Table4A.CellBiochemicalActivitiesUsedinNaturalGeneticEngineering(...

http://shapiro.bsd.uchicago.edu/Table4A.CellBiochemicalActivitiesUse...

Table 4A. Cell Biochemical Activities Used in Natural Genetic Engineering (NGE) NGE activities
Endo- & exonucleases

Functions
Cleave nucleic acid chains or duplexes at interior (endo) or terminal (exo) positions

References
(Haber 1995; Khare and Eckert 2002; Gogarten and Hilario 2006; Calvin and Li 2008; Zhuang, Jiang et al. 2009; Wakamatsu, Kitamura et al. 2010; Barzel, Obolski et al. 2011; Schwartz and Heyer 2011; Cao 2012) (Pascal 2008; Vago, Leva et al. 2009; Vicens and Cech 2009; Yutin and Koonin 2009; Simsek, Brunet et al. 2011) (Goodman 2002; Fujii and Fuchs 2004; Livneh, Ziv et al. 2010; McHenry 2011; Nikitina, Tischenko et al. 2011; Werner and Grohmann 2011; Fijalkowska, Schaaper et al. 2012; Hsin and Manley 2012; Kwak, Fuda et al. 2013)

DNA & RNA ligases

Splice together 3 OH and 5 phosphate ends of nucleic acid chains Template-directed DNA and RNA polymerization; both precise and error-prone processes

DNA & RNA polymerases

Ribonucleotide and deoxyribonucleotide terminal transferases Reverse transcriptases

Template-independent addition of nucleotides to the 3 OH end of a nucleic acid chain

(Greider and Blackburn 1985; Greider and Blackburn 1987; Fowler and Suo 2006; Martin and Keller 2007; Motea and Berdis 2010)

Make a DNA strand complementary to an RNA template

(Varmus 1987; Zimmerly, Moran et al. 1999; Liu, Deora et al. 2002; Simon and Zimmerly 2008; Belfort, Curcio et al. 2011; Gladyshev and Arkhipova 2011) (Mohr, Matsuura et al. 2006; Rajkowitsch and Schroeder 2007; Kim, Jung et al. 2010; Martin 2010; Batisse, Guerrero et al. 2012) (Kowalczykowski 2000; Szekvolgyi and Nicolas 2010; White 2011; Grabarz, Barascu et al. 2012; Krejci, Altmannova et al. 2012)

RNA chaperones

Hold RNA molecules in position for reverse transcription or splicing Carry out the process of reciprocal exchange or [1] gene conversion between two homologous duplexes

Coordinated multiprotein homologous recombination (Rec) complexes

Coordinated multiprotein non-homologous end-joining (NHEJ) complexes

Join together the ends of two linear DNA molecules; generally involves processing the ends so they can be ligated together

(Pitcher, Wilson et al. 2005; van Gent and van der Burg 2007; Weterings and Chen 2008; Fattah, Lee et al. 2010; Mladenov and Iliakis 2011; Grabarz, Barascu et al. 2012)

Serine & tyrosine site-specific recombinases

Carry out reciprocal exchange between specific recombination sites by a series of single-strand DNA-protein [2] transesterifications

(Smith and Thorpe 2002; Poulter and Goodwin 2005; Hallet and Sherratt 2010; Rice, Mouw et al. 2010; Van Houdt, Leplae et al. 2012)

Transposases and integrases

Bind to specific sequences at the end of paired duplex regions to induce transient cleavages that are subsequently ligated into a target duplex to mobilize a segment of DNA

(Polard and Chandler 1995; Nowacki, Higgins et al. 2009; Aziz, Breitbart et al. 2010; Hallet and Sherratt 2010; Hickman, Chandler et al. 2010; Montano and Rice 2011; Yuan and Wessler 2011)

Homing endonucleases and inteins

Site-specific duplex endonucleases; sometimes encoded by self-splicing protein domains (inteins) Self-splicing type II introns capable of reversesplicing into RNA or DNA strains

(Gogarten, Senejani et al. 2002; Stoddard 2005; Dassa, London et al. 2009; Raghavan and Minnick 2009; Elleuche and Poggeler 2010; Marcaida, Munoz et al. 2010; Barzel, Naor et al. 2011; Taylor and Stoddard 2012) (Zimmerly, Guo et al. 1995; Eickbush 1999; Mohr, Smith et al. 2000; Dickson, Huang et al. 2001; Lambowitz and Zimmerly 2004; Mohr, Matsuura et al. 2006)

Retrosplicing introns

REFERENCES Aziz, R. K., M. Breitbart, et al. (2010). "Transposases are the most abundant, most ubiquitous genes in nature." Nucleic Acids Res 38(13): 4207-4217. http://www.ncbi.nlm.nih.gov/pubmed/20215432.

1 of 4

7/20/2013 2:04 PM

Table4A.CellBiochemicalActivitiesUsedinNaturalGeneticEngineering(...

http://shapiro.bsd.uchicago.edu/Table4A.CellBiochemicalActivitiesUse...

Barzel, A., A. Naor, et al. (2011). "Homing endonucleases residing within inteins: evolutionary puzzles awaiting genetic solutions." Biochem Soc Trans 39(1): 169-173. http://www.ncbi.nlm.nih.gov/pubmed/21265767. Barzel, A., U. Obolski, et al. (2011). "Home and away- the evolutionary dynamics of homing endonucleases." BMC Evol Biol 11: 324. http://www.ncbi.nlm.nih.gov/pubmed/22054298. Batisse, J., S. Guerrero, et al. (2012). "The role of Vif oligomerization and RNA chaperone activity in HIV-1 replication." Virus Res 169(2): 361-376. http://www.ncbi.nlm.nih.gov/pubmed/22728817. Belfort, M., M. J. Curcio, et al. (2011). "Telomerase and retrotransposons: reverse transcriptases that shaped genomes." Proc Natl Acad Sci U S A 108(51): 20304-20310. http://www.ncbi.nlm.nih.gov/pubmed/22187457. Calvin, K. and H. Li (2008). "RNA-splicing endonuclease structure and function." Cell Mol Life Sci 65(7-8): 1176-1185. http://www.ncbi.nlm.nih.gov/pubmed/18217203. Cao, W. (2012). "Endonuclease V: an unusual enzyme for repair of DNA deamination." Cell Mol Life Sci. http://www.ncbi.nlm.nih.gov/pubmed/23263163. Dassa, B., N. London, et al. (2009). "Fractured genes: a novel genomic arrangement involving new split inteins and a new homing endonuclease family." Nucleic Acids Res 37(8): 2560-2573. http://www.ncbi.nlm.nih.gov/pubmed /19264795. Dickson, L., H. R. Huang, et al. (2001). "Retrotransposition of a yeast group II intron occurs by reverse splicing directly into ectopic DNA sites." Proc Natl Acad Sci U S A 98(23): 13207-13212. http://www.ncbi.nlm.nih.gov/pubmed /11687644. Eickbush, T. H. (1999). "Mobile introns: retrohoming by complete reverse splicing." Curr Biol 9(1): R11-14. http://www.ncbi.nlm.nih.gov/pubmed/9889113. Elleuche, S. and S. Poggeler (2010). "Inteins, valuable genetic elements in molecular biology and biotechnology." Appl Microbiol Biotechnol 87(2): 479-489. http://www.ncbi.nlm.nih.gov/pubmed/20449740. Fattah, F., E. H. Lee, et al. (2010). "Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells." PLoS Genet 6(2): e1000855. http://www.ncbi.nlm.nih.gov/pubmed /20195511. Fijalkowska, I. J., R. M. Schaaper, et al. (2012). "DNA replication fidelity in Escherichia coli: a multi-DNA polymerase affair." FEMS Microbiol Rev 36(6): 1105-1121. http://www.ncbi.nlm.nih.gov/pubmed/22404288. Fowler, J. D. and Z. Suo (2006). "Biochemical, structural, and physiological characterization of terminal deoxynucleotidyl transferase." Chem Rev 106(6): 2092-2110. http://www.ncbi.nlm.nih.gov/pubmed/16771444. Fujii, S. and R. P. Fuchs (2004). "Defining the position of the switches between replicative and bypass DNA polymerases." Embo J 23(21): 4342-4352. http://www.ncbi.nlm.nih.gov/pubmed/15470496. Gladyshev, E. A. and I. R. Arkhipova (2011). "A widespread class of reverse transcriptase-related cellular genes." Proc Natl Acad Sci U S A 108(51): 20311-20316. http://www.ncbi.nlm.nih.gov/pubmed/21876125. Gogarten, J. P. and E. Hilario (2006). "Inteins, introns, and homing endonucleases: recent revelations about the life cycle of parasitic genetic elements." BMC Evol Biol 6: 94. http://www.ncbi.nlm.nih.gov/pubmed/17101053. Gogarten, J. P., A. G. Senejani, et al. (2002). "Inteins: structure, function, and evolution." Annu Rev Microbiol 56: 263-287. http://www.ncbi.nlm.nih.gov/pubmed/12142479. Goodman, M. (2002). "Error-prone repair DNA polymerases in prokaryotes and eukaryotes." Ann Rev Biochem 71: 17-50. http://www.ncbi.nlm.nih.gov/pubmed/12045089. Grabarz, A., A. Barascu, et al. (2012). "Initiation of DNA double strand break repair: signaling and single-stranded resection dictate the choice between homologous recombination, non-homologous end-joining and alternative end-joining." Am J Cancer Res 2(3): 249-268. http://www.ncbi.nlm.nih.gov/pubmed/22679557. Greider, C. W. and E. H. Blackburn (1985). "Identification of a specific telomere terminal transferase activity in Tetrahymena extracts." Cell 43(2 Pt 1): 405-413. http://www.ncbi.nlm.nih.gov/pubmed/3907856. Greider, C. W. and E. H. Blackburn (1987). "The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity." Cell 51(6): 887-898. http://www.ncbi.nlm.nih.gov/pubmed/3319189. Haber, J. E. (1995). "In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases." Bioessays 17(7): 609-620. http://www.ncbi.nlm.nih.gov/pubmed/7646483. Hallet, B. and D. J. Sherratt (2010). "Transposition and site-specific recombination: adapting DNA cut-and-paste mechanisms to a variety of genetic rearrangements." FEMS Microbiol Rev 21(2): 157-178. http://www.ncbi.nlm.nih.gov/pubmed/9348666. Hickman, A. B., M. Chandler, et al. (2010). "Integrating prokaryotes and eukaryotes: DNA transposases in light of structure." Crit Rev Biochem Mol Biol 45(1): 50-69. http://www.ncbi.nlm.nih.gov/pubmed/20067338%22. Hsin, J. P. and J. L. Manley (2012). "The RNA polymerase II CTD coordinates transcription and RNA processing." Genes Dev 26(19): 2119-2137. http://www.ncbi.nlm.nih.gov/pubmed/23028141. Khare, V. and K. A. Eckert (2002). "The proofreading 3'-->5' exonuclease activity of DNA polymerases: a kinetic barrier to translesion DNA synthesis." Mutat Res 510(1-2): 45-54. http://www.ncbi.nlm.nih.gov/pubmed/12459442. Kim, W. Y., H. J. Jung, et al. (2010). "The Arabidopsis U12-type spliceosomal protein U11/U12-31K is involved in U12 intron splicing via RNA chaperone activity and affects plant development." Plant Cell 22(12): 3951-3962. http://www.ncbi.nlm.nih.gov/pubmed/21148817. Kowalczykowski, S. C. (2000). "Initiation of genetic recombination and recombination-dependent replication." Trends Biochem Sci 25(4): 156-165. http://www.ncbi.nlm.nih.gov/pubmed/10754547. Krejci, L., V. Altmannova, et al. (2012). "Homologous recombination and its regulation." Nucleic Acids Res 40(13):

2 of 4

7/20/2013 2:04 PM

Table4A.CellBiochemicalActivitiesUsedinNaturalGeneticEngineering(...

http://shapiro.bsd.uchicago.edu/Table4A.CellBiochemicalActivitiesUse...

5795-5818. http://www.ncbi.nlm.nih.gov/pubmed/22467216. Kwak, H., N. J. Fuda, et al. (2013). "Precise maps of RNA polymerase reveal how promoters direct initiation and pausing." Science 339(6122): 950-953. http://www.ncbi.nlm.nih.gov/pubmed/23430654. Lambowitz, A. M. and S. Zimmerly (2004). "Mobile group II introns." Annu. Rev. Genet. 38: 1-35. http://www.ncbi.nlm.nih.gov/pubmed/15568970. Liu, M., R. Deora, et al. (2002). "Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage." Science 295(5562): 2091-2094. http://www.ncbi.nlm.nih.gov/pubmed/11896279. Livneh, Z., O. Ziv, et al. (2010). "Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis." Cell Cycle 9(4): 729-735. http://www.ncbi.nlm.nih.gov/pubmed/20139724. Marcaida, M. J., I. G. Munoz, et al. (2010). "Homing endonucleases: from basics to therapeutic applications." Cell Mol Life Sci 67(5): 727-748. http://www.ncbi.nlm.nih.gov/pubmed/19915993. Martin, G. and W. Keller (2007). "RNA-specific ribonucleotidyl transferases." Rna 13(11): 1834-1849. http://www.ncbi.nlm.nih.gov/pubmed/17872511. Martin, S. L. (2010). "Nucleic acid chaperone properties of ORF1p from the non-LTR retrotransposon, LINE-1." RNA Biol 7(6): 706-711. http://www.ncbi.nlm.nih.gov/pubmed/21045547. McHenry, C. S. (2011). "Bacterial replicases and related polymerases." Curr Opin Chem Biol 15(5): 587-594. http://www.ncbi.nlm.nih.gov/pubmed/21855395. Mladenov, E. and G. Iliakis (2011). "Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways." Mutat Res 711(1-2): 61-72. http://www.ncbi.nlm.nih.gov/pubmed /21329706. Mohr, G., D. Smith, et al. (2000). "Rules for DNA target-site recognition by a lactococcal group II intron enable retargeting of the intron to specific DNA sequences." Genes Dev 14(5): 559-573. http://www.ncbi.nlm.nih.gov /pubmed/10716944. Mohr, S., M. Matsuura, et al. (2006). "A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone." Proc Natl Acad Sci U S A 103(10): 3569-3574. http://www.ncbi.nlm.nih.gov /pubmed/16505350. Montano, S. P. and P. A. Rice (2011). "Moving DNA around: DNA transposition and retroviral integration." Curr Opin Struct Biol 21(3): 370-378. http://www.ncbi.nlm.nih.gov/pubmed/21439812. Motea, E. A. and A. J. Berdis (2010). "Terminal deoxynucleotidyl transferase: the story of a misguided DNA polymerase." Biochim Biophys Acta 1804(5): 1151-1166. http://www.ncbi.nlm.nih.gov/pubmed/19596089. Nikitina, T. V., L. I. Tischenko, et al. (2011). "Recent insights into regulation of transcription by RNA polymerase III and the cellular functions of its transcripts." Biol Chem 392(5): 395-404. http://www.ncbi.nlm.nih.gov/pubmed /21417954. Nowacki, M., B. P. Higgins, et al. (2009). "A functional role for transposases in a large eukaryotic genome." Science 324(5929): 935-938. http://www.ncbi.nlm.nih.gov/pubmed/19372392. Pascal, J. M. (2008). "DNA and RNA ligases: structural variations and shared mechanisms." Curr Opin Struct Biol 18(1): 96-105. http://www.ncbi.nlm.nih.gov/pubmed/18262407. Pitcher, R. S., T. E. Wilson, et al. (2005). "New insights into NHEJ repair processes in prokaryotes." Cell Cycle 4(5): 675-678. . Polard, P. and M. Chandler (1995). "Bacterial transposases and retroviral integrases." Mol Microbiol 15(1): 13-23. http://www.ncbi.nlm.nih.gov/pubmed/7752887. Poulter, R. T. and T. J. Goodwin (2005). "DIRS-1 and the other tyrosine recombinase retrotransposons." Cytogenet Genome Res 110(1-4): 575-588. http://www.ncbi.nlm.nih.gov/pubmed/16093711. Raghavan, R. and M. F. Minnick (2009). "Group I introns and inteins: disparate origins but convergent parasitic strategies." J Bacteriol 191(20): 6193-6202. http://www.ncbi.nlm.nih.gov/pubmed/19666710. Rajkowitsch, L. and R. Schroeder (2007). "Dissecting RNA chaperone activity." Rna 13(12): 2053-2060. http://www.ncbi.nlm.nih.gov/pubmed/17901153. Rice, P. A., K. W. Mouw, et al. (2010). "Orchestrating serine resolvases." Biochem Soc Trans 38(2): 384-387. http://www.ncbi.nlm.nih.gov/pubmed/20298188. Schwartz, E. K. and W. D. Heyer (2011). "Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes." Chromosoma 120(2): 109-127. http://www.ncbi.nlm.nih.gov /pubmed/21369956. Simon, D. M. and S. Zimmerly (2008). "A diversity of uncharacterized reverse transcriptases in bacteria." Nucleic Acids Res\ 36\(22\): 7219-7229\. http://www.ncbi.nlm.nih.gov/pubmed/19004871%22. Simsek, D., E. Brunet, et al. (2011). "DNA Ligase III Promotes Alternative Nonhomologous End-Joining during Chromosomal Translocation Formation." PLoS Genet 7(6): e1002080. http://www.ncbi.nlm.nih.gov/pubmed /21655080. Smith, M. C. and H. M. Thorpe (2002). "Diversity in the serine recombinases." Mol Microbiol 44(2): 299-307. http://www.ncbi.nlm.nih.gov/pubmed/11972771. Stoddard, B. L. (2005). "Homing endonuclease structure and function." Q Rev Biophys 38(1): 49-95. http://www.ncbi.nlm.nih.gov/pubmed/16336743. Szekvolgyi, L. and A. Nicolas (2010). "From meiosis to postmeiotic events: homologous recombination is obligatory but flexible." FEBS J 277(3): 571-589. http://www.ncbi.nlm.nih.gov/pubmed/20015080.

3 of 4

7/20/2013 2:04 PM

Table4A.CellBiochemicalActivitiesUsedinNaturalGeneticEngineering(...

http://shapiro.bsd.uchicago.edu/Table4A.CellBiochemicalActivitiesUse...

Taylor, G. K. and B. L. Stoddard (2012). "Structural, functional and evolutionary relationships between homing endonucleases and proteins from their host organisms." Nucleic Acids Res 40(12): 5189-5200. http://www.ncbi.nlm.nih.gov/pubmed/22406833. Vago, R., V. Leva, et al. (2009). "DNA ligase I and Nbs1 proteins associate in a complex and colocalize at replication factories." Cell Cycle 8(16): 2600-2607. http://www.ncbi.nlm.nih.gov/pubmed/19597347. van Gent, D. C. and M. van der Burg (2007). "Non-homologous end-joining, a sticky affair." Oncogene 26(56): 7731-7740. http://www.ncbi.nlm.nih.gov/pubmed/18066085. Van Houdt, R., R. Leplae, et al. (2012). "Towards a more accurate annotation of tyrosine-based site-specific recombinases in bacterial genomes." Mob DNA 3(1): 6. http://www.ncbi.nlm.nih.gov/pubmed/22502997. Varmus, H. (1987). "Reverse Transcription." Scientific American 257(3): 56-64. http://www.ncbi.nlm.nih.gov/pubmed /2443971. Vicens, Q. and T. R. Cech (2009). "A natural ribozyme with 3',5' RNA ligase activity." Nat Chem Biol\ 5\(2\): 97-99\. http://www.ncbi.nlm.nih.gov/pubmed/19125157%22. Wakamatsu, T., Y. Kitamura, et al. (2010). "Structure of RecJ exonuclease defines its specificity for single-stranded DNA." J Biol Chem 285(13): 9762-9769. http://www.ncbi.nlm.nih.gov/pubmed/20129927. Werner, F. and D. Grohmann (2011). "Evolution of multisubunit RNA polymerases in the three domains of life." Nat Rev Microbiol 9(2): 85-98. http://www.ncbi.nlm.nih.gov/pubmed/21233849. Weterings, E. and D. J. Chen (2008). "The endless tale of non-homologous end-joining." Cell Res 18(1): 114-124. http://www.ncbi.nlm.nih.gov/pubmed/18166980. White, M. F. (2011). "Homologous recombination in the archaea: the means justify the ends." Biochem Soc Trans 39(1): 15-19. http://www.ncbi.nlm.nih.gov/pubmed/21265740. Yuan, Y. W. and S. R. Wessler (2011). "The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies." Proc Natl Acad Sci U S A 108(19): 7884-7889. http://www.ncbi.nlm.nih.gov/pubmed/21518873. Yutin, N. and E. V. Koonin (2009). "Evolution of DNA ligases of Nucleo-Cytoplasmic Large DNA viruses of eukaryotes: a case of hidden complexity." Biol Direct 4: 51. http://www.ncbi.nlm.nih.gov/pubmed/20021668. Zhuang, J., G. Jiang, et al. (2009). "Exonuclease function of human Mre11 promotes deletional nonhomologous end joining." J Biol Chem 284(44): 30565-30573. http://www.ncbi.nlm.nih.gov/pubmed/19744924. Zimmerly, S., H. Guo, et al. (1995). "Group II intron mobility occurs by target DNA-primed reverse transcription." Cell 82(4): 545-554. http://www.ncbi.nlm.nih.gov/pubmed/7664334. Zimmerly, S., J. V. Moran, et al. (1999). "Group II intron reverse transcriptase in yeast mitochondria. Stabilization and regulation of reverse transcriptase activity by the intron RNA." J Mol Biol 289(3): 473-490. http://www.ncbi.nlm.nih.gov/pubmed/10356323. [1] Gene conversion occurs when only a small segment of one molecule is substituted for the corresponding region of the homologous molecule
without altering the linkages of flanking regions.

[2] The OH groups of a serine or tyrosine residue in the recombinase form a transient phosphodiester linkage with a DNA strand 5 phosphate
group.

4 of 4

7/20/2013 2:04 PM