Direct demonstration and quantification of long-range DNA looping by the λ bacteriophage repressor

Nucleic Acids Research

Volumn 37, Issue 9, 2009, Pages 2789-2795

  Zurla, Chiara ^a   Manzo, Carlo ^a   Dunlap, David ^b   Lewis, Dale E A ^c   Adhya, Sankar ^c   Finzi, Laura ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; LAMBDA REPRESSOR PROTEIN; PLASMID DNA; TETRAMER; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; BACTERIOPHAGE LAMBDA; CONTROLLED STUDY; DNA CONTENT; DNA DETERMINATION; GENE MUTATION; GENE REPRESSION; MOLECULAR MODEL; MOLECULAR STABILITY; NONHUMAN; NUCLEIC ACID ANALYSIS; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; OPERATOR GENE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TETHERED PARTICLE MOTION TECHNIQUE; WILD TYPE;

BACTERIOPHAGE LAMBDA; BINDING SITES; DNA, VIRAL; NUCLEIC ACID CONFORMATION; OPERATOR REGIONS, GENETIC; REPRESSOR PROTEINS; THERMODYNAMICS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 66249111861     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp134     Document Type: Article

References (45)

1. Ptashne, M.C.P. (1986) A Genetic Switch: Gene Control and Phage Lambda. Cell Press, Cambridge, MA pp. 1.
2. Parisien, A., Allain, B., Zhang, J., Mandeville, R. and Lan, C.Q. (2008) Novel alternatives to antibiotics: Bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. J. Appl. Microbiol., 104, 1-13.
3. Waehler, R., Russell, S.J. and Curiel, D.T. (2007) Engineering targeted viral vectors for gene therapy. Nat. Rev. Genet., 8, 573-587.
4. Projan, S. (2004) Phage-inspired antibiotics? Nat. Biotechnol., 22, 167-168.
5. Barksdal, L. and Arden, S.B. (1974) Persisting bacteriophage infections, lysogeny, and phage conversions. Annu. Rev. Microbiol., 28, 265-299.
6. Boyd, E.F. and Brussow, H. (2002) Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol., 10, 521-529.
7. Wagner, P.L. and Waldor, M.K. (2002) Bacteriophage control of bacterial virulence. Infect. Immun., 70, 3985-3993.
8. Wagner, P.L. (2006) In Calender, R. (ed.), The Bacteriophages. Oxford University Press, New York, pp. 710-719.
9. Wagner, P.L., Livny, J., Neely, M.N., Acheson, D.W.K., Friedman, D.I. and Waldor, M.K. (2002) Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol. Microbiol., 44 957-970.
10. Wagner, P.L., Neely, M.N., Zhang, X.P., Acheson, D.W.K., Waldor, M.K. and Friedman, D.I. (2001) Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J. Bacteriol. 183, 2081-2085.
11. Bensing, B.A., Rubens, C.E. and Sullam, P.M. (2001) Genetic loci of Streptococcus mitis that mediate binding to human platelets. Infect. Immun., 69, 1373-1380.
12. Bensing, B.A., Siboo, I.R. and Sullam, P.M. (2001) Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect. Immun., 69, 6186-6192.
13. Ptashne, M. (2004) A Genetic Switch: Phage Lambda Revisited, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY pp. 11-29.
14. Maniatis, T. and Ptashne, M. (1973) Multiple Repressor Binding At Operators In Bacteriophage-Lambda - (Nuclease Protection Polynucleotide Sizing Pyrimidine Tracts Supercoils E-Coli). Proc. Natl Acad. Sci. USA, 70, 1531-1535.
15. Koblan, K.S. and Ackers, G.K. (1992) Site-specific enthalpic regulation of DNA-transcription at bacteriophage-lambda Or. Biochemistry, 31, 57-65.
16. Senear, D.F., Brenowitz, M., Shea, M.A. and Ackers, G.K. (1986) Energetics of cooperative protein DNA interactions - comparison between quantitative deoxyribonuclease footprint titration and filter binding. Biochemistry, 25, 7344-7354.
17. Meyer, B.J., Maurer, R. and Ptashne, M. (1980) Gene-regulation at the right operator (Or) of bacteriophage-lambda.2. Or1, Or2, and Or3 - their roles in mediating the effects of repressor and Cro. J. Mol. Biol. 139, 163-194.
18. Revet, B., von Wilcken-Bergmann, B., Bessert, H., Barker, A. and Muller-Hill, B. (1999) Four dimers of lambda repressor bound to two suitably spaced pairs of lambda operators form octamers and DNA loops over large distances. Curr. Biol., 9, 151-154.
19. Dodd, I.B., Perkins, A.J., Tsemitsidis, D. and Egan, J.B. (2001) Octamerization of lambda CI repressor is needed for effective repression of P-RM and efficient switching from lysogeny. Genes Dev., 15 3013-3022.
20. Dodd, I.B., Shearwin, K.E., Perkins, A.J., Burr, T., Hochschild, A. and Egan, J.B. (2004) Cooperativity in long-range gene regulation by the lambda CI repressor. Genes Dev., 18, 344-354.
21. Svenningsen, S.L., Costantino, N., Court, D.L. and Adhya, S. (2005) On the role of Cro in lambda prophage induction. Proc. Natl Acad. Sci. USA, 102, 4465-4469.
22. Bandyopadhyay, S., Mukhopadhyay, C. and Roy, S. (1996) Dimer-dimer interfaces of the lambda-repressor are different in liganded and free states. Biochemistry, 35, 5033-5040.
23. Bell, C.E. and Lewis, M. (2001) Crystal structure of the lambda repressor C-terminal domain octamer. J. Mol. Biol., 314, 1127-1136.
24. Senear, D.F., Laue, T.M., Ross, J.B.A., Waxman, E., Eaton, S. and Rusinova, E. (1993) The primary self-assembly reaction of bacteriophage-lambda Ci repressor dimers is to octamer. Biochemistry 32, 6179-6189.
25. Stayrook, S., Jaru-Ampornpan, P., Ni, J., Hochschild, A. and Lewis, M. (2008) Crystal structure of the lambda repressor and a model for pairwise cooperative operator binding. Nature, 452, 1022-1026.
26. Anderson, L.M. and Yang, H. (2008) DNA looping can enhance lysogenic CI transcription in phage lambda. Proc. Natl Acad. Sci. USA, 105 5827-5832.
27. Zurla, C., Franzini, A., Galli, G., Dunlap, D.D., Lewis, D.E.A., Adhya, S. and Finzi, L. (2006) Novel tethered particle motion analysis of CI protein-mediated DNA looping in the regulation of bacteriophage lambda. J. Phys.-Condens. Matter, 18, S225-S234.
28. Finzi, L. and Gelles, J. (1995) Measurement of lactose repressor-mediated loop formation and breakdown in single DNA-molecules. Science, 267, 378-380.
29. Nelson, P.C., Zurla, C., Brogioli, D., Beausang, J.F., Finzi, L. and Dunlap, D. (2006) Tethered particle motion as a diagnostic of DNA tether length. J. Phys. Chem. B, 110, 17260-17267.
30. Pouget, N., Dennis, C., Turlan, C., Grigoriev, M., Chandler, M. and Salome, L. (2004) Single-particle tracking for DNA tether length monitoring. Nucleic Acids Res., 32, e73.
31. Johnson, A.D., Meyer, B.J. and Ptashne, M. (1979) Interactions between DNA-bound repressors govern regulation by the lambdaphage repressor. Proc. Natl Acad. Sci. USA, 76, 5061-5065.
32. Maurer, R., Meyer, B.J. and Ptashne, M. (1980) Gene-regulation at the right operator (Or) of bacteriophage-lambda.1. Or3 and autogenous negative control by repressor. J. Mol. Biol., 139, 147-161.
33. Finzi, L. and Dunlap, D. (2003) Single-molecule studies of DNA architectural changes induced by regulatory proteins. Methods Enzymol., 370, 369-378.
34. Vanzi, F., Broggio, C., Sacconi, L. and Pavone, F.S. (2006) Lac repressor hinge flexibility and DNA looping: Single molecule kinetics by tethered particle motion. Nucleic Acids Res., 34, 3409-3420.
35. Bakk, A. and Metzler, R. (2004) In vivo non-specific binding of lambda CI and Cro repressors is significant. FEBS Lett., 563, 66-68.
36. Koblan, K.S. and Ackers, G.K. (1991) Energetics of subunit dimerization in bacteriophage-lambda CI repressor-linkage to protons, temperature, and KCL. Biochemistry, 30, 7817-7821.
37. Bakk, A. and Metzler, R. (2004) Nonspecific binding of the O-R repressors CI and Cro of bacteriophage lambda. J. Theor. Biol., 231, 525-533.
38. Rippe, K. (2001) Making contacts on a nucleic acid polymer. Trends Biochem. Sci., 26, 733-740.
39. Shimada, J. and Yamakawa, H. (1984) Ring-closure probabilities for twisted wormlike chains - applications to DNA. Macromolecules, 17, 689-698.
40. Strahs, D. and Brenowitz, M. (1994) DNA Conformational-changes associated with the cooperative binding of CI-repressor of bacteriophage-lambda to O-R. J. Mol. Biol., 244, 494-510.
41. Purohit, P.K. and Nelson, P.C. (2006) Effect of supercoiling on formation of protein-mediated DNA loops. Phys. Rev. E, 74.
42. Strick, T.R., Croquette, V. and Bensimon, D. (1998) Homologous pairing in stretched supercoiled DNA. Proc. Natl Acad. Sci. USA, 95, 10579-10583.
43. Wang, M.D., Yin, H., Landick, R., Gelles, J. and Block, S.M. (1997) Stretching DNA with optical tweezers. Biophys. J., 72, 1335-1346.
44. Little, J.W., Shepley, D.P. and Wert, D.W. (1999) Robustness of a gene regulatory circuit. EMBO J., 18, 4299-4307.
45. Press, W.H., Teukolsky, S. A., Vettering, W.T. and Flannery, B.P. (1992) Numerical Recipes in C. Cambridge University Press. Cambridge, U.K. Chapter 15.6, pp. 692-694.