DNA bending and looping in the transcriptional control of bacteriophage φ29

FEMS Microbiology Reviews

Volumn 34, Issue 5, 2010, Pages 828-841

  Camacho, Ana ^a   Salas, Margarita ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

gene regulation; indirect readout; nucleoprotein complexes; protein induced DNA bending; transcriptional regulators

Indexed keywords

CURVED DNA; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN P1; PROTEIN P2; PROTEIN P3; PROTEIN P4; PROTEIN P5; PROTEIN P56; PROTEIN P6; RNA POLYMERASE; TRANSCRIPTION FACTOR; TRANSLATION TERMINATION FACTOR; UNCLASSIFIED DRUG;

BACILLUS PHAGE; BACILLUS SUBTILIS; BINDING SITE; DNA BINDING; DNA LOOPING; DNA MODIFICATION; DNA PROTEIN COMPLEX; DNA SEQUENCE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC STABILITY; NONHUMAN; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY DNA SEQUENCE; REVIEW; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

BACILLUS PHAGES; BACILLUS SUBTILIS; BASE SEQUENCE; DNA, VIRAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, VIRAL; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

BACILLUS PHAGE PHI29; PROKARYOTA;

EID: 77955136882     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2010.00219.x     Document Type: Review

References (136)

1. Adhya S (1989) Multipartite genetic control elements: communication by DNA loop. Annu Rev Genet 23 : 227 250.
2. Adhya S, Geanocopoulos M, Lewis DE, Roy S Aki T (1998) Transcription regulation by repressosome and by RNA polymerase contact. Cold Spring Harbor Symposium Quant Biol. 63 : 1 9.
3. Aiba H (1983) Negative control of transcription by cAMP and cAMP receptor protein in Escherichia coli. Adv Biophys 21 : 193 204.
4. Badia D, Camacho A, Pérez-Lago L, Escandón C, Salas M Coll M (2006) The structure of phage φ29 transcription regulator p4-DNA complex reveals an N-hook motif for DNA. Mol Cell 22 : 73 81.
5. Bareket-Samish A, Cohen I Haran TE (1998) Direct versus indirect readout in the interaction of the trp repressor with non-canonical binding sites. J Mol Biol 277 : 1071 1080.
6. Bar-Nahum G, Epshtein V, Ruckenstein AE, Rafikov R, Mustaev A Nudler E (2005) A ratchet mechanism of transcription elongation and its control. Cell 120 : 155 156.
7. 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.
8. 70 subunit is responsible for the recognition of the 'extended -10' motif at promoters. EMBO J 16 : 4034 4040.
9. Barthelemy I Salas M (1989) Characterization of a new prokaryotic transcriptional activator and its DNA recognition site. J Mol Biol 208 : 225 232.
10. Barthelemy I, Salas M Mellado RP (1986) In vivo transcription of bacteriophage φ29 DNA: transcription initiation sites. J Virol 60 : 874 879. (Pubitemid 17179260)
11. Barthelemy I, Salas M Mellado RP (1987) In vivo transcription of bacteriophage φ29 DNA: transcription termination. J Virol 61 : 1751 1755.
12. Barthelemy I, Mellado RP Salas M (1989) In vitro transcription of bacteriophage φ29 DNA: inhibition of early promoters by the viral replication protein p6. J Virol 63 : 460 462.
13. Beloin C, Jeusset J, Revet B, Mirambeau G, Le Hégarat F Le Cam E (2003) Contribution of DNA conformation and topology in right-handed DNA wrapping by the Bacillus subtilis LrpC protein. J Biol Chem 278 : 5333 5342.
14. Blanco L, Gutierrez C, Lázaro JM, Bernard A Salas M (1986) Replication of φ29 DNA in vitro: role of the viral p6 in initiation and elongation. Nucleic Acids Res 14 : 4923 4937.
15. Bourgerie SJ, Michan CM, Thomas MS, Busby SJ Hyde EI (1997) DNA binding and DNA bending by the MelR transcription activator protein from Escherichia coli. Nucleic Acids Res 25 : 1685 1693.
16. Brown NL, Stoyanov JV, Kidd SP Hobman JL (2003) The MelR family of transcriptional regulators. FEMS Microbiol Rev 27 : 145 163.
17. Browning DF Busby SJW (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2 : 57 65.
18. Buckle M, Pemberton IK, Jacquet MA Buc H (1999) The kinetics of sigma subunit directed promoter recognition by E. coli RNA polymerase. J Mol Biol 285 : 955 964.
19. Calles B, Salas M Rojo F (2002) The φ29 transcriptional regulator contacts the nucleoid protein p6 to organize a repression complex. EMBO J 21 : 6185 6194.
20. A-RNA polymerase-dependent promoters. J Mol Biol 286 : 683 693.
21. Camacho A Salas M (2000) Pleiotropic effect of protein p6 on the viral cycle of bacteriophage φ29. J Bacteriol 182 : 6927 6932.
22. Camacho A Salas M (2001a) Repression of bacteriophage φ29 early promoter C2 by viral protein p6 is due to impairment of closed complex. J Biol Chem 276 : 28927 28932.
23. Camacho A Salas M (2001b) Mechanism for the switch of φ29 DNA early to late transcription by regulatory protein p4 and histone-like protein p6. EMBO J 20 : 6060 6070.
24. Camacho A Salas M (2004) Molecular interplay between RNA polymerase and two transcriptional regulators in promoter switch. J Mol Biol 336 : 357 368.
25. Campbell EA, Muzzin O, Chlenov M, Sun JL, Olson CA, Weinman O, Trester-Zedlitz ML Darst SA (2002) Structure of the bacterial RNA polymerase promoter specificity σ subunit. Mol Cell 9 : 527 539.
26. Carrascosa JL, Camacho A, Moreno F, Jiménez F, Mellado RP, Viñuela E Salas M (1976) Bacillus subtilis phage φ29. Characterization of gene products and functions. Eur J Biochem 66 : 229 241.
27. Cellai S, Mangiarotti L, Vannini N, Naryshkin N, Kortkhonjia E, Ebright RH Rivetti C (2007) Upstream promoter sequences and αCTD mediate stable DNA wrapping within the RNA polymerase-promoter open complex. EMBO Rep 3 : 271 278.
28. A (sigma A) factor and RNA polymerase with promoters. Biochimie 74 : 601 612.
29. Choy HE, Park SW, Aki T, Parrack P, Fujita N, Ishihama A Adhya S (1995) Repression and activation of transcription by Gal and Lac repressors: involvement of α subunit of RNA polymerase. EMBO J 14 : 4523 4529.
30. Crucitti P, Abril AM Salas M (2003) Bacteriophage φ29 early protein p17. Self-association and hetero-association with the viral histone-like protein p6. J Biol Chem 278 : 4906 4911.
31. Darst SA (2001) Bacterial RNA polymerase. Curr Opin Struc Biol 11 : 155 162.
32. Dobinson KF Spiegelman GB (1985) Nucleotide sequence and transcription of a bacteriophage φ29 early promoter. J Biol Chem 260 : 950 955.
33. Drlica K Rouviere-Yaniv J (1987) Histone-like proteins of bacteria. Microbiol Rev 51 : 301 319.
34. Dunn TM, Hahn S, Ogden S Schleif RF (1984) An operator at -280 base pairs that is required for repression of araBAD operon promoter: addition of DNA helical turns between the operator and promoter cyclically hinders repression. P Natl Acad Sci USA 81 : 5017 5020.
35. Ebright RH (2002) RNA polymerase: structural similarities between bacterial RNA polymerase and eukaryotic RNA polymerase II. J Mol Biol 304 : 687 698.
36. Echols H (1990) Nucleoprotein structures initiating DNA replication, transcription, and site-specific recombination. J Biol Chem 265 : 14697 14700.
37. Elías-Arnanz M Salas M (1999) Functional interactions between a phage histone-like protein and a transcriptional factor in regulation of φ29 early-late transcriptional switch. Gene Dev 13 : 2502 2513.
38. Falco SC, Zehring W Rothman-Denes LB (1980) DNA-dependent RNA polymerase from bacteriophage N4 virions. Purification and characterization. J Biol Chem 255 : 4339 4347.
39. Gartenberg MR Crothers DM (1988) DNA sequence determinants of CAP-induced bending and protein binding affinity. Nature 333 : 824 829.
40. González-Huici V, Alcorlo M, Salas M Hermoso JM (2004) Bacteriophage φ29 protein p6: an architectural protein involved in genome organization, replication and control of transcription. J Mol Recognit 17 : 390 396. (Pubitemid 39218981)
41. González-Huici V, Salas M Hermoso JM (2006) Requirements for Bacillus subtilis bacteriophage φ29 DNA ejection. Gene 374 : 19 25.
42. Gourse RL, Ross W Gaal T (2000) UP and downs in bacterial transcription initiation: the role of the α subunit of RNA polymerase in promoter recognition. Mol Microbiol 4 : 687 695.
43. Grosschedl R (1995) Higher-order nucleoprotein complexes in transcription: analogies with site-specific recombination. Curr Opin Cell Biol 7 : 362 370.
44. Gruber TM Gross CA (2003) Multiple σ subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57 : 441 466.
45. Guo P, Erickson S Anderson D (1987) A small viral RNA is required for in vitro packaging of bacteriophage φ29 DNA. Science 236 : 690 694.
46. Gutiérrez C, Freire R, Salas M Hermoso JM (1994) Assembly of phage φ29 genome with viral protein p6 into a compact complex. EMBO J 13 : 269 276.
47. Gutiérrez del Arroyo PG, Vélez M, Piétrement O, Salas M, Carrascosa JL Camacho A (2009) A nucleoprotein-hairpin in transcription regulation. J Struct Biol 168 : 444 451.
48. Haugen SP, Ross W, Manrique M Gourse RL (2008) Fine structure of the promoter-σ region 1.2 interaction. P Natl Acad Sci USA 105 : 3292 3297.
49. Heffernan L Wilcox G (1976) Effect of araC gene product on catabolite repression in the l-arabinose regulon. J Bacteriol 126 : 1132 1135.
50. A-dependent promoter sequences: evidence for extended contact between RNA polymerase and upstream promoter DNA. Nucleic Acids Res 23 : 2351 2360.
51. Hochschild A Dove SL (1998) Protein-protein contacts that activate and repress prokaryotic transcription. Cell 92 : 597 600.
52. Hochschild A Ptashne M (1986) Cooperative binding of lambda repressors to sites separated by integral turns of the DNA helix. Cell 44 : 681 687.
53. Hogan ME Austin RH (1987) Importance of DNA stiffness in protein-DNA binding specificity. Nature 329 : 263 266.
54. 70 region 1.1 of Escherichia coli RNA polymerase. P Natl Acad Sci USA 106 : 737 742.
55. A with RNA polymerase. Protein Sci 18 : 2287 2297.
56. Joly N, Bohm A Richet E (2004) MalK, the Atp-binding cassette component of the Escherichia coli maltodextrin transporter, inhibits the transcriptional activator MalT and antagonizing inducer binding. J Biol Chem 279 : 33123 33130.
57. Kahn JD Crothers DM (1998) Measurement of the DNA bend angle induced by the catabolite activator protein using Monte Carlo simulation of cyclization kinetics. J Mol Biol 276 : 287 309.
58. Kalodimos CG, Biris N, Bonvin AM, Levandoski MM, Guennuegues M, Boelens R Kaptein R (2004a) Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science 305 : 386 389.
59. Kalodimos CG, Boelens R Kaptein R (2004b) Toward an integrated model of protein-DNA recognition as inferred from NMR studies on the Lac repressor system. Chem Rev 104 : 3567 3586.
60. Kawamura F Ito J (1977) Transcription of the genome of bacteriophage φ29: isolation and mapping of the major early mRNA synthesized in vivo and in vitro. J Virol 23 : 562 577.
61. Kim SI, Jourlin-Caselli C, Wellington SR Sonenshein AL (2003) Mechanism of repression by Bacillus subtilis CcpC, a LysR family regulator. J Mol Biol 334 : 609 624.
62. Krämer H, Niemöller M, Amouyal M, Revet B, von Wilcken-Bergmann B Müller-Hill B (1987) Lac repressor forms loops with linear DNA carrying two suitably spaced lac operators. EMBO J 6 : 1481 1491.
63. Lavigne M, Kolb A, Yeramian E Buc H (1994) CRP fixes the rotational orientation of covalently closed DNA molecules. EMBO J 13 : 4983 4990.
64. Lee DH Schleif RF (1989) In vivo DNA loops in araCBAD: size limits and helical repeat. P Natl Acad Sci USA 86 : 4764 4780.
65. Lewis DE Adhya S (2002) In vitro repression of the gal promoters by GalR and HU depends on the proper helical phasing of the two operators. J Biol Chem 277 : 2498 2504.
66. Lewis DE, Lee HJ, Liu M Adhya S (2003) Effect of varying the supercoiling of DNA on transcription and its regulation. Biochemistry 42 : 10718 10725.
67. Lim FL, Hayes A, West AG, Pic-Taylor A, Darieva Z, Morgan BA, Oliver SG Sharrocks AD (2003) Mcm1p-induced DNA bending regulates the formation of ternary transcription factor complex. Mol Cell Biol 23 : 450 461.
68. Lloyd GP, Landini P Busby S (2001) Activator and repression of transcription initiation in bacteria. Essays Biochem 37 : 17 31.
69. Loskutoff DJ Pène JJ (1973) Gene expression during the development of Bacillus subtilis bacteriophage φ29. I. Analysis of viral-specific transcription by deoxyribonucleic acid-ribonucleic acid competition hybridization. J Virol 11 : 78 86.
70. Loskutoff DJ, Pène JJ Andrews DP (1973) Gene expression during the development of Bacillus subtilis bacteriophage φ29. II. Resolution of viral-specific ribonucleic acid molecules. J Virol 11 : 87 97.
71. 70 subunit fragment from E. coli RNA polymerase. Cell 87 : 127 136. (Pubitemid 26337397)
72. Mathew R Chatterji D (2006) The evolving story of the omega subunit of bacterial RNA polymerase. Trends Microbiol 14 : 450 455.
73. Matthews KS (1992) DNA looping. Microbiol Rev 56 : 123 136.
74. Mauro SA, Pawlowski D Koudelka GB (2003) The role of the minor groove substituents in indirect readout of DNA sequence by 434 repressor. J Biol Chem 278 : 12955 12960.
75. McAllister WT Raskin CA (1993) The phage RNA polymerases are related to DNA polymerases and reverse transcriptases. Mol Microbiol 10 : 1 6.
76. Meijer WJ Salas M (2004) Relevance of UP elements for three strong Bacillus subtilis phage φ29 promoters. Nucleic Acids Res 32 : 1166 1176.
77. Meijer WJ, Horcajadas JA Salas M (2001) φ29 family of phages. Microbiol Mol Biol R 65 : 261 287.
78. Mekler V, Kortkhonjia E, Mukhopadhyay J, Knight J, Revyakin A, Kapanidis AN, Niu W, Ebright YW, Levy R Ebright RH (2002) Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell 108 : 599 614.
79. Mellado RP, Barthelemy I Salas M (1986a) In vitro transcription of bacteriophage φ29 DNA. Correlation between in vitro and in vivo promoters. Nucleic Acids Res 14 : 4731 4741.
80. Mellado RP, Barthelemy I Salas M (1986b) In vivo transcription of bacteriophage φ29 DNA early and late promoter sequences. J Mol Biol 191 : 191 197. (Pubitemid 16027918)
81. Mencía M, Monsalve M, Rojo F Salas M (1996a) Transcription activation by phage φ29 protein p4 is mediated by interaction with the α subunit of Bacillus subtilis RNA polymerase. P Natl Acad Sci USA 93 : 6616 6620. (Pubitemid 26230357)
82. Mencía M, Monsalve M, Salas M Rojo F (1996b) Transcriptional activator of phage φ29 late promoter: mapping of residues involved in interaction with RNA polymerase and in DNA bending. Mol Microbiol 20 : 273 282.
83. Mendieta J, Pérez-Lago L, Salas M Camacho A (2007) DNA sequence-specific recognition by a transcriptional regulator requires indirect readout of A-tracts. Nucleic Acids Res 35 : 3252 3261.
84. Milani P, Marilley M Rocca-Serra J (2007) TBP binding capacity of the TATA box is associated with specific structural properties: AFM study of the IL-2R α gene promoter. Biochimie 89 : 528 533.
85. Minakhin L, Bhagat S, Brunning A, Campbell EA, Darst SA, Ebright RH Severinov K (2001) Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. P Natl Acad Sci USA 98 : 892 897.
86. Monsalve M, Mencía M, Rojo F Salas M (1995) Transcription regulation in Bacillus subtilis phage φ29: expression of the viral promoters throughout the infection cycle. Virology 207 : 23 31.
87. Monsalve M, Mencía M, Salas M Rojo F (1996) Protein p4 represses phage φ29 A2c promoter by interacting with the α subunit of Bacillus subtilis RNA polymerase. P Natl Acad Sci USA 93 : 8913 8918.
88. Moreno-Herrero F, Colchero J Baró AM (2003) DNA height in scanning force microscopy. Ultramicroscopy 96 : 167 174.
89. Murakami KS, Masuda S, Campbell EA, Muzzin O Darst SA (2002a) Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science 296 : 1285 1290. (Pubitemid 34522778)
90. Murakami KS, Masuda S Darst SA (2002b) Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 Åresolution. Science 296 : 1280 1284. (Pubitemid 34522777)
91. Murray CL Rabinowitz JC (1982) Nucleotide sequences of transcription and translation initiation regions in Bacillus phage φ29 early genes. J Biol Chem 257 : 1053 1062.
92. Napoli AA, Lawson CL, Ebright RH Berman HM (2006) Indirect readout of DNA sequence at the primary-kink site in the CAP-DNA complex: recognition of pyrimidine-purine and purine-purine steps. J Mol Biol 357 : 173 183.
93. Naryshkin N, Druzhinin S, Revyakin A, Kim Y, Mekler V Ebright RH (2009) Static and kinetic site-specific protein-DNA photocrosslinking: analysis of bacterial transcription initiation complexes. Methods Mol Biol 543 : 403 437.
94. Nudler E (2009) RNA polymerase active center: the molecular engine of transcription. Annu Rev Biochem 78 : 335 361.
95. Nuez B, Rojo F Salas M (1992) Phage φ29 regulatory protein p4 stabilizes the binding of the RNA polymerase to the late promoter in a process involving direct protein-protein contact. P Natl Acad Sci USA 89 : 11401 11405.
96. Nuez B, Rojo F Salas M (1994) Requirement for an A-tract structure at the binding site of phage φ29 transcriptional activator. J Mol Biol 237 : 175 181.
97. Pérez-Lago L, Salas M Camacho A (2005a) A precise DNA bend angle is essential for the function of the phage φ29 transcriptional regulator. Nucleic Acids Res 33 : 126 134.
98. Pérez-Lago L, Salas M Camacho A (2005b) Homologies and divergences in the transcription regulatory system of two related Bacillus subtilis phages. J Bacteriol 187 : 6403 6649.
99. Pérez-Martin J de Lorenzo V (1997) Clues and consequences of DNA bending in transcription. Annu Rev Microbiol 51 : 593 628.
100. Prieto I, Serrano M, Lázaro JM, Salas M Hermoso JM (1988) Interaction of the bacteriophage φ29 protein p6 with double-stranded DNA. P Natl Acad Sci USA 85 : 314 318.
101. Ptashne M (2006) Lambda's Switch: lessons from a module swap. Curr Biol 16 : R459 R462.
102. Ptashne M Gann A (1997) Transcriptional activation by recruitment. Nature 386 : 569 577.
103. Rojo F, Zaballos A Salas M (1990) Bend induced by the phage φ29 transcriptional activator in the viral late promoter is required for activation. J Mol Biol 211 : 713 725.
104. Rojo F, Mencía M, Monsalve M Salas M (1998) Transcription activation and repression by interaction of a regulator with the α subunit of RNA polymerase: the model of phage φ29 protein p4. Prog Nucleic Acid Re 60 : 29 46.
105. Ross ED, Keating AM Maher LJ (2000) DNA constraints on transcription activation in vitro. J Mol Biol 297 : 321 334.
106. Ross W Gourse RL (2009) Analysis of RNA polymerase-promoter complex formation. Methods 47 : 13 24.
107. Ross W, Gosink KK, Salomon J, Igarashi K, Zou C, Ishihama A, Severinov K Gourse RL (1993) A third recognition element in bacterial promoters: DNA binding by the α subunit of RNA polymerase. Science 262 : 1407 1413.
108. Salas M (1991) Protein-priming of DNA replication. Annu Rev Biochem 60 : 39 71.
109. Sanderson A, Mitchell JE, Minchin SD Busby SJ (2003) Substitutions in the Escherichia coli RNA polymerase σ70 factor that affect recognition of extended -10 elements at promoters. FEBS Lett 544 : 199 205.
110. Scaffidi P Bianchi ME (2001) Spatially precise DNA bending is an essential activity of the Sox2 transcription factor. J Biol Chem 276 : 47296 47302.
111. Schleif R (1992) DNA looping. Annu Rev Biochem 61 : 199 223.
112. Schleif R (2000) Regulation of the l-arabinose operon of Escherichia coli. Trends Genet 16 : 559 565.
113. Schreiber V, Steegborn C, Clausen T, Boos W Richet E (2000) A new mechanism for the control of a prokaryotic transcriptional regulator: antagonistic binding of positive and negative effectors. Mol Microbiol 35 : 765 776.
114. Schwartz EC, Shekhtman A, Dutta K, Pratt MR, Cowburn D, Darst S Muir TW (2008) A full-length group 1 bacterial sigma factor adopts a compact structure incompatible with DNA binding. Chem Biol 15 : 1091 1103.
115. Semsey S, Virnik K Adhya S (2005) A gamut of loops: meandering DNA. Trends Biochem Sci 30 : 334 341.
116. Serna-Rico A, Salas M Meijer WJ (2002) The Bacillus subtilis phage φ29 protein p16.7, involved in φ29 DNA replication, is a membrane-localized single-stranded DNA-binding protein. J Biol Chem 277 : 6733 6742.
117. Serrano M, Gutiérrez J, Prieto I, Hermoso JM Salas M (1989) Signals at the bacteriophage φ29 DNA replication origins required for protein p6 binding and activity. EMBO J 8 : 1879 1885.
118. Serrano M, Salas M Hermoso JM (1990) A novel nucleoprotein complex at a replication origin. Science 248 : 1012 1016.
119. Serrano M, Gutierrez C, Salas M Hermoso JM (1993a) Superhelical path of the DNA in the nucleoprotein complex that activates the initiation of phage φ29 DNA replication. J Mol Biol 230 : 248 259.
120. Serrano M, Salas M Hermoso JM (1993b) Multimeric complexes formed by DNA-binding proteins of low sequence specificity. Trends Biochem Sci 18 : 202 206.
121. Serrano-Heras G, Salas M Bravo A (2003) In vivo assembly of phage φ29 replication protein p1 into membrane-associated multimeric structures. J Biol Chem 278 : 40771 40777.
122. Serrano-Heras G, Salas M Bravo A (2006) A uracil-DNA glycosylase inhibitor encoded by a non-uracil containing viral DNA. J Biol Chem 281 : 7068 7074.
123. Shore D, Langowski J Baldwin RL (1981) DNA flexibility studied by covalent closure of short fragments into circles. P Natl Acad Sci USA 78 : 4833 4837.
124. Sogo JM, Inciarte MR, Corral J, Viñuela E Salas M (1979) RNA polymerase binding sites and transcription map of the DNA of Bacillus subtilis phage φ29. J Mol Biol 127 : 411 436.
125. Sorel I, Piétrement O, Hamon L, Baconnais S, Cam EL Pastré D (2006) The EcoRI-DNA complex as a model for investigating protein-DNA interactions by atomic force microscopy. Biochemistry 45 : 14675 14682.
126. Svetlov V Nudler E (2009) Macromolecular micromovements: how RNA polymerase translocates. Curr Opin Struc Biol 19 : 701 707.
127. Toulokhonov I, Zhang J, Palangat M Landick R (2007) A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol Cell 27 : 406 419.
128. van Hijum SA, Medema MH Kuipers OP (2009) Mechanisms and evolution of control logic in prokaryotic transcriptional regulation. Microbiol Mol Biol R 73 : 481 509.
129. Vassylyev DG, Sekine S, Laptenko O, Lee J, Vassylyeva MN, Borukhov S Yokoyama S (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature 417 : 712 719. (Pubitemid 34640620)
130. von Hippel PH (1994) Protein-DNA recognition: new perspectives and underlying themes. Science 263 : 769 770.
131. Voskuil MI, Voepel K Chambliss GH (1995) The -16 region, a vital sequence for the utilization of a promoter in Bacillus subtilis and Escherichia coli. Mol Microbiol 17 : 271 279.
132. Wang D, Bushnell DA, Huang X, Westover KD, Levitt M Kornberg RD (2009) Structural basis of transcription: backtracked RNA polymerase II at 3.4 angstrom resolution. Science 324 : 1203 1206.
133. Whiteley HR, Ramey WD, Spiegelman GD Holder RD (1986) Modulation of in vivo and in vitro transcription of bacteriophage φ29 early genes. Virology 155 : 92 401.
134. Yang J, Hwang JS, Camakaris H, Irawaty W, Ishihama A Pittard J (2004) Mode of action of the TyrR protein: repression and activation of the tyrP promoter of Escherichia coli. Mol Microbiol 52 : 243 256.
135. Young BA, Gruber TM Gross CA (2002) Views of transcription initiation. Cell 109 : 417 420.
136. Zhang G, Campbell EA, Minakhin L, Richter C, Severinov K Darst SA (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 resolution. Cell 98 : 811 824.