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Crystal structure of the lambda repressor C-terminal domain provides a model for cooperative operator binding.

Bell CE, Frescura P, Hochschild A, Lewis M
Cell 101 801-11 (2000)
Cited: 86 times
EuropePMC logo PMID: 10892750

Abstract

Interactions between transcription factors bound to separate operator sites commonly play an important role in gene regulation by mediating cooperative binding to the DNA. However, few detailed structural models for understanding the molecular basis of such cooperativity are available. The c1 repressor of bacteriophage lambda is a classic example of a protein that binds to its operator sites cooperatively. The C-terminal domain of the repressor mediates dimerization as well as a dimer-dimer interaction that results in the cooperative binding of two repressor dimers to adjacent operator sites. Here, we present the x-ray crystal structure of the lambda repressor C-terminal domain determined by multiwavelength anomalous diffraction. Remarkably, the interactions that mediate cooperativity are captured in the crystal, where two dimers associate about a 2-fold axis of symmetry. Based on the structure and previous genetic and biochemical data, we present a model for the cooperative binding of two lambda repressor dimers at adjacent operator sites.

Reviews - 1f39 mentioned but not cited (1)

  1. Slicing a protease: structural features of the ATP-dependent Lon proteases gleaned from investigations of isolated domains. Rotanova TV, Botos I, Melnikov EE, Rasulova F, Gustchina A, Maurizi MR, Wlodawer A. Protein Sci. 15 1815-1828 (2006)

Articles - 1f39 mentioned but not cited (5)

  1. A comparative three-dimensional model of the carboxy-terminal domain of the lambda repressor and its use to build intact repressor tetramer models bound to adjacent operator sites. Chattopadhyaya R, Ghosh K. J. Struct. Biol. 141 103-114 (2003)
  2. Structure of a hyper-cleavable monomeric fragment of phage lambda repressor containing the cleavage site region. Ndjonka D, Bell CE. J. Mol. Biol. 362 479-489 (2006)
  3. Predicted binding site information improves model ranking in protein docking using experimental and computer-generated target structures. Maheshwari S, Brylinski M. BMC Struct. Biol. 15 23 (2015)
  4. Non-canonical LexA proteins regulate the SOS response in the Bacteroidetes. Sánchez-Osuna M, Cortés P, Lee M, Smith AT, Barbé J, Erill I. Nucleic Acids Res 49 11050-11066 (2021)
  5. Solving the molecular distance geometry problem with inaccurate distance data. Souza M, Lavor C, Muritiba A, Maculan N. BMC Bioinformatics 14 Suppl 9 S7 (2013)


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  1. Unconventional serine proteases: variations on the catalytic Ser/His/Asp triad configuration. Ekici OD, Paetzel M, Dalbey RE. Protein Sci. 17 2023-2037 (2008)
  2. Revisited gene regulation in bacteriophage lambda. Dodd IB, Shearwin KE, Egan JB. Curr. Opin. Genet. Dev. 15 145-152 (2005)
  3. Eukaryotic transcriptional regulatory complexes: cooperativity from near and afar. Ogata K, Sato K, Tahirov TH. Curr. Opin. Struct. Biol. 13 40-48 (2003)
  4. Bacteriophage lambda: alive and well and still doing its thing. Friedman DI, Court DL. Curr. Opin. Microbiol. 4 201-207 (2001)
  5. High local protein concentrations at promoters: strategies in prokaryotic and eukaryotic cells. Dröge P, Müller-Hill B. Bioessays 23 179-183 (2001)
  6. The bacteriophage lambda CI protein finds an asymmetric solution. Hochschild A, Lewis M. Curr. Opin. Struct. Biol. 19 79-86 (2009)
  7. Gene regulation at-a-distance in E. coli: new insights. Amouyal M. C. R. Biol. 328 1-9 (2005)
  8. Cooperativity: action at a distance in a classic system. Koudelka GB. Curr. Biol. 10 R704-7 (2000)

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  1. Directed evolution of a genetic circuit. Yokobayashi Y, Weiss R, Arnold FH. Proc. Natl. Acad. Sci. U.S.A. 99 16587-16591 (2002)
  2. Cooperativity in long-range gene regulation by the lambda CI repressor. Dodd IB, Shearwin KE, Perkins AJ, Burr T, Hochschild A, Egan JB. Genes Dev. 18 344-354 (2004)
  3. Octamerization of lambda CI repressor is needed for effective repression of P(RM) and efficient switching from lysogeny. Dodd IB, Perkins AJ, Tsemitsidis D, Egan JB. Genes Dev. 15 3013-3022 (2001)
  4. Crystal structure of LexA: a conformational switch for regulation of self-cleavage. Luo Y, Pfuetzner RA, Mosimann S, Paetzel M, Frey EA, Cherney M, Kim B, Little JW, Strynadka NC. Cell 106 585-594 (2001)
  5. Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. Shi K, Brown CK, Gu ZY, Kozlowicz BK, Dunny GM, Ohlendorf DH, Earhart CA. Proc. Natl. Acad. Sci. U.S.A. 102 18596-18601 (2005)
  6. Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Kovacikova G, Lin W, Skorupski K. Mol. Microbiol. 53 129-142 (2004)
  7. Structure of malonamidase E2 reveals a novel Ser-cisSer-Lys catalytic triad in a new serine hydrolase fold that is prevalent in nature. Shin S, Lee TH, Ha NC, Koo HM, Kim SY, Lee HS, Kim YS, Oh BH. EMBO J. 21 2509-2516 (2002)
  8. Crystal structure of the lambda repressor and a model for pairwise cooperative operator binding. Stayrook S, Jaru-Ampornpan P, Ni J, Hochschild A, Lewis M. Nature 452 1022-1025 (2008)
  9. Crystal structure of the lambda repressor C-terminal domain octamer. Bell CE, Lewis M. J. Mol. Biol. 314 1127-1136 (2001)
  10. Crystal structure of a novel viral protease with a serine/lysine catalytic dyad mechanism. Feldman AR, Lee J, Delmas B, Paetzel M. J. Mol. Biol. 358 1378-1389 (2006)
  11. Single-cell analysis of lambda immunity regulation. Baek K, Svenningsen S, Eisen H, Sneppen K, Brown S. J. Mol. Biol. 334 363-372 (2003)
  12. Converting a DNA damage checkpoint effector (UmuD2C) into a lesion bypass polymerase (UmuD'2C). Ferentz AE, Walker GC, Wagner G. EMBO J. 20 4287-4298 (2001)
  13. Multilevel autoregulation of λ repressor protein CI by DNA looping in vitro. Lewis D, Le P, Zurla C, Finzi L, Adhya S. Proc. Natl. Acad. Sci. U.S.A. 108 14807-14812 (2011)
  14. Enhancer-like long-range transcriptional activation by λ CI-mediated DNA looping. Cui L, Murchland I, Shearwin KE, Dodd IB. Proc. Natl. Acad. Sci. U.S.A. 110 2922-2927 (2013)
  15. Genomes and characterization of phages Bcep22 and BcepIL02, founders of a novel phage type in Burkholderia cenocepacia. Gill JJ, Summer EJ, Russell WK, Cologna SM, Carlile TM, Fuller AC, Kitsopoulos K, Mebane LM, Parkinson BN, Sullivan D, Carmody LA, Gonzalez CF, LiPuma JJ, Young R. J. Bacteriol. 193 5300-5313 (2011)
  16. RecA-dependent cleavage of LexA dimers. Giese KC, Michalowski CB, Little JW. J. Mol. Biol. 377 148-161 (2008)
  17. The structural basis of cooperative regulation at an alternate genetic switch. Pinkett HW, Shearwin KE, Stayrook S, Dodd IB, Burr T, Hochschild A, Egan JB, Lewis M. Mol. Cell 21 605-615 (2006)
  18. A tale of two repressors. Lewis M. J. Mol. Biol. 409 14-27 (2011)
  19. Entropy loss in long-distance DNA looping. Hanke A, Metzler R. Biophys. J. 85 167-173 (2003)
  20. Sequence recognition, cooperative interaction, and dimerization of the initiator protein DnaA of Streptomyces. Majka J, Zakrzewska-Czerwiñska J, Messer W. J. Biol. Chem. 276 6243-6252 (2001)
  21. Cleavage of bacteriophage lambda cI repressor involves the RecA C-terminal domain. Galkin VE, Yu X, Bielnicki J, Ndjonka D, Bell CE, Egelman EH. J. Mol. Biol. 385 779-787 (2009)
  22. AFM studies of lambda repressor oligomers securing DNA loops. Wang H, Finzi L, Lewis DE, Dunlap D. Curr Pharm Biotechnol 10 494-501 (2009)
  23. Tetramerization of the LexA repressor in solution: implications for gene regulation of the E.coli SOS system at acidic pH. Sousa FJ, Lima LM, Pacheco AB, Oliveira CL, Torriani I, Almeida DF, Foguel D, Silva JL, Mohana-Borges R. J. Mol. Biol. 359 1059-1074 (2006)
  24. The designability of protein switches by chemical rescue of structure: mechanisms of inactivation and reactivation. Xia Y, DiPrimio N, Keppel TR, Vo B, Fraser K, Battaile KP, Egan C, Bystroff C, Lovell S, Weis DD, Anderson JC, Karanicolas J. J. Am. Chem. Soc. 135 18840-18849 (2013)
  25. Cooperative DNA binding by CI repressor is dispensable in a phage lambda variant. Babić AC, Little JW. Proc. Natl. Acad. Sci. U.S.A. 104 17741-17746 (2007)
  26. Lambda's switch: lessons from a module swap. Ptashne M. Curr. Biol. 16 R459-62 (2006)
  27. An unusual repressor controls the expression of a crucial nicotine-degrading gene cluster in Pseudomonas putida S16. Wang L, Tang H, Yu H, Yao Y, Xu P. Mol. Microbiol. 91 1252-1269 (2014)
  28. Physicochemical properties and distinct DNA binding capacity of the repressor of temperate Staphylococcus aureus phage phi11. Ganguly T, Das M, Bandhu A, Chanda PK, Jana B, Mondal R, Sau S. FEBS J. 276 1975-1985 (2009)
  29. The lambda switch: cI closes the gap in autoregulation. Hochschild A. Curr. Biol. 12 R87-9 (2002)
  30. A single aromatic residue in transcriptional repressor protein KorA is critical for cooperativity with its co-regulator KorB. Bingle LE, Rajasekar KV, Muntaha St, Nadella V, Hyde EI, Thomas CM. Mol. Microbiol. 70 1502-1514 (2008)
  31. Identification of quaternary structure and functional domains of the CI repressor from bacteriophage TP901-1. Pedersen M, Lo Leggio L, Grossmann JG, Larsen S, Hammer K. J. Mol. Biol. 376 983-996 (2008)
  32. Bacterial lipid droplets bind to DNA via an intermediary protein that enhances survival under stress. Zhang C, Yang L, Ding Y, Wang Y, Lan L, Ma Q, Chi X, Wei P, Zhao Y, Steinbüchel A, Zhang H, Liu P. Nat Commun 8 15979 (2017)
  33. The lysis-lysogeny decision of bacteriophage 933W: a 933W repressor-mediated long-distance loop has no role in regulating 933W P(RM) activity. Bullwinkle TJ, Koudelka GB. J. Bacteriol. 193 3313-3323 (2011)
  34. A small protein-protein interaction domain common to KlcB and global regulators KorA and TrbA of promiscuous IncP plasmids. Bhattacharyya A, Figurski DH. J. Mol. Biol. 310 51-67 (2001)
  35. Indirect readout of DNA sequence by p22 repressor: roles of DNA and protein functional groups in modulating DNA conformation. Harris LA, Watkins D, Williams LD, Koudelka GB. J. Mol. Biol. 425 133-143 (2013)
  36. Structure and activity of Streptococcus pyogenes SipA: a signal peptidase-like protein essential for pilus polymerisation. Young PG, Proft T, Harris PW, Brimble MA, Baker EN. PLoS ONE 9 e99135 (2014)
  37. Transcriptional regulation and structural modelling of the Synechocystis sp. PCC 6803 carboxyl-terminal endoprotease family. Jansèn T, Kidron H, Soitamo A, Salminen T, Mäenpää P. FEMS Microbiol. Lett. 228 121-128 (2003)
  38. Probing the DNA sequence specificity of Escherichia coli RECA protein. Rajan R, Wisler JW, Bell CE. Nucleic Acids Res. 34 2463-2471 (2006)
  39. Split-TALE: A TALE-Based Two-Component System for Synthetic Biology Applications in Planta. Schreiber T, Prange A, Hoppe T, Tissier A. Plant Physiol 179 1001-1012 (2019)
  40. A λ Cro-Like Repressor Is Essential for the Induction of Conjugative Transfer of SXT/R391 Elements in Response to DNA Damage. Poulin-Laprade D, Burrus V. J. Bacteriol. 197 3822-3833 (2015)
  41. Effect of supercoiling on formation of protein-mediated DNA loops. Purohit PK, Nelson PC. Phys Rev E Stat Nonlin Soft Matter Phys 74 061907 (2006)
  42. Exploiting elements of transcriptional machinery to enhance protein stability. Barakat NH, Barakat NH, Carmody LJ, Love JJ. J. Mol. Biol. 366 103-116 (2007)
  43. Purification of bacteriophage lambda repressor. Gao N, Shearwin K, Mack J, Finzi L, Dunlap D. Protein Expr. Purif. 91 30-36 (2013)
  44. The C-terminal domain of the Escherichia coli RNA polymerase alpha subunit plays a role in the CI-dependent activation of the bacteriophage lambda pM promoter. Kedzierska B, Szambowska A, Herman-Antosiewicz A, Lee DJ, Busby SJ, Wegrzyn G, Thomas MS. Nucleic Acids Res. 35 2311-2320 (2007)
  45. The N-terminal domain of the repressor of Staphylococcus aureus phage Φ11 possesses an unusual dimerization ability and DNA binding affinity. Biswas A, Mandal S, Sau S. PLoS ONE 9 e95012 (2014)
  46. Digestion of the lambda cI repressor with various serine proteases and correlation with its three dimensional structure. Pal A, Chattopadhyaya R. J. Biomol. Struct. Dyn. 26 339-354 (2008)
  47. pH-dependent autocleavage of lambda repressor occurs in the operator-bound form: characterization of lambda repressor autocleavage. Ghosh K, Pal A, Chattopadhyaya R. Biochem. J. 379 325-330 (2004)
  48. Half-of-the-sites reactivity of F235C lambda-repressor: implications for the structure of the whole repressor. Bandyopadhyay S, Deb S, Bose S, Roy S. Protein Eng. 15 393-401 (2002)
  49. Papain does not cleave operator-bound lambda repressor: structural characterization of the carboxy terminal domain and the hinge. Ghosh K, Chattopadhyaya R. J. Biomol. Struct. Dyn. 18 557-567 (2001)
  50. Structural and dynamics studies of a truncated variant of CI repressor from bacteriophage TP901-1. Rasmussen KK, Frandsen KE, Boeri Erba E, Pedersen M, Varming AK, Hammer K, Kilstrup M, Thulstrup PW, Blackledge M, Jensen MR, Lo Leggio L. Sci Rep 6 29574 (2016)
  51. The application of fluorescence-conjugated pyrrole/imidazole polyamides in the characterization of protein-DNA complex formation. Han YW, Sugiyama H, Harada Y. Biomater Sci 4 391-399 (2016)
  52. Mutagenic dissection of the sequence determinants of protein folding, recognition, and machine function. Sauer RT. Protein Sci. 22 1675-1687 (2013)
  53. Structural basis for regulation of SOS response in bacteria. Gao B, Liang L, Su L, Wen A, Zhou C, Feng Y. Proc Natl Acad Sci U S A 120 e2217493120 (2023)
  54. The Pseudomonas aeruginosa AmrZ C-terminal domain mediates tetramerization and is required for its activator and repressor functions. Xu B, Ju Y, Soukup RJ, Ramsey DM, Fishel R, Wysocki VH, Wozniak DJ. Environ Microbiol Rep 8 85-90 (2016)
  55. Bacteriophage λ RexA and RexB functions assist the transition from lysogeny to lytic growth. Thomason LC, Schiltz CJ, Court C, Hosford CJ, Adams MC, Chappie JS, Court DL. Mol Microbiol 116 1044-1063 (2021)
  56. Communication between binding sites is required for YqjI regulation of target promoters within the yqjH-yqjI intergenic region. Wang S, Blahut M, Wu Y, Philipkosky KE, Outten FW. J. Bacteriol. 196 3199-3207 (2014)
  57. Environmental stress perception activates structural remodeling of extant Streptococcus mutans biofilms. Marx P, Sang Y, Qin H, Wang Q, Guo R, Pfeifer C, Kreth J, Merritt J. NPJ Biofilms Microbiomes 6 17 (2020)
  58. Fold conservation and proteolysis in zebrafish IRBP structure: Clues to possible enzymatic function? Ghosh D, Haswell KM, Sprada M, Gonzalez-Fernandez F. Exp. Eye Res. 147 78-84 (2016)
  59. GABPα Binding to Overlapping ETS and CRE DNA Motifs Is Enhanced by CREB1: Custom DNA Microarrays. He X, Syed KS, Tillo D, Mann I, Weirauch MT, Vinson C. G3 (Bethesda) 5 1909-1918 (2015)
  60. RecA-mediated cleavage of lambda cI repressor accepts repressor dimers: probable role of prolyl cis-trans isomerization and catalytic involvement of H163, K177, and K232 of RecA. Pal A, Chattopadhyaya R. J. Biomol. Struct. Dyn. 27 221-233 (2009)
  61. Alignment of major-groove hydrogen bond arrays uncovers shared information between different DNA sequences that bind the same protein. Sedhom J, Kinser J, Solomon LA. NAR Genom Bioinform 4 lqac101 (2022)
  62. Biochemical characterization of Mycobacterium tuberculosis LexA and structural studies of its C-terminal segment. Chandran AV, Srikalaivani R, Paul A, Vijayan M. Acta Crystallogr D Struct Biol 75 41-55 (2019)
  63. Construction of a highly error-prone DNA polymerase for developing organelle mutation systems. Ji J, Day A. Nucleic Acids Res 48 11868-11879 (2020)
  64. Discovery of Spatially Cohesive Itemsets in Three-Dimensional Protein Structures. Zhou C, Meysman P, Cule B, Laukens K, Goethals B. IEEE/ACM Trans Comput Biol Bioinform 11 814-825 (2014)
  65. Expression, purification and crystallization of a birnavirus-encoded protease, VP4, from blotched snakehead virus (BSNV). Lee J, Feldman AR, Delmas B, Paetzel M. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 353-356 (2006)
  66. High diversity in the regulatory region of Shiga toxin encoding bacteriophages. Fagerlund A, Aspholm M, Węgrzyn G, Lindbäck T. BMC Genomics 23 230 (2022)
  67. Lambda CI Binding to Related Phage Operator Sequences Validates Alignment Algorithm and Highlights the Importance of Overlooked Bonds. Sedhom J, Solomon LA. Genes (Basel) 14 2221 (2023)
  68. Microscopic understanding of the conformational features of a protein-DNA complex. Mondal S, Chakraborty K, Bandyopadhyay S. Phys Chem Chem Phys 19 32459-32472 (2017)
  69. Molecular parts and genetic circuits for metabolic engineering of microorganisms. Kim SG, Noh MH, Lim HG, Jang S, Jang S, Koffas MAG, Jung GY. FEMS Microbiol. Lett. 365 (2018)
  70. Refactoring the λ phage lytic/lysogenic decision with a synthetic regulator. Durante-Rodríguez G, Mancheño JM, Díaz E, Carmona M. Microbiologyopen 5 575-581 (2016)
  71. Specific DNA sequences allosterically enhance protein-protein interaction in a transcription factor through modulation of protein dynamics: implications for specificity of gene regulation. Mazumder A, Batabyal S, Mondal M, Mondol T, Choudhury S, Ghosh R, Chatterjee T, Bhattacharyya D, Pal SK, Roy S. Phys Chem Chem Phys 19 14781-14792 (2017)
  72. Using a synthetic machinery to improve carbon yield with acetylphosphate as the core. Guo L, Liu M, Bi Y, Qi Q, Xian M, Zhao G. Nat Commun 14 5286 (2023)


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