A basic/hydrophobic cleft of the T4 activator MotA interacts with the C-terminus of E. coliσ70 to activate middle gene transcription

Molecular Microbiology

Volumn 69, Issue 2, 2008, Pages 331-343

  Bonocora, Richard P ^a   Caignan, Gregori ^b,c   Woodrell, Christopher ^b,d   Werner, Milton H ^b,e   Hinton, Deborah M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c Institut de Professionalisation en Biotechnologies   (France)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e ATDC Biosciences Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASIA PROTEIN; BACTERIAL PROTEIN; MOTA PROTEIN;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ESCHERICHIA COLI; GENE MUTATION; GENETIC TRANSCRIPTION; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; ARTIFICIAL GENE FUSION; BACTERIOPHAGE T4; BETA-GALACTOSIDASE; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL VIABILITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SIGMA FACTOR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS;

ESCHERICHIA COLI;

EID: 47249114444     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06276.x     Document Type: Article

References (59)

1. Barnard, A., Wolfe, A. Busby, S. (2004) Regulation at complex bacterial promoters: how bacteria use different promoter organizations to produce different regulatory outcomes. Curr Opin Microbiol 7 : 102 108.
2. Baxter, K., Lee, J., Minakhin, L., Severinov, K. Hinton, D.M. (2006) Mutational analysis of sigma(70) region 4 needed for appropriation by the bacteriophage T4 transcription factors AsiA and MotA. J Mol Biol 363 : 931 944.
3. Bhende, P.M. Egan, S.M. (2000) Genetic evidence that transcription activation by RhaS involves specific amino acid contacts with sigma 70. J Bacteriol 182 : 4959 4969.
4. Browning, D.F. Busby, S.J. (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2 : 57 65.
5. Campbell, E.A., Muzzin, O., Chlenov, M., Sun, J.L., Olson, C.A., Weinman, O., et al. (2002) Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell 9 : 527 539.
6. Chen, B.S. Hampsey, M. (2002) Transcription activation: unveiling the essential nature of TFIID. Curr Biol 12 : 620 622.
7. Cicero, M.P., Alexander, K.A. Kreuzer, K.N. (1998) The MotA transcriptional activator of bacteriophage T4 binds to its specific DNA site as a monomer. Biochemistry 37 : 4977 4984.
8. Colland, F., Orsini, G., Brody, E.N., Buc, H. Kolb, A. (1998) The bacteriophage T4 AsiA protein: a molecular switch for sigma 70-dependent promoters. Mol Microbiol 27 : 819 829.
9. Dove, S.L. Hochschild, A. (2004) A bacterial two-hybrid system based on transcription activation. Meth Mol Biol 261 : 231 246.
10. Dove, S.L., Joung, J.K. Hochschild, A. (1997) Activation of prokaryotic transcription through arbitrary protein-protein contacts. Nature 386 : 627 630.
11. Dove, S.L., Huang, F.W. Hochschild, A. (2000) Mechanism for a transcriptional activator that works at the isomerization step. Proc Natl Acad Sci USA 97 : 13215 13220.
12. Finnin, M.S., Hoffman, D.W., Kreuzer, K.N., Porter, S.J., Schmidt, R.P. White, S.W. (1993) The MotA protein from bacteriophage T4 contains two domains. Preliminary structural analysis by X-ray diffraction and nuclear magnetic resonance. J Mol Biol 232 : 301 304.
13. Finnin, M.S., Hoffman, D.W. White, S.W. (1994) The DNA-binding domain of the MotA transcription factor from bacteriophage T4 shows structural similarity to the TATA-binding protein. Proc Natl Acad Sci USA 91 : 10972 10976.
14. Finnin, M.S., Cicero, M.P., Davies, C., Porter, S.J., White, S.W. Kreuzer, K.N. (1997) The activation domain of the MotA transcription factor from bacteriophage T4. EMBO J 16 : 1992 2003.
15. Gerber, J.S. Hinton, D.M. (1996) An N-terminal mutation in the bacteriophage T4 motA gene yields a protein that binds DNA but is defective for activation of transcription. J Bacteriol 178 : 6133 6139.
16. Gruber, T.M. Gross, C.A. (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57 : 441 466.
17. Guzman, L.M., Belin, D., Carson, M.J. Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 : 4121 4130.
18. Hinton, D.M. (1991) Transcription from a bacteriophage T4 middle promoter using T4 motA protein and phage-modified RNA polymerase. J Biol Chem 266 : 18034 18044.
19. Hinton, D.M. Vuthoori, S. (2000) Efficient inhibition of Escherichia coli RNA polymerase by the bacteriophage T4 AsiA protein requires that AsiA binds first to free sigma70. J Mol Biol 304 : 731 739.
20. Hinton, D.M., March-Amegadzie, R., Gerber, J.S. Sharma, M. (1996) Bacteriophage T4 middle transcription system: T4-modified RNA polymerase; AsiA, a sigma 70 binding protein; and transcriptional activator MotA. Methods Enzymol 274 : 43 57.
21. Hinton, D.M., Pande, S., Wais, N., Johnson, X.B., Vuthoori, M., Makela, A. Hook-Barnard, I. (2005) Transcriptional takeover by sigma appropriation: remodelling of the sigma70 subunit of Escherichia coli RNA polymerase by the bacteriophage T4 activator MotA and co-activator AsiA. Microbiology 151 : 1729 1740.
22. Hobman, J.L., Wilkie, J. Brown, N.L. (2005) A design for life: prokaryotic metal-binding MerR family regulators. Biometals 18 : 429 436.
23. Hook-Barnard, I.G. Hinton, D.M. (2007) Transcription initiation by mix and match elements: flexibility for polymerase binding to bacterial promoters. Gene Regulation and Systems Biology. http://la-press.com/article.php?article_id= 481
24. Hu, J.C., Kornacker, M.G. Hochschild, A. (2000) Escherichia coli one- and two-hybrid systems for the analysis and identification of protein-protein interactions. Methods 20 : 80 94.
25. Jain, D., Nickels, B.E., Sun, L., Hochschild, A. Darst, S.A. (2004) Structure of a ternary transcription activation complex. Mol Cell 13 : 45 53.
26. Kuldell, N. Hochschild, A. (1994) Amino acid substitutions in the -35 recognition motif of sigma 70 that result in defects in phage lambda repressor-stimulated transcription. J Bacteriol 176 : 2991 2998.
27. Kuznedelov, K., Minakhin, L., Niedziela-Majka, A., Dove, S.L., Rogulja, D., Nickels, B.E., et al. (2002) A role for interaction of the RNA polymerase flap domain with the sigma subunit in promoter recognition. Science 295 : 855 857.
28. Lambert, L.J., Schirf, V., Demeler, B., Cadene, M. Werner, M.H. (2001) Flipping a genetic switch by subunit exchange. EMBO J 20 : 7149 7159.
29. Lambert, L.J., Wei, Y., Schirf, V., Demeler, B. Werner, M.H. (2004) T4 AsiA blocks DNA recognition by remodeling sigma(70) region 4. EMBO J 23 : 2952 2962.
30. Landini, P. Busby, S.J. (1999) The Escherichia coli Ada protein can interact with two distinct determinants in the sigma70 subunit of RNA polymerase according to promoter architecture: identification of the target of Ada activation at the alkA promoter. J Bacteriol 181 : 1524 1529.
31. Lawson, C.L., Swigon, D., Murakami, K.S., Darst, S.A., Berman, H.M. Ebright, R.H. (2004) Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol 14 : 10 20.
32. Li, M., Moyle, H. Susskind, M.M. (1994) Target of the transcriptional activation function of phage lambda cI protein. Science 263 : 75 77.
33. Li, N., Zhang, W., White, S.W. Kriwacki, R.W. (2001) Solution structure of the transcriptional activation domain of the bacteriophage T4 protein, MotA. Biochemistry 40 : 4293 4302.
34. Li, N., Sickmier, E.A., Zhang, R., Joachimiak, A. White, S.W. (2002) The MotA transcription factor from bacteriophage T4 contains a novel DNA-binding domain: the 'double wing' motif. Mol Microbiol 43 : 1079 1088.
35. Lonetto, M.A., Rhodius, V., Lamberg, K., Kiley, P., Busby, S. Gross, C. (1998) Identification of a contact site for different transcription activators in region 4 of the Escherichia coli RNA polymerase sigma70 subunit. J Mol Biol 284 : 1353 1365.
36. March-Amegadzie, R. Hinton, D.M. (1995) The bacteriophage T4 middle promoter PuvsX: analysis of regions important for binding of the T4 transcriptional activator MotA and for activation of transcription. Mol Microbiol 15 : 649 660.
37. Mattson, T., Van Houwe, G. Epstein, R.H. (1978) Isolation and characterization of conditional lethal mutations in the mot gene of bacteriophage T4. J Mol Biol 126 : 551 570.
38. Murakami, K.S. Darst, S.A. (2003) Bacterial RNA polymerases: the wholo story. Curr Opin Struct Biol 13 : 31 39.
39. Murakami, K.S., Masuda, S. Darst, S.A. (2002) Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 A resolution. Science 296 : 1280 1284.
40. Nickels, B.E., Dove, S.L., Murakami, K.S., Darst, S.A. Hochschild, A. (2002) Protein-protein and protein-DNA interactions of sigma70 region 4 involved in transcription activation by lambda cI. J Mol Biol 324 : 17 34.
41. Ouhammouch, M., Adelman, K., Harvey, S.R., Orsini, G. Brody, E.N. (1995) Bacteriophage T4 MotA and AsiA proteins suffice to direct Escherichia coli RNA polymerase to initiate transcription at T4 middle promoters. Proc Natl Acad Sci USA 92 : 1451 1455.
42. Paget, M.S. Helmann, J.D. (2003) The sigma70 family of sigma factors. Genome Biol 4 : 203.
43. Pal, D., Vuthoori, M., Pande, S., Wheeler, D. Hinton, D.M. (2003) Analysis of regions within the bacteriophage T4 AsiA protein involved in its binding to the sigma70 subunit of E. coli RNA polymerase and its role as a transcriptional inhibitor and co-activator. J Mol Biol 325 : 827 841.
44. Pande, S., Makela, A., Dove, S.L., Nickels, B.E., Hochschild, A. Hinton, D.M. (2002) The bacteriophage T4 transcription activator MotA interacts with the far-C-terminal region of the sigma70 subunit of Escherichia coli RNA polymerase. J Bacteriol 184 : 3957 3964.
45. Patikoglou, G.A., Westblade, L.F., Campbell, E.A., Lamour, V., Lane, W.J. Darst, S.A. (2007) Crystal structure of the Escherichia coli regulator of sigma(70), Rsd, in complex with sigma(70) domain 4. J Mol Biol 372 : 649 659.
46. Pineda, M., Gregory, B.D., Szczypinski, B., Baxter, K.R., Hochschild, A., Miller, E.S. Hinton, D.M. (2004) A family of anti-sigma70 proteins in T4-type phages and bacteria that are similar to AsiA, a transcription inhibitor and co-activator of bacteriophage T4. J Mol Biol 344 : 1183 1197.
47. Pulitzer, J.F., Coppo, A. Caruso, M. (1979) Host-virus interactions in the control of T4 prereplicative transcription. II. Interaction between tabC (rho) mutants and T4 mot mutants. J Mol Biol 135 : 979 997.
48. Rhodius, V.A. Busby, S.J. (2000) Interactions between activating region 3 of the Escherichia coli cyclic AMP receptor protein and region 4 of the RNA polymerase sigma(70) subunit: application of suppression genetics. J Mol Biol 299 : 311 324.
49. Severinova, E., Severinov, K., Fenyo, D., Marr, M., Brody, E.N., Roberts, J.W., et al. (1996) Domain organization of the Escherichia coli RNA polymerase sigma 70 subunit. J Mol Biol 263 : 637 647.
50. Severinova, E., Severinov, K. Darst, S.A. (1998) Inhibition of Escherichia coli RNA polymerase by bacteriophage T4 AsiA. J Mol Biol 279 : 9 18.
51. Sharma, M. Hinton, D.M. (1994) Purification and characterization of the SegA protein of bacteriophage T4, an endonuclease related to proteins encoded by group I introns. J Bacteriol 176 : 6439 6448.
52. Sharma, M., Marshall, P. Hinton, D.M. (1999) Binding of the bacteriophage T4 transcriptional activator, MotA, to T4 middle promoter DNA: evidence for both major and minor groove contacts. J Mol Biol 290 : 905 915.
53. Stevens, A. (1976) A salt-promoted inhibitor of RNA polymerase isolated from T4 phage-infected E. coli. In RNA Polymerase. Losick, R. Chamberlin, M. (eds). Cold Spring Harbor, NY : Cold Spring Harbor Laboratory, pp. 617 627.
54. Stevens, A. Rhoton, J.C. (1975) Characterization of an inhibitor causing potassium chloride sensitivity of an RNA polymerase from T4 phage-infected Escherichia coli. Biochemistry 14 : 5074 5079.
55. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673 4680.
56. Triezenberg, S.J. (1995) Structure and function of transcriptional activation domains. Curr Opin Genet Dev 5 : 190 196.
57. Vassylyev, D.G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M.N., Borukhov, S. Yokoyama, S. (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 A resolution. Nature 417 : 712 719.
58. Watanabe, S., Kita, A., Kobayashi, K. Miki, K. (2008) Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc Natl Acad Sci USA 105 : 4121 4126.
59. Wickstrum, J.R. Egan, S.M. (2004) Amino acid contacts between sigma 70 domain 4 and the transcription activators RhaS and RhaR. J Bacteriol 186 : 6277 6285.