Home LiteratureArticle Details
PMID: 11711436 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Octamerization of lambda CI repressor is needed for effective repression of P(RM) and efficient switching from lysogeny.

Genes & development ·Vol. 15 ·No. 22 ·2001-11-15 ·Pages 3013-22

Dodd IB, Perkins AJ, Tsemitsidis D, Egan JB

Abstract

The CI repressor of bacteriophage lambda is a model for the role of cooperativity in the efficient functioning of genetic switches. Pairs of CI dimers interact to cooperatively occupy adjacent operator sites at O(R) and at O(L). These CI tetramers repress the lytic promoters and activate transcription of the cI gene from P(RM). CI is also able to octamerize, forming a large DNA loop between O(R) and O(L), but the physiological role of this is unclear. Another puzzle is that, although a dimer of CI is able to repress P(RM) by binding to the third operator at O(R), O(R)3, this binding seems too weak to affect CI production in the lysogenic state. Here we show that repression of P(RM) at lysogenic CI concentrations is absolutely dependent on O(L), in this case 3.8 kb away. A mutant defective in this CI negative autoregulation forms a lysogen with elevated CI levels that cannot efficiently switch from lysogeny to lytic development. Our results invalidate previous evidence that Cro binding to O(R)3 is important in prophage induction. We propose the octameric CI:O(R)-O(L) complex increases the affinity of CI for O(R)3 by allowing a CI tetramer to link O(R)3 and the third operator at O(L), O(L)3.

MeSH Terms
Bacteriophage lambda/metabolism Base Sequence Blotting, Western DNA/metabolism DNA-Binding Proteins/metabolism Dimerization Dose-Response Relationship, Drug Dose-Response Relationship, Radiation Genes, Reporter Kinetics Lac Operon Lysogeny Models, Biological Molecular Sequence Data Mutation Oxygen/metabolism Plasmids/metabolism Promoter Regions, Genetic Protein Binding Repressor Proteins/chemistry,metabolism Time Factors Transcription, Genetic Ultraviolet Rays Viral Proteins Viral Regulatory and Accessory Proteins
Chemicals
DNA-Binding Proteins Repressor Proteins Viral Proteins Viral Regulatory and Accessory Proteins phage repressor proteins DNA Oxygen
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Dodd I B
Department of Molecular Biosciences, University of Adelaide, South Australia 5005, Australia. ian.dodd@adelaide.edu.au
Perkins A J
Tsemitsidis D
Egan J B
References (30)
30 references, click to expand
  1. Bacteriophage lambda: alive and well and still doing its thing.
    Curr Opin Microbiol. 2001 Apr;4(2):201-7 PMID: 11282477
  2. Cooperativity: action at a distance in a classic system.
    Curr Biol. 2000 Oct 5;10(19):R704-7 PMID: 11050405
  3. Inactivation of prophage lambda repressor in vivo.
    J Mol Biol. 1979 Jul 5;131(3):553-72 PMID: 159955
  4. Gene regulation at the right operator (OR) bacteriophage lambda. I. OR3 and autogenous negative control by repressor.
    J Mol Biol. 1980 May 15;139(2):147-61 PMID: 6447794
  5. Gene regulation at the right operator (OR) of bacteriophage lambda. II. OR1, OR2, and OR3: their roles in mediating the effects of repressor and cro.
    J Mol Biol. 1980 May 15;139(2):163-94 PMID: 6447795
  6. Gene regulation at the right operator (OR) of bacteriophage lambda. III. lambda repressor directly activates gene transcription.
    J Mol Biol. 1980 May 15;139(2):195-205 PMID: 6447796
  7. lambda Repressor and cro--components of an efficient molecular switch.
    Nature. 1981 Nov 19;294(5838):217-23 PMID: 6457992
  8. Autodigestion of lexA and phage lambda repressors.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1375-9 PMID: 6231641
  9. Cooperative binding of lambda repressors to sites separated by integral turns of the DNA helix.
    Cell. 1986 Mar 14;44(5):681-7 PMID: 3948245
  10. Quantitative DNase footprint titration: a method for studying protein-DNA interactions.
    Methods Enzymol. 1986;130:132-81 PMID: 3773731
  11. Improved single and multicopy lac-based cloning vectors for protein and operon fusions.
    Gene. 1987;53(1):85-96 PMID: 3596251
  12. Interaction at a distance between lambda repressors disrupts gene activation.
    Nature. 1988 Nov 24;336(6197):353-7 PMID: 2973565
  13. Analysis of the sequence-specific interactions between Cro repressor and operator DNA by systematic base substitution experiments.
    Proc Natl Acad Sci U S A. 1989 Jan;86(2):439-43 PMID: 2911590
  14. Lambda repressor recognizes the approximately 2-fold symmetric half-operator sequences asymmetrically.
    Proc Natl Acad Sci U S A. 1989 Sep;86(17):6513-7 PMID: 2771938
  15. Improved vector system for constructing transcriptional fusions that ensures independent translation of lacZ.
    J Bacteriol. 1990 Feb;172(2):1077-84 PMID: 2137119
  16. Carboxy-terminal determinants of intracellular protein degradation.
    Genes Dev. 1990 Feb;4(2):277-86 PMID: 2186965
  17. Theoretical and experimental analysis of the phage lambda genetic switch implies missing levels of co-operativity.
    J Theor Biol. 1990 Aug 9;145(3):295-318 PMID: 2146446
  18. The primary self-assembly reaction of bacteriophage lambda cI repressor dimers is to octamer.
    Biochemistry. 1993 Jun 22;32(24):6179-89 PMID: 8512927
  19. Rapid confirmation of single copy lambda prophage integration by PCR.
    Nucleic Acids Res. 1994 Dec 25;22(25):5765-6 PMID: 7838735
  20. Rapid bacterial permeabilization reagent useful for enzyme assays.
    Biotechniques. 1995 Jul;19(1):18-20 PMID: 7669288
  21. A versatile low-copy-number cloning vector derived from plasmid F.
    Gene. 1995 Oct 16;164(1):55-8 PMID: 7590321
  22. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements.
    Nucleic Acids Res. 1997 Mar 15;25(6):1203-10 PMID: 9092630
  23. Initiation and velocity of chromosome replication in Escherichia coli B/r and K-12.
    J Bacteriol. 1998 Jan;180(2):265-73 PMID: 9440515
  24. Four dimers of lambda repressor bound to two suitably spaced pairs of lambda operators form octamers and DNA loops over large distances.
    Curr Biol. 1999 Feb 11;9(3):151-4 PMID: 10021390
  25. Robustness of a gene regulatory circuit.
    EMBO J. 1999 Aug 2;18(15):4299-307 PMID: 10428968
  26. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells.
    Science. 2000 Mar 3;287(5458):1652-5 PMID: 10698740
  27. Engineering stability in gene networks by autoregulation.
    Nature. 2000 Jun 1;405(6786):590-3 PMID: 10850721
  28. Crystal structure of the lambda repressor C-terminal domain provides a model for cooperative operator binding.
    Cell. 2000 Jun 23;101(7):801-11 PMID: 10892750
  29. Coupled energetics of lambda cro repressor self-assembly and site-specific DNA operator binding II: cooperative interactions of cro dimers.
    J Mol Biol. 2000 Sep 22;302(3):625-38 PMID: 10986123
  30. Computational studies of gene regulatory networks: in numero molecular biology.
    Nat Rev Genet. 2001 Apr;2(4):268-79 PMID: 11283699
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2001-11-15
Pages
3013-22
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC312832
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com