An RNA toolbox for single-molecule force spectroscopy studies

Nucleic Acids Research

Volumn 35, Issue 19, 2007, Pages 6625-6639

  Vilfan, Igor D ^a   Kamping, Wiecher ^a   van den Hout, Michiel ^a   Candelli, Andrea ^a   Hage, Susanne ^a   Dekker, Nynke H ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DIVALENT CATION; NUCLEOTIDE; RIBONUCLEASE; RNA; SINGLE STRANDED DNA; SINGLE STRANDED RNA;

ACCURACY; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; GENETIC MANIPULATION; IMMOBILIZATION; MEDICAL RESEARCH; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN INTERACTION; RNA ANALYSIS; RNA DEGRADATION; RNA HYBRIDIZATION; RNA STRUCTURE; SPECTROSCOPY; THERMOSTABILITY;

OPTICAL TWEEZERS; RNA; RNA, DOUBLE-STRANDED; SPECTRUM ANALYSIS; TRANSCRIPTION, GENETIC;

EID: 36148970871     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm585     Document Type: Article

References (118)

1. Pennazio,S. and Roggero,P. (2000) Tobacco mosaic virus RNA as genetic determinant: Genesis of a discovery. Riv. Biol. Forum, 93, 431-455.
2. Domingo,E., Escarmis,C., Sevilla,N., Moya,A., Elena,S.F., Quer,J., Novella,I.S. and Holland,J.J. (1996) Basic concepts in RNA virus evolution. F ASEB J., 10, 859-864.
3. Domingo,E. and Holland,J.J. (1997) RNA virus mutations and fitness for survival. Annu. Rev. Microbiol., 51, 151-178.
4. Holland,J.J., Delatorre,J.C. and Steinhauer,D.A. (1992) RNA virus populations as quasi-species. Curr. Top. Microbiol. Immunol., 176, 1-20.
5. Volkin,E. and Astrachan,L. (1956) Phosphorus incorporation in Escherichia coli ribonucleic acid after infection with bacteriophage-T2. Virology, 2, 149-161.
6. Stahley,M.R. and Strobel,S.A. (2006) RNA splicing: Group I intron crystal structures reveal the basis of splice site selection and metal ion catalysis. Curr. Opin. Struct. Biol., 16, 319-326.
7. Weinger,J.S., Parnell,K.M., Dorner,S., Green,R. and Strobel,S.A. (2004) Substrate-assisted catalysis of peptide bond formation by the ribosome. Nat. Struct. Mol. Biol., 11, 1101-1106.
8. Moore,M.J. and Sharp,P.A. (1993) Evidence for 2 active-sites in the spliceosome provided by stereochemistry of premessenger RNA splicing. Nature, 30, 364-368.
9. Kazantsev,A.V. and Pace,N.R. (2006) Bacterial RNase P: A new view of an ancient enzyme. Nat. Rev. Microbiol., 4, 729-740.
10. Beebe,J.A. and Fierke,C.A. (1994) A kinetic mechanism for cleavage of precursor tRNA(asp) catalyzed by the RNA component of Bacillus-subtilis ribonuclease-P. Biochemistry, 33, 10294-10304.
11. Steitz,T.A. and Steitz,J.A. (1993) A general 2-metal-ion mechanism for catalytic RNA. Proc. Natl Acad. Sci. USA, 90, 6498-6502.
12. Smith,D. and Pace,N.R. (1993) Multiple magnesium-ions in the ribonuclease-P reaction-mechanism. Biochemistry, 32, 5273-5281.
13. Bergman,N.H., Johnston,W.K. and Bartel,D.P. (2000) Kinetic framework for ligation by an efficient RNA ligase ribozyme. Biochemistry, 39 3115-3123.
14. Birikh,K.R., Heaton,P.A. and Eckstein,F. (1997) The structure, function and application of the hammerhead ribozyme. Eur. J. Biochem., 245, 1-16.
15. Brimacombe,R. and Stiege,W. (1985) Structure and function of ribosomal-RNA. Biochem. J., 229, 1-17.
16. Serganov,A., Polonskaia,A., Phan,A.T.N., Breaker,R.R. and Patel,D.J. (2006) Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature, 441, 1167.
17. Winkler,W.C., Nahvi,A., Roth,A., Colhns,J.A. and Breaker,R.R. (2004) Control of gene expression by a natural metabolite-responsive ribozyme. Nature, 428, 281,
18. Ahlquist,P. (2002) RNA-dependent RNA polymerases, viruses, and RNA silencing. Science, 296, 1270-1273.
19. Fire,A., Xu,S., Montgomery,M.K., Kostas,S.A., Driver,S.E. and Mello,C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditìs elegans. Nature, 391, 806.
20. Haley,B. and Zamore,P.D. (2004) Kinetic analysis of the RNAi enzyme complex. Nat. Struct. Mol. Biol., 11, 599-606.
21. Hannon,J. (2002) RNA interference. Nature, 418 244-251.
22. McManus,M.T. and Sharp,P.A. (2002) Gene silencing in mammals by small interfering RNAs. Nat. Rev. Genet., 3, 737-747.
23. Charvin,G., Strick,T.R., Bensimon,D. and Croquette,V. (2005) Tracking topoisomerase, activity at the single-molecule level. Annu. Rev. Biophys. Biomol: Struct., 34, 201-219.
24. Williams,M.C., Rouzina,I. and Bloomfield,V.A. (2002) Thermodynamics of DNA interactions from single molecule stretching experiments. Acc. Chem. Res., 35, 159-166.
25. Williams,M.C., Wenner,J.R., Rouzina,I. and Bloomfield,V.A. (2001) Entropy and heat capacity of DNA melting from temperature dependence of single molecule stretching. Biophys. J., 80, 1932-1939.
26. Tamarat,P., Maali,A., Lounis,B. and Orrit,M. (2000) Ten years of single-molecule spectroscopy. J. Phys. Chem. A, 104, 1-16.
27. Hong,F. and Root,D.D. (2006) Downscaling functional bioassays by single-molecule techniques. Drug Discov. Today, 11, 640-645.
28. Skinner,G.M. and Visscher,K. (2004) Single-molecule techniques for drug discovery. Assay Drug Dev. Technol., 2, 397-405.
29. Mashanov,G.I. and Molloy,J.E. (2007) Automatic detection of single fluorophores in live cells. Biophys. J., 92, 2199-2211.
30. Sako,Y. and Uyemura,T. (2002) Total internal reflection fluorescence microscopy for single-molecule imaging in living cells. Cell Struct. Funct., 27, 357-365.
31. Sako,Y. and Yanagida,T. (2003) Single-molecule visualization in cell biology. Nat. Cell. Biol., SS1-SS5.
32. Abels,J.A., Moreno-Herrero,F., van der Heijden,T., Veenhuizen,P.T.M., Bruinink,M.M., Dekker,C. and Dekker,N.H. (2005) Single-molecule measurements of the persistence length of double-stranded RNA. Biophys. J., 88, 2737-2744.
33. Seol,Y., Skinner,G.M. and Visscher,K. (2004) Elastic properties of a single-stranded charged homopolymeric ribonucleotide. Phys. Rev. Lett., 93, Art. No. 118102.
34. Lambert,M.N., Vocker,E., Blumberg,S., Redemann,S., Gajraj,A., Meiners,J.C. and Walter,N.G. (2006) Mg2+-induced compaction of single RNA molecules monitored by tethered particle microscopy. Biophys. J. 90, 3672-3685.
35. Bokinsky,G., Rueda,D., Misra,V.K., Rhodes,M.M., Gordus,A., Babcock,H.P., Walter,N.G. and Zhuang,X.W. (2003) Single-molecule transition-state analysis of RNA folding. Proc. Natl Acad. Sci. USA, 100, 9302-9307.
36. Bokinsky,G. and Zhuang,X.W. (2005) Single-molecule RNA folding. Acc. Chem. Res., 38, 566-573.
37. Li,P.T.X., Bustamante,C. and Tinoco,I. (2006) Unusual mechanical stability of a minimal RNA kissing complex. Proc. Natl Acad. Sci. USA 103, 15847-15852.
38. Liphardt,J., Onoa,B., Smith,S.B., Tinoco,I. and Bustamante,C. (2001) Reversible unfolding of single RNA molecules by mechanical force. Science, 292, 733-737.
39. Mangeol,P., Cote,D., Bizebard,T., Legrand,O. and Bockelmann,U. (2006) Probing DNA and RNA single molecules with a double optical tweezer. Eur. Phys. J. E., 19, 311-317.
40. Onoa,B. and Tinoco,I. (2004) RNA folding and unfolding. Curr. Opin. Struct. Biol., 14, 374-379.
41. Pan,T. and Sosnick,T. (2006) RNA folding during transcription. Annu. Rev. Biophys. Biomol. Struct., 35, 161-175.
42. Tinoco,I., Li,P.T.X. and Bustamante,C. (2006) Determination of thermodynamics and kinetics of RNA reactions by force. Q. Rev. Biophys., 39, 325-360.
43. Zhuang,X.W. and Rief,M. (2003) Single-molecule folding. Curr. Opin. Struct. Biol., 13, 88-97.
44. Davenport,R.J., Wuite,G.J.L., Landick,R. and Bustamante,C. (2000) Single-molecule study of transcriptional pausing and arrest by E. coli RNA polymerase. Science, 287, 2497-2500.
45. Dumont,S., Cheng,W., Serebrov,V., Beran,R.K., Tinoco,I., Pyle,A.M. and Bustamante,C. (2006) RNA translocation and unwinding mechanism of HCVNS3 helicase and its coordination by ATP. Nature, 439, 105-108.
46. Henn,A., Medalia,O., Shi,H.P., Steinberg,M., Franceschi,F. and Sagi,I. (2001) Visualization of unwinding activity of duplex RNA by DbpA, a DEAD box helicase, at single-molecule resolution by atomic force microscopy. Proc. Natl Acad. Sci. USA, 98, 5007-5012.
47. Rueda,D., Bokinsky,G., Rhodes,M.M., Rust,M.J., Zhuang,X.W. and Walter,N.G. (2004) Single-molecule enzymology of RNA: Essential functional groups impact catalysis from a distance. Proc. Natl Acad. Sci. USA, 101, 10066-10071.
48. Yin,H., Wang,M.D., Svoboda,K., Landick,R., Block,S.M. and Gelles,J. (1995) Transcription against an applied force. Science, 270, 1653-1657.
49. Zhuang,X., Bartley,L.E., Babcock,H.P., Russell,R., Ha,T., Herschlag,D. and Chu,S. (2000) A single-molecule study of RNA catalysis and folding. Science, 288, 2048-2051.
50. Dekker,N.H., Abels,J.A., Veenhuizen,P.T.M., Bruinink,M.M. and Dekker,C. (2004) Joining of long double-stranded RNA molecules through controlled overhangs. Nucleic Acids Res., 32, Art. No. e140.
51. Stark,M.R., Pleiss,J.A., Deras,M., Scaringe,S.A. and Rader,S.D. (2006) An RNA ligase-mediated method for the efficient creation of large, synthetic RNAs. RNA-Publ. RNA Soc., 12, 2014-2019.
52. Walter,N.G. (2001) Structural dynamics of catalytic RNA highlighted by fluorescence resonance energy transfer. Methods, 25, 19-30.
53. Qin,P.Z.F. and Pyle,A.M. (1999) Site-specific labeling of RNA with fluorophores and other structural probes. Methods, 18, 60-70.
54. Ke,A. and Doudna,J.A. (2004) Crystallization of RNA and RNA-protein complexes. Methods, 34, 408-414.
55. Amitani,I., Baskin,R.J. and Kowalczykowski,S.C. (2006) Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. Mol. Cell, 23, 143-148.
56. Keyser,U.F., Koeleman,B.N., Van Dorp,S., Krapf,D., Smeets,R.M.M., Lemay,S.G., Dekker,N.H. and Dekker,C. (2006) Direct force measurements on DNA in a solid-state nanopore. Nat. Phys., 2, 473-477.
57. Yin,H., Landick,R. and Gelles,J. (1994) Tethered particle motion method for studying transcript elongation by a single RNA-polymerase molecule. Biophys. J., 67, 2468-2478.
58. Hartvig,L. and Christiansen,J. (1996) Intrinsic termination of T7 RNA polymerase mediated by either RNA or DNA. EMBO J., 15, 4767-4774.
59. He,B., Kukarin,A., Temiakov,D., Chin-Bow,S.T., Lyakhov,D.L., Rong,M.Q., Durbin,R.K. and McAllister,W.T. (1998) Characterization of an unusual, sequence-specific termination signal for T7 RNA polymerase. J. Biol. Chem., 273, 18802-18811.
60. Jeng,S.T., Gardner,J.F. and Gumport,R.I. (1990) Transcription termination by Bacteriophage T7 RNA polymerase at Rho-independent terminators. J. Biol. Chem., 265, 3823-3830.
61. Lyakhov,D.L., He,B., Zhang,X., Studier,F.W., Dunn,J.J. and McAllister,W.T. (1998) Pausing and termination by bacteriophage T7 RNA polymerase. J. Mol. Biol., 280, 201-213.
62. Macdonald,L.E., Durbin,R.K., Dunn,J.J. and McAllister,W.T. (1994) Characterization of 2 types of termination signal for bacteriophage T7 RNA polymerase. J. Mol. Biol., 238, 145-158.
63. Logel,J., Dill,D. and Leonard,S. (1992) Synthesis of cRNA probes from PCR-generated DNA. Biotechniques, 13, 604-610.
64. Melton,D.A., Krieg,P.A., Rebagliati,M.R., Maniatis,T., Zinn,K. and Green,M.R. (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage-SP6 promoter. Nucleic Acids Res., 12, 7035-7056.
65. Milligan,J.F., Groebe,D.R., Witherell,G.W. and Uhlenbeck,O.C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res., 15, 8783-8798.
66. Draper,D.E., White,S.A. and Kean,J.M. (1988) Preparation of specific ribosomal-RNA fragments. Method Enzymol., 164, 221-237.
67. Kholod,N., Vassilenko,K., Shlyapnikov,M., Ksenzenko,V. and Kisselev,L. (1998) Preparation of active tRNA gene transcripts devoid of 3′-extended products and dimers. Nucleic Acids Res., 26, 2500-2501.
68. Milligan,J.F. and Uhlenbeck,O.C. (1989) Determination of RNA-protein contacts using thiophosphate substitutions. Biochemistry, 28 2849-2855.
69. Donis-Keller,H. (1979) Site specific enzymatic cleavage of RNA. Nucleic Acids Res., 7, 179-192.
70. Lapham,J. and Crothers,D.M. (1996) RNase H1 cleavage for processing of in vitro transcribed RNA for NMR studies and RNA ligation. RNA, 2, 289-296.
71. Li,J. and Wartell,R.M. (1998) RNase H1 can catalyze RNA/DNA hybrid formation and cleavage with stable hairpin or duplex DNA oligomers. Biochemistry, 37, 5154-5161.
72. Lima,W.F. and Crooke,S.T. (1997) Cleavage of single strand RNA adjacent to RNA-DNA duplex regions by Escherichia coli RNase H1. J. Biol. Chem., 272, 27513-27516.
73. Yu,Y.T. and Steitz,J.A. (1997) A new strategy for introducing photoactivatable 4-thiouridine ((4S)U) into specific positions in a long RNA molecule. RNA, 3, 807-810.
74. Zamaratski,E., Pradeepkumar,P.I. and Chattopadhyaya,J. (2001) A critical survey of the structure-function of the antisense oligo/RNA heteroduplex as substrate for RNase H. J. Biochem. Biophys. Methods, 48, 189-208.
75. FerreDamare,A.R. and Doudna,J.A. (1996) Use of cis- and trans-ribozymes to remove 5′ and 3′ heterogeneities from milligrams of in vitro transcribed RNA. Nucleic Acids Res., 24, 977-978.
76. Walker,S.C., Avis,J.M. and Conn,G.L. (2003) General plasmids for producing RNA in vitro transcripts with homogeneous ends. Nucleic Acids Res., 31, Art. No. e82.
77. Wichlacz,A., Legiewicz,M. and Ciesiolka,J. (2004) Generating in vitro transcripts with homogenous 3′ ends using trans-acting antigenomic delta ribozyme. Nucleic Acids Res., 32, Art. No. e39.
78. Kao,C., Zheng,M. and Rudisser,S. (1999) A simple and efficient method to reduce nontemplated nucleotide addition at the 3′ terminus of RNAs transcribed by T7 RNA polymerase. RNA-Publ. RNA Soc., 5, 1268-1272.
79. Grunbergmanago,M. and Ochoa,S. (1955) Enzymatic synthesis and breakdown of polynucleotides - Polynucleotide phosphorylase. J. Am. Chem. Soc. 77, 3165-3166.
80. Grunbergmanago,M., Ortiz,P.J. and Ochoa,S. (1955) Enzymatic synthesis of nucleic acid-fike polynucleotides. Science, 122, 907-910.
81. Adami,R.C. and Rice,K.G. (1999) Metabolic stability of glutaraldehyde cross-linked peptide DNA condensates. J. Pharm. Sci., 88, 739-746.
82. Vanzi,F., Vladimirov,S., Knudsen,C.R., Goldman,Y.E. and Cooperman,B.S. (2003) Protein synthesis by single ribosomes. RNA-Publ. RNA Soc., 9, 1174-1179.
83. Zlatanova,J., Lindsay,S.M. and Leuba,S.H. (2000) Single molecule force spectroscopy in biology using the atomic force microscopy. Prog. Biophys. Mol. Biol., 74, 37-61.
84. Gore,J., Bryant,Z., Nollmann,M., Le,M.U., Cozzarelli,N.R. and Bustamante,C. (2006) DNA overwinds when stretched. Nature, 442 836-839.
85. Hansske,F. and Cramer,F. (1979) Modification of the 3′ terminus of tRNA by periodate oxidation and subsequent reaction with hydrazides. Meth. Enzymol., 59, 172-181.
86. Willkomm,D.K. and Hartmann,R.K. (2005) In Hartmann,R.K., Bindereif,A., Schön,A. and Westhof,E. (eds), Handbook of RN A Biochemistry, Vol. 1. Wiley-VCH GmbH &.Co. KGaA, Weinheim, pp. 86-94.
87. Bakin,A.V., Borisova,O.F., Shatsky,I.N. and Bogdanov,A.A. (1991) Spatial-organization of template polynucleotides on the ribosome determined by fluorescence methods. J. Mol. Biol., 221, 441-453.
88. Kinoshita,Y., Nishigaki,K. and Husimi,Y. (1997) Fluorescence-, isotope- or biotin-labeling of the 5′-end of single-stranded DNA/RNA using T4 RNA ligase. Nucleic Acids Res., 25, 3747-3748.
89. Martin,G. and Keller,W. (1998) Tailing and 3′-end labeling of RNA with yeast poly(A) polymerase and various nucleotides. RNA-Publ. RNA Soc. 4, 226-230.
90. Rosemeyer,V., Laubrock,A. and Seibl,R. (1995) Nonradioactive 3′-end labeling of RNA molecules of different lengths by terminal deoxynucleotidyltransferase. Anal. Biochem., 224, 446-449.
91. Green,N.H., Wilhams,P.M., Wahab,O., Davies,M.C., Roberts,C.J., Tendler,S.J.B. and Allen,S. (2004) Single-molecule investigations of RNA dissociation. Biophys. J., 86, 3811-3821.
92. Itakura,K., Rossi,J.J. and Wallace,R.B. (1984) Synthesis and use of synthetic oligonucleotides. Annu. Rev. Biochem., 53, 323-356.
93. Koster,D.A., Croquette,V., Dekker,C., Shuman,S. and Dekker,N.H. (2005) Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature, 434, 671-674.
94. Casey,J. and Davidson,N. (1977) Rates of formation and thermal stabilities of RNA-DNA and DNA-DNA duplexes at high concentrations of formamide. Nucleic Acids Res., 4, 1539-1552.
95. Bodkin,D.K. and Knudson,D.L. (1985) Assessment of sequence relatedness of double-stranded-RNA genes by RNA-RNA blot hybridization. J. Virol. Methods, 10, 45-52.
96. Bolton,E.T. and McCarthy,B.J. (1962) A general method for isolation of RNA complementary to DNA. Proc. Natl Acad. Sci. USA, 48, 1390-1397.
97. McConaug,BL., Laird,C.D. and McCarthy,B.J. (1969) Nucleic acid reassociation in formamide. Biochemistry, 8, 3289-3295.
98. Butzow,J.J. and Eichhorn,G.L. (1975) Different susceptibility of DNA znd RNA to cleavage by metal ions. Nature, 254, 358-359.
99. Eichhorn,G.L., Clark,P. and Tarian,E. (1969) Interaction of metal ions with polynucleotides; and related compounds.13. Effect of metal ions on enzymatic degradation of ribonucleic acid by bovine pancreatic ribonuclease and of deoxyribonicleic acid by bovine pancreatic deoxyribonuclease I. J. Biol. Chem., 244, 937-942.
100. Kaga,E., Nakagomi,O. and Uesugi,S. (1992) Thermal degradation of RNA-RNA hybrids during hybridization in solution. Mol. Cell. Probes, 6 261-264.
101. Tenhunen,J. (1989) Hydrolysis of single-stranded RNA in aqueous solutions - Effect on quantitative hybridizations. Mol. Cell. Probes 3, 391-396.
102. Dammer,U., Hegner,M., Anselmetti,D., Wagner,P., Dreier,M., Huber,W. and Guntherodt,H.J. (1996) Specific antigen/antibody interactions measured by force microscopy. Biophys. J., 70, 2437-2441.
103. Lee,G.U., Kidwell,D.A. and Colton,R.J. (1994) Sensing discrete streptavidin biotin interactions with atomic force microscopy. Langmuir, 10, 354-357.
104. Moy,V.T., Florin,E.L. and Gaub,H.E. (1994) Intermolecular forces and energies between ligands and receptors. Science, 266, 257-259.
105. Pincet,F. and Husson,J. (2005) The solution to the streptavidinbiotin paradox: The influence of history on the strength of single molecular bonds. Biophys. J., 89, 4374-4381.
106. Merkel,R., Nassoy,P., Leung,A., Ritchie,K. and Evans,E. (1999) Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature, 397, 50-53.
107. Persson,T., Willkomm,D.K. and Hartmann,R.K. (2005) In Hartmann,R.K., BindereifA., Schön,A. and Westhof,E. (eds), Handbook of RNA Biochemistry, Vol. 1. Wiley-VCH GmbH & Co. KGaA, Weinheim, pp. 53-74.
108. Sugino,A., Goodman,H.M., Heyneker,H.L., Shine,J., Boyer,H.W. and Cozzarelli,N.R. (1977) Interaction of Bacteriophage T4 RNA and DNA hgases in joining of duplex DNA at base-paired ends. J. Biol. Chem. 252, 3987-3994.
109. Bain,J.D. and Switzer,C. (1992) Regioselective ligation of oligoribonucleotides using DNA splints. Nucleic Acids Res., 20 4372.
110. Kurschat,W.C., Muller,J., Wombacher,R. and Helm,M. (2005) Optimizing splinted ligation of highly structured small RNAs. RNA-Publ. RNA Soc. 11, 1909-1914.
111. Moore,M.J. and Query,C.C. (2000) Joining of RNAs by splinted ligation. Methods in Enzymology, 317, 109-123.
112. Nandakumar,J., Ho,C.K., Uma,C.D. and Shuman,S. (2004) RNA substrate specificity and structure-guided mutational analysis of bacteriophage 14 RNA ligase 2. J. Biol. Chem., 279, 31337 31347.
113. Nishigaki,K., Taguchi,K., Kinoshita,Y., Aita,T. and Husimi,Y. (1998) Y-ligation: An efficient method for ligating single-stranded DNAs and RNAs with T4 RNA ligase. Mol. Divers., 4, 187-190.
114. Strick,T.R., Allemand,J.F., Bensimon,D., Bensimon,A. and Croquette,V. (1996) The elasticity of a single supercoiled DNA molecule. Science 271, 1835-1837.
115. Bullard,D.R. and Bowater,R.P. (2006) Direct comparison of nick-joining activity of the nucleic acid ligases from bacteriophage T4. Biochem. J., 398, 135-144.
116. Shapiro,D.J. (1981) Quantitative ethanol precipitation of nanogram quantities of DNA and RNA. Anal. Biochem., 110, 229-231.
117. Wu,W. and Welsh,M.J. (1995) A method for purification of DNA species by high-speed centrifugation of agarose gel slices. Anal. Biochem., 229, 350-352.
118. Yaphe,W. (1957) The use of agarase from Pseudomonas atlantica the identification of agar in marine algae (Rhodophyceae). Can. J. Microbiol., 3, 987-993.