Exploring translocation of proteins on DNA by NMR

Journal of Biomolecular NMR

Volumn 51, Issue 3, 2011, Pages 209-219

  Marius Clore, G ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Direct transfer; Lineshape analysis; Paramagnetic relaxation enhancement; Protein DNA interactions; Sliding; Target search process; z Exchange spectroscopy

Indexed keywords

DNA;

ANALYTICAL PARAMETERS; DISSOCIATION; KINETICS; NUCLEAR MAGNETIC RESONANCE; PARAMAGNETIC RELAXATION ENHANCEMENT; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN TRANSPORT; REVIEW; ROTATION; SPECTROSCOPY; Z EXCHANGE SPECTROSCOPY;

BINDING SITES; DNA; DNA-BINDING PROTEINS; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN TRANSPORT; PROTEINS;

EID: 80755172250     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-011-9555-8     Document Type: Review

References (56)

1. FH Allain YM Yen JE Masse P Schultze T Dieckmann, et al. 1999 Solution structure of the HMG protein NHP6A and its interaction with DNA reveals the structural determinants for non-sequence-specific binding EMBO J 18 2563 2579 10.1093/emboj/18.9.2563 (Pubitemid 29213287)
2. OG Berg PH von Hippel 1985 Diffusion-controlled macromolecular interactions Annu Rev Biophys Biophys Chem 14 131 160 10.1146/annurev.bb.14. 060185.001023
3. OG Berg RB Winter PH von Hippel 1981 Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory Biochemistry 20 6929 6948 10.1021/bi00527a028
4. M Billeter YQ Qian G Otting M Muller W Gehring, et al. 1993 Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex J Mol Biol 234 1084 1093 10.1006/jmbi.1993.1661
5. PC Blainey G Luo SC Kou WF Mangel GL Verdine, et al. 2009 Nonspecifically bound proteins spin while diffusing along DNA Nat Struct Mol Biol 16 1224 1229 10.1038/nsmb.1716
6. N Bloembergen LO Morgan 1961 Proton relaxation times in paramagnetic solution J Chem Phys 34 842 850 1961JChPh..34..842B 10.1063/1.1731684
7. R Boelens RM Scheek JH van Boom R Kaptein 1987 Complex of lac repressor headpiece with a 14 base-pair lac operator fragment studied by two-dimensional nuclear amgnetic resonance J Mol Biol 193 213 216 10.1016/0022-2836(87)90638-3
8. VP Chuprina JA Rullmann RM Lamerichs JH van Boom R Boelens R Kaptein 1993 Structure of the complex of lac repressor headpiece and a 11 base-pair half-operator determined by nuclear magnetic resonance spectroscopy and restrained molecular dynamics J Mol Biol 234 446 462 10.1006/jmbi.1993.1598 (Pubitemid 23361213)
9. GM Clore 2008 Visualizing lowly-populated regions of the free energy landscape of macromolecular complexes by paramagnetic relaxation enhancement Mol Biosyst 4 1058 1069 10.1039/b810232e
10. GM Clore J Iwahara 2009 Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes Chem Rev 109 4108 4139 10.1021/cr900033p
11. M Deschamps ID Campbell 2006 Cooling overall spin temperature: protein NMR experiments optimized for longitudinal relaxation effects J Magn Reson 178 206 211 2006JMagR.178..206D 10.1016/j.jmr.2005.09.011 (Pubitemid 43107928)
12. M Doucleff GM Clore 2008 Global jumping and domain-specific intersegment transfer between DNA cognate sites of the multidomain transcription factor Oct-1 Proc Natl Acad Sci USA 105 13871 13876 2008PNAS..10513871D 10.1073/pnas. 0805050105
13. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium J Biomol NMR 4 727 734 10.1007/BF00404280
14. IJ Finkelstein ML Visnapuu EC Greene 2010 Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase Nature 468 983 987 2010Natur.468..983F 10.1038/nature09561
15. MP Foster DS Wuttke I Radhakrishnan DA Case JM Gottesfeld, et al. 1997 Domain packing and dynamics in the DNA complex of the N-terminal zinc fingers of TFIIIA Nat Struct Biol 4 605 608 10.1038/nsb0897-605 (Pubitemid 27323438)
16. J Gorman AJ Plys ML Visnapuu E Alani EC Greene 2010 Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice Nat Struct Mol Biol 17 932 938 10.1038/nsmb.1858
17. SE Halford JF Marko 2004 How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res 32 3040 3052 10.1093/nar/gkh624 (Pubitemid 39022995)
18. JR Huth CA Bewley MS Nissen JN Evans R Reeves, et al. 1997 The solution structure of an HMG-I(Y)-DNA complex defines a new architectural minor groove binding motif Nature Struct Biol 4 657 665 10.1038/nsb0897-657 (Pubitemid 27323449)
19. J Iwahara GM Clore 2006 Direct observation of enhanced translocation of a homeodomain between DNA cognate sites by NMR exchange spectroscopy J Am Chem Soc 128 404 405 10.1021/ja056786o (Pubitemid 43157521)
20. J Iwahara GM Clore 2006 Detecting transient intermediates in macromolecular binding by paramagnetic NMR Nature 440 1227 1230 2006Natur.440.1227I 10.1038/nature04673
21. J Iwahara GM Clore 2010 Structure-independent analysis of the breadth of the positional distribution of disordered groups in macromolecules from order parameters for long, variable-length vectors using NMR paramagnetic relaxation enhancement J Am Chem Soc 132 13346 13356 10.1021/ja1048187
22. J Iwahara DE Anderson EC Murphy GM Clore 2003 EDTA-derivatized deoxythymidine as a tool for rapid determination of protein binding polarity to DNA by intermolecular paramagnetic relaxation enhancement J Am Chem Soc 125 6634 6635 10.1021/ja034488q (Pubitemid 36667439)
23. J Iwahara CD Schwieters GM Clore 2004 Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule J Am Chem Soc 126 5879 5896 10.1021/ja031580d (Pubitemid 38621427)
24. J Iwahara CD Schwieters GM Clore 2004 Characterization of nonspecific protein-DNA interactions by 1H paramagnetic relaxation enhancement J Am Chem Soc 126 12800 12808 10.1021/ja046246b (Pubitemid 39372309)
25. J Iwahara M Zweckstetter GM Clore 2006 NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA Proc Natl Acad Sci USA 103 15062 15067 2006PNAS..10315062I 10.1073/pnas.0605868103 (Pubitemid 44583164)
26. 1H transverse paramagnetic relaxation enhancement measurements on macromolecules J Magn Reson 184 185 195 2007JMagR.184..185I 10.1016/j.jmr.2006.10.003 (Pubitemid 46177665)
27. CG Kalodimos AM Bonvin RK Salinas R Wechselberger R Boelens, et al. 2002 Plasticity in protein-DNA recognition: lac repressor interacts with its natural operator 01 through alternative conformations of its DNA-binding domain EMBO J 21 2866 2876 10.1093/emboj/cdf318 (Pubitemid 34670371)
28. CG Kalodimos N Biris AM Bonvin MM Levandoski M Guennuegues, et al. 2004 Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes Science 305 386 389 2004Sci...305..386K 10.1126/science.1097064 (Pubitemid 38938152)
29. Y Levy JN Onuchic PG Wolynes 2007 Fly-casting in protein-DNA binding: frustration between protein folding and electrostatics facilitates target recognition J Am Chem Soc 129 738 739 10.1021/ja065531n (Pubitemid 46183905)
30. JJ Love X Li DA Case K Giese R Grosschedl, et al. 1995 Structural basis for DNA bending by the architectural transcription factor LEF-1 Nature 376 791 795 1995Natur.376..791L 10.1038/376791a0
31. JJ Love X Li J Chung HJ Dyson PE Wright 2004 The LEF-1 high-mobility group domain undergoes a disorder-to-order transition upon formation of a complex with cognate DNA Biochemistry 43 8725 8734 10.1021/bi049591m (Pubitemid 38880043)
32. GT Montelione G Wagner 1989 2D chemical-exchange NMR spectroscopy by proton-detected heteronuclear correlation J Am Chem Soc 111 3096 3098 10.1021/ja00190a072
33. EC Murphy VB Zhurkin JM Louis G Cornilescu GM Clore 2001 Structural basis for SRY-dependent 46-X, Y sex reversal: modulation of DNA bending by a naturally occurring point mutation J Mol Biol 312 481 499 10.1006/jmbi.2001.4977 (Pubitemid 32928119)
34. K Ogata S Morikawa H Nakamura A Sekikawa T Inoue H Kanai A Sarai S Ishii Y Nishimura 1994 Solution structure of a specific DNA complex of the Myb DNA binding domain with cooperative recognition helices Cell 79 639 648 10.1016/0092-8674(94)90549-5 (Pubitemid 24363807)
35. JG Omichinski GM Clore O Schaad G Felsenfeld C Trainor, et al. 1993 NMR structure of a specific DNA complex of a Zn-containing DNA binding domain of GATA-1 Science 261 438 446 1993Sci...261..438O 10.1126/science.8332909 (Pubitemid 23276551)
36. JG Omichinski PV Pedone G Felsenfeld AM Gronenborn GM Clore 1997 The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode Nat Struct Biol 4 122 132 10.1038/nsb0297-122 (Pubitemid 27066387)
37. AD Riggs S Bourgeois M Cohn 1970 The lac repressor-operator interaction. 3. Kinetic studies J Mol Biol 53 401 417 10.1016/0022-2836(70)90074-4
38. D Sahu GM Clore J Iwahara 2007 TROSY-based z-exchange spectroscopy: application to the determination of the activation energy for intermolecular protein translocation between specific sites on different DNA molecules J Am Chem Soc 129 13232 13237 10.1021/ja074604f (Pubitemid 350058364)
39. I Solomon 1955 Relaxation processes in a system of two spins Phys Rev 99 559 565 1955PhRv...99..559S 10.1103/PhysRev.99.559
40. CA Spronk AM Bonvin PK Radha G Melacini R Boelens, et al. 1999 The solution structure of Lac repressor headpiece 62 complexed to a symmetrical lac operator Structure 7 1483 1492 10.1016/S0969-2126(00)88339-2 (Pubitemid 30007234)
41. R Stoll BM Lee EW Debler JH Laity IA Wilson, et al. 2007 Structure of the Wilms tumor suppressor protein zinc finger domain bound to DNA J Mol Biol 372 1227 1245 10.1016/j.jmb.2007.07.017 (Pubitemid 47374717)
42. Y Takayama GM Clore 2011 PNAS plus: Intra- and intermolecular translocation of the bi-domain transcription factor Oct1 characterized by liquid crystal and paramagnetic NMR Proc Natl Acad Sci USA 108 E169 E176 2011PNAS..108E.169T 10.1073/pnas.1100050108
43. Y Takayama D Sahu J Iwahara 2010 NMR studies of translocation of the Zif268 protein between its target DNA Sites Biochemistry 49 7998 8005 10.1021/bi100962h
44. A Toth-Petroczy I Simon M Fuxreiter Y Levy 2009 Disordered tails of homeodomains facilitate DNA recognition by providing a trade-off between folding and specific binding J Am Chem Soc 131 15084 15085 10.1021/ja9052784
45. V Tsui I Radhakrishnan PE Wright DA Case 2000 NMR and molecular dynamics studies of the hydration of a zinc finger-DNA complex J Mol Biol 302 1101 1117 10.1006/jmbi.2000.4108
46. V Tsui L Zhu TH Huang PE Wright DA Case 2000 Assessment of zinc finger orientations by residual dipolar coupling constants J Biomol NMR 16 9 21 10.1023/A:1008302430561 (Pubitemid 30114720)
47. PH von Hippel 2004 Completing the view of transcriptional regulation Science 305 350 352 10.1126/science.1101270 (Pubitemid 38938142)
48. PH von Hippel OG Berg 1989 Facilitated target location in biological systems J Biol Chem 264 675 678 (Pubitemid 19038039)
49. D Vuzman Y Levy 2010 DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail Proc Natl Acad Sci USA 107 21004 21009 2010PNAS..10721004V 10.1073/pnas.1011775107
50. D Vuzman A Azia Y Levy 2010 Searching DNA via a "Monkey Bar" mechanism: the significance of disordered tails J Mol Biol 396 674 684 10.1016/j.jmb.2009.11.056
51. D Vuzman M Polonsky Y Levy 2010 Facilitated DNA search by multidomain transcription factors: cross talk via a flexible linker Biophys J 99 1202 1211 10.1016/j.bpj.2010.06.007
52. MH Werner JR Huth AM Gronenborn GM Clore 1995 Molecular basis of human 46X, Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex Cell 81 705 714 10.1016/0092-8674(95)90532-4
53. DC Williams Jr M Cai GM Clore 2004 Molecular basis for synergistic transcriptional activation by Oct1 and Sox2 revealed from the solution structure of the 42-kDa Oct1 Sox2 Hoxb1-DNA ternary transcription factor complex J Biol Chem 279 1449 1457 10.1074/jbc.M309790200 (Pubitemid 38082673)
54. RB Winter OG Berg PH von Hippel 1981 Diffusion-driven mechanisms of protein translocation on nucleic acids. 3. The Escherichia coli lac repressor-operator interaction: kinetic measurements and conclusions Biochemistry 20 6961 6977 10.1021/bi00527a030 (Pubitemid 12185949)
55. DS Wuttke MP Foster DA Case JM Gottesfeld PE Wright 1997 Solution structure of the first three zinc fingers of TFIIIA bound to the cognate DNA sequence: determinants of affinity and sequence specificity J Mol Biol 273 183 206 10.1006/jmbi.1997.1291 (Pubitemid 27460224)
56. H Zhang D Zhao M Revington W Lee X Jia C Arrowsmith O Jardtzky 1994 The solution structures of the trp repressor-operator DNA complex J Mol Biol 239 592 614 10.1006/jmbi.1994.1317 (Pubitemid 24160285)