Time-resolved synchrotron x-ray 'footprinting', a new approach to the study of nucleic acid structure and function: Application to Protein-DNA interactions and RNA folding

Journal of Molecular Biology

Volumn 266, Issue 1, 1997, Pages 144-159

  Sclavi, Bianca ^a   Woodson, Sarah ^b   Sullivan, Michael ^a   Chance, Mark R ^a   Brenowitz, Michael ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Footprinting; Kinetics; RNA folding; Synchrotron; X rays

Indexed keywords

HYDROXYL RADICAL; MAGNESIUM ION; PROTOZOAL RNA; RIBOZYME; SCAVENGER; THIOUREA;

ARTICLE; CONTROLLED STUDY; DNA FOOTPRINTING; IRRADIATION; LIGHT; MAGNET; NONHUMAN; NUCLEIC ACID STRUCTURE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; RNA STRUCTURE; STRUCTURE ACTIVITY RELATION; SYNCHROTRON; TETRAHYMENA THERMOPHILA; TITRIMETRY; X RAY;

EID: 0031566962     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0775     Document Type: Article

References (81)

1. Banerjee A. R., Turner D. H. The time dependence of chemical modification reveals slow steps in the folding of a group I ribozyme. Biochemistry. 34:1995;6504-6512.
2. Banerjee A. R., Jaeger J. A., Turner D. H. Thermal unfolding of a group I ribozyme: the low-temperature transition is primarily disruption of tertiary structure. Biochemistry. 32:1993;153-163.
3. Baskin J. S., Tullius T. D. Hydroxyl radical footprinting. Footprinting Techniques for Studying Nucleic Acid-Protein Complexe: A Volume of Separation, Detection, and Characterization of Biological Macromolecules. 1993;Academic Press, New York.
4. Beesk F., Dizdargoglu M., Schulte-Frohlinde D., von Sonntag C. Radiation-induced DNA strand breaks in deoxygenated aqueous solutions. The formation of altered sugars as end groups. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 36:1979;565-576.
5. Beyreuther K., Adler K., Geisler N., Klemm A. The amino-acid sequence of lac repressor. Proc. Natl Acad. Sci. USA. 70:1973;3576-3580.
6. Biagolow J. E. Ionizing radiation in mammalian cells. Farhatazis I., Rodgers M. A. Radiation Chemistry Principles & Applications. 1987;VCH Pubs, TX.
7. Brenowitz M., Jamison E. Modulation of the stability of a lac repressor mediated looped complex by temperature and ions: allosteric regulation by chloride. Biochemistry. 32:1993;8693-8701.
8. Brenowitz M., Senear D. F. DNase I footprint analysis of protein-DNA binding. Ausubel F. M., Brent R, Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. Current Protocols in Molecular Biology. 1989;John Wiley and Sons, New York.
9. Brenowitz M., Senear D. F., Shea M. A., Ackers G. K. Quantitative DNase footprint titration: a method for studying protein-DNA interactions. Methods. Enzymol. 130:1986;132-181.
10. Brenowitz M., Pickar A., Jamison E. The stability of a lac repressor mediated looped complex. Biochemistry. 30:1991;5986-5998.
11. Brenowitz M., Senear D. F., Jamison L., Dalma-Weiszhausz D. D. Quantitative DNase I footprinting. Revzin A. Footprinting Techniques for Studying Nucleic Acid-Protein Complexes A Volume of Separation, Detection, and Characterization of Biological Macromolecules.1993;Academic Press, New York.
12. Burkhoff A. M., Tullius T. D. The unusual conformation adopted by the adenine tracts in kinetoplast DNA. Cell. 48:1987;935-943.
13. Buxton G. V. Radiation chemistry of the liquid state: (1) water and homogeneous aqueous solutions. Farhatazis I., Rodgers M. A. Radiation Chemistry Principles & Applications.1987;VCH Pubs, TX.
14. Cate J. H., Gooding A. R., Podell E., Zhou K., Golden B. L., Kundrot C. E., Cech T. R., Doudna J. A. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science. 273:1996;1678-1685.
15. Cech T. R. Structure and mechanism of the large catalytic RNAs: group I and group II introns and ribonuclease. Gesteland R. F., Atkins J. F. The RNA World. 1993;Cold Spring Harbor Laboratory PressCold Spring Harbor, New York.
16. Cech T. R., Damberger S. H., Gutell R. R. Representation of the secondary and tertiary structure of group I introns. Nature. Struct. Biol. 1:1994;273-280.
17. Celander D. C., Cech T. R. Iron(II)-ethylenediaminetraacetic acid catalyzed cleavage of RNA and DNA oligonucleotides: similar reactivity toward single- and double-stranded forms. Biochemistry. 29:1990;1355-1361.
18. Celander D. C., Cech T. R. Visualizing the higher order folding of a catalytic RNA molecule. Science. 251:1991;401-407.
19. Christian E. L., Yarus M. Analysis of the role of phosphate oxygens in the group I intron from Tetrahymena. J. Mol. Biol. 228:1992;743-758.
20. Christian E. L., Yarus M. Metal coordination sites that contribute to structure and catalysis in the group I intron fromTetrahymena. Biochemistry. 32:1993;4475-4480.
21. Crothers D. M., Cole P. E., Hilbers C. W., Shulman R. G. The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA. J. Mol. Biol. 87:1974;63-88.
22. Dalma-Weiszhausz, D. D. 1995, The Escherichia coli gal operon: cross-talk between positive and negative regulation of transcription PhD. thesis, Albert Einstein College of Medicine, Bronx, NY.
23. Dixon W. J., Hayes J. J., Levin J. R., Weidner M. F., Dombroski B. A., Tullius T. D. Hydroxyl radical footprinting. Methods Enzymol. 208:1991;380-413.
24. Dizdaroglu M., Bergtold D. S. Characterization of free radical-induced base damage in DNA at biologically relevant levels. Anal. Biochem. 156:1986;182-188.
25. Doudna J. A., Cech T. R. Self-assembly of a group I intron active site from its component tertiary structural domains. RNA. 1:1995;36-45.
26. Duplaa A. M., Teoule R. Sites of gamma radiation-induced DNA strand breaks after alkali treatment. Int. J. Radiat. Biol. 48:1985;19-32.
27. Farabaugh P. J. Sequence of the lacI gene. Nature. 274:1978;765-769.
28. Farhatazis I., Rodgers M. A. Radiation Chemistry Principles & Applications.1987;VCH Pubs. TX.
29. Flor P. J., Flanegan J. B., Cech T. R. A conserved base-pair within the helix P4 of the Tetrahymena ribozyme helps to form the tertiary structure required for self-splicing. EMBO J. 8:1989;3391-3399.
30. Franchet-Beuzit J., Spotheim-Maurizot M., Sabattier R., Blazy-Baudras B., Charlier M. Radiolytic footprinting. B rays, γ photons and fast neutrons probe protein-DNA interactions. Biochemistry. 32:1993;2104-2110.
31. Galas D., Schmitz A. DNase footprinting: a simple method for the detection of protein-DNA binding specificity. Nucl. Acids Res. 5:1978;3157-3170.
32. Grosshans C. A., Cech T. R. Metal-ion requirements for sequence-specific endoribonuclease activity of the Tetrahymena ribozyme. Biochemistry. 28:1989;6888-6894.
33. Ha J. H., Capp M. W., Hohenwalter M. D., Baskerville M., Record M. T. Jr. Thermodynamic stoichiometries of participation of water, cations and anions in specific and non-specific binding of lac repressor to DNA. Possible thermodynamic origins of the "glutamate effect" on protein-DNA interactions. J. Mol. Biol. 228:1992;252-264.
34. Hayes J. J., Kam L., Tullius T. D. Footprinting protein-DNA complexes with gamma-rays. Methods Enzymol. 186:1990;545-549.
35. Heuer T. S., Chandry P. S., Belfort M., Celander D. W., Cech T. R. Folding of group I introns from bacteriophage T4 involves internalization of the catalytic core. Proc. Natl Acad. Sci. USA. 88:1991;11105-11109.
36. Hill A. V. The combination of hemoglobin with oxygen and with carbon monoxide. Biochem. J. 7:1913;471-480.
37. Hoshi M., Uehara S., Yamamotos O., Sawada S., Asao T., Kobayashi K., Maezawa H., Furusawa Y., Hieda K., Yamada T. Iron (II) sulphate (Fricke Solution) oxidation yields for 8.9 and 13.6 keV X-Rays from synchrotron radiation. Int. J. Radiat. Biol. 61:1992;21-27.
38. Hsieh M., Brenowitz M. Quantitative kinetics footprinting of protein-DNA association reactions. Methods Enzymol. 274:1996;478-492.
39. Hsieh M., Hensley P., Brenowitz M., Fetrow J. S. A molecular model of the inducer binding domain of the galactose repressor of Escherichia coli. J. Biol. Chem. 269:1994;13825-13835.
40. Joyce G. F., van der Horst G., Inoue T. Catalytic activity is retained in the Tetrahymena group I intron despite removal of the large extension of element P5. Nucl. Acids. Res. 17:1989;7879-7889.
41. King P. A., Anderson V. E., Edwards J. O., Gustafson G., Plumb R. C., Suggs J. W. A stable solid that generates hydroxyl radical upon dissolution in aqueous solutions: reaction with proteins and nucleic acid. J. Am. Chem. Soc. 114:1992;5430-5432.
42. King P. A., Jamison E., Strahs D., Anderson V. E., Brenowitz M. Footprinting of protein-DNA interactions using potassium peroxonitrite. Nucl. Acids Res. 21:1993;2473-2478.
43. Klassen N. V. Primary products in radiation chemistry. Farhatazis I., Rodgers M. A. Radiation Chemistry Principles & Applications. 1987;VCH Pubs. TX.
44. Kobayashi K. Radiobiology using synchrotron radiation. Proc. Enrico Fermi Inst. Phys. 1994;In the press.
45. Koblan K. S., Bain D. L., Beckett D., Shea M. A., Ackers G. K. Analysis of site-specific interaction parameters in protein-DNA complexes. Methods Enzymol. 210:1982;405-425.
46. Laggerbauer B., Murphy F. L., Cech T. R. Two major tertiary folding transitions of the Tetrahymena catalytic RNA. EMBO J. 13:1994;2699-2676.
47. Latham J. A., Cech T. R. Defining the inside and outside of a catalytic RNA molecule. Science. 245:1989;276-282.
48. Lewis M., Chang G., Horton N. C., Kercher M. A., Pace H. C., Schumacher M. A., Brennen R. G., Lu P. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science. 271:1996;1247-1254.
49. Michel F., Westhof E. Modeling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216:1990;585-610.
50. Michel F., Ellington A. D., Couture S., Szostak J. W. Phylogenetic and genetic evidence for base triples in the catalytic domain of group I introns. Nature. 347:1990;578-580.
51. Murphy F. L., Cech T. R. An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme. Biochemistry. 32:1993;5291-5300.
52. Murphy F. L., Cech T. R. GAAA tetraloop and conserved bulge stabilize tertiary structure of a group I intron domain. J. Mol. Biol. 236:1994;49-63.
53. Murphy F. L., Wang Y.-H., Griffith J. D., Cech T. R. Coaxially stacked RNA helices in the catalytic center of the Tetrahymena ribozyme. Science. 265:1994;1709-1712.
54. Petri V., Hsieh M., Brenowitz M. Thermodynamic and kinetic characterization of the binding of the TATA binding protein to the adenovirus E4 promoter. Biochemistry. 34:1995;9977-9984.
55. Price M. A., Tullius T. D. Using hydroxyl radical to probe DNA structure. Methods Enzymol. 212:1992;194-219.
56. Price M. A., Tullius T. D. How the structure of an adenine tract depends on sequence context: a new model for the structure of TnAn DNA sequences. Biochemistry. 32:1993;127-136.
57. Pyle A. M., Murphy F. L., Cech T. R. RNA substrate binding site in the catalytic core of the Tetrahymena ribozyme. Nature. 358:1992;123-128.
58. Revzin A. Footprinting Techniques for Studying Nucleic Acid-Protein Complexes:1993;Academic Press, New York.
59. Schmitz A., Galas D. The interaction of RNA polymerase and lac repressor with the lac control region. Nucl. Acids Res. 6:1979;111-137.
60. Schumacher M. A., Choi K. Y., Zalkin H., Brennen R. G. Crystal structure of LacI member PurR, bound to DNA: minor groove binding by α helices. Science. 266:1994;763-769.
61. Sclavi B., Newman J., Chance M. R., Brenowitz M. A new method for DNA footprinting by photolysis of methyl- and adenosyl-cobalamin bound to DNA. Biophys. J. 66:1994;A155.
62. Sclavi B., Chance M., Brenowitz M. New methods for time-resolved footprinting. Biophys. J. 68:1995;A296.
63. Sclavi B., Woodson S., Sullivan M., Chance M., Brenowitz M. The application of synchrotron X-ray radiation to the development of time resolved methods for the study of RNA folding. Biophys. J. 70:1996;A443.
64. Senear D. F., Bolen D. W. Simultaneous analysis for testing of models and parameter estimation. Methods Enzymol. 210:1992;463-481.
65. Shenoy G. K., Viccaro P. J., Mills D. M. Characteristics of the 7-GeV Advanced Photon Source : A Guide for Users. 1988;Argonne National Laboratory publication ANL-88-9.
66. Stelter L., Von Sonntag C., Schulte-Frohlinde D. Phosphate ester cleavage in ribose-5-phosphate induced by OH radicals in deoxygenated aqueous solution. The effect of Fe(II) and Fe(III) ions. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 29:1976;255-269.
67. Strahs D., Brenowitz M. Correlation of DNA conformational changes with the cooperative binding of cI-repressor of bacteriophage λ J. Mol. Biol. 244:1994;494-510.
68. Thirumalai D., Woodson S. A. Kinetics of folding of proteins and RNA. Acc. Chem. Res. 1996;In the press.
69. Tullius T. D., Dombroski B. A. Hydroxyl radical footprinting: high-resolution information about DNA-protein contacts and application to λ repressor and Cro protein. Proc. Natl Acad. Sci. USA. 83:1986;5469-5473.
70. Tullius T. D., Dombroski B. A., Churchill M. E., Kam L. Hydroxyl radical footprinting: a high resolution method for mapping protein-DNA contacts. Methods Enzymol. 155:1987;537-558.
71. van der Horst G., Christian A., Inoue T. Reconstitution of a group I intron self-splicing reaction with an activator RNA. Proc. Natl Acad. Sci. USA. 88:1991;184-188.
72. von Sonntag C. The Chemical Basis of Radiation Biology. 1987;Taylor and Francis, London.
73. von Sonntag C., Dizdaroglu M. The reaction of OH radicals with D-ribose in deoxygenated and oxygenated aqueous solution. Carbohydr. Res. 58:1977;21-30.
74. von Sonntag C., Schulte-Frohlinde D. Radiation-induced degradation of the sugar in model compounds and in DNA. Mol. Biol. Biochem. Biophys. 27:1978;204-226.
75. Wang J.-F., Cech T. R. Tertiary structure around the guanosine-binding site of the Tetrahymena ribozyme. Science. 256:1992;526-529.
76. Wang J.-F., Cech T. R. Metal ion dependence of active-site structure of the Tetrahymena ribozyme revealed by site-specific photo-cross-linking. J. Am. Chem. Soc. 116:1994;4178-4182.
77. Weickert M. J., Adhya S. A family of bacterial regulators homologous to gal and lac repressors. J. Biol. Chem. 267:1992;15869-15874.
78. Zarrinkar P. P., Williamson J. R. Kinetic intermediates in RNA folding. Science. 265:1994;918-924.
79. Zarrinkar P. P., Williamson J. R. The kinetic folding pathway of the Tetrahymena ribozyme reveals possible similarities between RNA and protein folding. Nature Struct. Biol. 3:1996a;432-438.
80. Zarrinkar P. P., Williamson J. R. The P9.1-P9.2 peripheral extension helps guide folding of the Tetrahymena ribozyme. Nucl. Acids Res. 24:1996b;854-858.
81. Zaug A. J., Grosshans C. A., Cech T. R. Sequence-specific endoribonuclease activity of the Tetrahymena ribozyme: enhanced cleavage of certain oligonucleotide substrates that form mismatched ribozyme-substrate complexes. Biochemistry. 27:1988;8924-8931.