic Acids Research, vol. 11, no. 22, pp. 7853–7871, 1983. View at Publisher · View at Google Scholar · View at Scopus
  91. V. Sgaramella, J. H. van de Sande, and H. G. Khorana, “Studies on polynucleotides, C. A novel joining reaction catalyzed by the T4-polynucleotide ligase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 67, no. 3, pp. 1468–1475, 1970. View at Google Scholar · View at Scopus
  92. R. H. Wilson, S. K. Morton, H. Deiderick et al., “Engineered DNA ligases with improved activities in vitro,” Protein Engineering, Design & Selection, vol. 26, no. 7, pp. 471–478, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. A. Sugino, H. M. Goodman, H. L. Heyneker, J. Shine, H. W. Boyer, and N. R. Cozzarelli, “Interaction of bacteriophage T4 RNA and DNA ligases in joining of duplex DNA at base paired ends,” The Journal of Biological Chemistry, vol. 252, no. 11, pp. 3987–3994, 1977. View at Google Scholar · View at Scopus
  94. G. J. S. Lohman, S. Tabor, and N. M. Nichols, “DNA ligases,” in Current Protocols in Molecular Biology, vol. 94, chapter 3, unit 3.14, pp. 1–7, 2011. View at Google Scholar
  95. K. Harada and L. E. Orgel, “Unexpected substrate specificity of T4 DNA ligase revealed by in vitro selection,” Nucleic Acids Research, vol. 21, no. 10, pp. 2287–2291, 1993. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Goffin, V. Bailly, and W. G. Verly, “Nicks 3′ or 5′ to AP sites or to mispaired bases, and one-nucleotide gaps can be sealed by T4 DNA ligase,” Nucleic Acids Research, vol. 15, no. 21, pp. 8755–8771, 1987. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Luo, D. E. Bergstrom, and F. Barany, “Improving the fidelity of Thermus thermophilus DNA ligase,” Nucleic Acids Research, vol. 24, no. 15, pp. 3071–3078, 1996. View at Publisher · View at Google Scholar · View at Scopus
  98. W. A. Beard, S. J. Stahl, H.-R. Kim et al., “Structure/function studies of human immunodeficiency virus type 1 reverse transcriptase. Alanine scanning mutagenesis of an α-helix in the thumb subdomain,” The Journal of Biological Chemistry, vol. 269, no. 45, pp. 28091–28097, 1994. View at Google Scholar · View at Scopus
  99. L. J. Reha-Krantz, R. L. Nonay, and S. Stocki, “Bacteriophage T4 DNA polymerase mutations that confer sensitivity to the PPi analog phosphonoacetic acid,” Journal of Virology, vol. 67, no. 1, pp. 60–66, 1993. View at Google Scholar · View at Scopus
  100. L. J. Reha-Krantz and R. L. Nonay, “Motif A of bacteriophage T4 DNA polymerase: role in primer extension and DNA replication fidelity,” The Journal of Biological Chemistry, vol. 269, no. 8, pp. 5635–5643, 1994. View at Google Scholar · View at Scopus
  101. Q. Dong, W. C. Copeland, and T. S.-F. Wang, “Mutational studies of human DNA polymerase,” The Journal of Biological Chemistry, vol. 268, no. 32, pp. 24163–24174, 1993. View at Google Scholar
  102. W. C. Copeland, N. K. Lam, and T. S.-F. Wang, “Fidelity studies of the human DNA polymerase α. The most conserved region among α-like DNA polymerases is responsible for metal-induced infidelity in DNA synthesis,” The Journal of Biological Chemistry, vol. 268, no. 15, pp. 11041–11049, 1993. View at Google Scholar · View at Scopus
  103. M. Tanabe, S. Ishino, M. Yohda, K. Morikawa, Y. Ishino, and H. Nishida, “Structure-based mutational study of an archaeal DNA ligase towards improvement of ligation activity,” ChemBioChem, vol. 13, no. 17, pp. 2575–2582, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Tanabe, S. Ishino, Y. Ishino, and H. Nishida, “Mutations of Asp540 and the domain-connecting residues synergistically enhance Pyrococcus furiosus DNA ligase activity,” FEBS Letters, vol. 588, no. 2, pp. 230–235, 2014. View at Publisher · View at Google Scholar · View at Scopus
  105. E. F. Pettersen, T. D. Goddard, C. C. Huang et al., “UCSF Chimera—a visualization system for exploratory research and analysis,” Journal of Computational Chemistry, vol. 25, no. 13, pp. 1605–1612, 2004. View at Publisher · View at Google Scholar · View at Scopus