Opening-closing dynamics of the mitochondrial transcription pre-initiation complex

Nucleic Acids Research

Volumn 40, Issue 1, 2012, Pages 371-380

  Kim, Hajin ^a,b   Tang, Guo Qing ^c   Patel, Smita S ^c   Ha, Taekjip ^a,b  

^a University of Illinois at Urbana Champaign   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INITIATION FACTOR; PROTEIN MTF1; PROTEIN RPO41; RNA POLYMERASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DNA DENATURATION; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION;

ADENOSINE TRIPHOSPHATE; DNA-DIRECTED RNA POLYMERASES; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 84855273566     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr736     Document Type: Article

References (45)

1. DeHaseth, P.L., Zupancic, M.L. and Record, M.T. Jr (1998) RNA polymerase-promoter interactions: the comings and goings of RNA polymerase. J. Bacteriol., 180, 3019-3025. (Pubitemid 28285012)
2. Bandwar, R.P. and Patel, S.S. (2001) Peculiar 2-aminopurine fluorescence monitors the dynamics of open complex formation by bacteriophage T7 RNA polymerase. J. Biol. Chem., 276, 14075-14082. (Pubitemid 37391792)
3. DeHaseth, P.L. and Helmann, J.D. (1995) Open complex formation by Escherichia coli RNA polymerase: the mechanism of polymerase-induced strand separation of double helical DNA. Mol. Microbiol., 16, 817-824.
4. Roy, S., Lim, H.M., Liu, M. and Adhya, S. (2004) Asynchronous basepair openings in transcription initiation: CRP enhances the rate-limiting step. EMBO J., 23, 869-875. (Pubitemid 38418753)
5. Wellington, S.R. and Spiegelman, G.B. (1993) The kinetics of formation of complexes between Escherichia coli RNA polymerase and the rrnB P1 and P2 promoters of Bacillus subtilis. Effects of guanosine tetraphosphate on select steps of transcription initiation. J. Biol. Chem., 268, 7205-7214. (Pubitemid 23105611)
6. Holstege, F.C., van der Vliet, P.C. and Timmers, H.T. (1996) Opening of an RNA polymerase II promoter occurs in two distinct steps and requires the basal transcription factors IIE and IIH. EMBO J., 15, 1666-1677. (Pubitemid 26112389)
7. Record, M.T., Reznikoff, W.S., Craig, M.L., McQuade, K.L. and Schlax, P.J. (1996) In Neidhardt, F.C., Curtiss, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S., Riley, M., Schaechter, M. and Umbarger, H.E. (eds), Escherichia coli and Salmonella Cellular and Molecular Biology. ASM Press, Washington, DC, pp. 792-821.
8. Masters, B.S., Stohl, L.L. and Clayton, D.A. (1987) Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7. Cell, 51, 89-99.
9. Gaspari, M., Larsson, N.G. and Gustafsson, C.M. (2004) The transcription machinery in mammalian mitochondria. Biochim. Biophys. Acta, 1659, 148-152. (Pubitemid 39575501)
10. Cermakian, N., Ikeda, T.M., Cedergren, R. and Gray, M.W. (1996) Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res., 24, 648-654.
11. Schinkel, A.H., Koerkamp, M.J., Touw, E.P. and Tabak, H.F. (1987) Specificity factor of yeast mitochondrial RNA polymerase. Purification and interaction with core RNA polymerase. J. Biol. Chem., 262, 12785-12791.
12. Fisher, R.P. and Clayton, D.A. (1988) Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol., 8, 3496-3509.
13. Tracy, R.L. and Stern, D.B. (1995) Mitochondrial transcription initiation: promoter structures and RNA polymerases. Curr. Genet., 28, 205-216.
14. Matsunaga, M. and Jaehning, J.A. (2004) Intrinsic promoter recognition by a "core" RNA polymerase. J. Biol. Chem., 279, 44239-44242. (Pubitemid 39430826)
15. Jang, S.H. and Jaehning, J.A. (1991) The yeast mitochondrial RNA polymerase specificity factor, MTF1, is similar to bacterial sigma factors. J. Biol. Chem., 266, 22671-22677. (Pubitemid 21908702)
16. Winkley, C.S., Keller, M.J. and Jaehning, J.A. (1985) A multicomponent mitochondrial RNA polymerase from Saccharomyces cerevisiae. J. Biol. Chem., 260, 14214-14223. (Pubitemid 16197491)
17. Shutt, T.E., Lodeiro, M.F., Cotney, J., Cameron, C.E. and Shadel, G.S. Core human mitochondrial transcription apparatus is a regulated two-component system in vitro. Proc. Natl Acad. Sci. USA, 107, 12133-12138.
18. Paratkar, S. and Patel, S.S. (2010) Mitochondrial transcription factor Mtf1 traps the unwound non-template strand to facilitate open complex formation. J. Biol. Chem., 285, 3949-3956.
19. Tang, G.-Q., Paratkar, S. and Patel, S.S. (2009) Fluorescence mapping of the open complex of yeast mitochondrial RNA polymerase. J. Biol. Chem., 284, 5514-5522.
20. Savkina, M., Temiakov, D., McAllister, W.T. and Anikin, M. (2010) Multiple functions of yeast mitochondrial transcription factor Mtf1p during initiation. J. Biol. Chem., 285, 3957-3964.
21. Grünberg, S., Bartlett, M.S., Naji, S. and Thomm, M. (2007) Transcription factor E is a part of transcription elongation complexes. J. Biol. Chem., 282, 35482-35490. (Pubitemid 350277092)
22. Grohmann, D. (2009) Molecular mechanisms of archaeal RNA polymerase. Biochem. Soc. Trans., 37, 12.
23. Werner, F. and Weinzierl, R.O.J. (2005) Direct modulation of RNA polymerase core functions by basal transcription factors. Mol. Cell. Biol., 25, 8344-8355. (Pubitemid 41263022)
24. Chen, H.-T., Warfield, L. and Hahn, S. (2007) The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat. Struct. Mol. Biol., 14, 696-703. (Pubitemid 47220058)
25. Forget, D., Langelier, M.-F., Therien, C., Trinh, V. and Coulombe, B. (2004) Photo-cross-linking of a purified preinitiation complex reveals central roles for the RNA polymerase II mobile clamp and TFIIE in initiation mechanisms. Mol. Cell. Biol., 24, 1122-1131. (Pubitemid 38112175)
26. Villemain, J., Guajardo, R. and Sousa, R. (1997) Role of open complex instability in kinetic promoter selection by bacteriophage T7 RNA polymerase. J. Mol. Biol., 273, 958-977. (Pubitemid 27501153)
27. Gourse, R.L. (1988) Visualization and quantitative analysis of complex formation between E.coli RNA polymerase and an rRNA promoter in vitro. Nucleic Acids Res., 16, 9789-9809.
28. Stano, N.M., Levin, M.K. and Patel, S.S. (2002) The+2 NTP binding drives open complex formation in T7 RNA polymerase. J. Biol. Chem., 277, 37292-37300.
29. Gaal, T., Bartlett, M.S., Ross, W., Turnbough, C.L. and Gourse, R.L. (1997) Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science, 278, 2092-2097. (Pubitemid 28028313)
30. Amiott, E.A. and Jaehning, J.A. (2006) Sensitivity of the yeast mitochondrial RNA polymerase to+1 and+2 initiating nucleotides. J. Biol. Chem., 281, 34982-34988. (Pubitemid 46036537)
31. Amiott, E.A. and Jaehning, J.A. (2006) Mitochondrial transcription is regulated via an ATP "sensing" mechanism that couples RNA abundance to respiration. Mol. Cell, 22, 329-338.
32. Ha, T., Enderle, T., Ogletree, D.F., Chemla, D.S., Selvin, P.R. and Weiss, S. (1996) Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl Acad. Sci. USA, 93, 6264-6268. (Pubitemid 26230293)
33. Kapanidis, A.N., Margeat, E., Ho, S.O., Kortkhonjia, E., Weiss, S. and Ebright, R.H. (2006) Initial transcription by RNA polymerase proceeds through a DNA-scrunching mechanism. Science, 314, 1144-1147. (Pubitemid 44789044)
34. Tang, G.-Q., Roy, R., Bandwar, R.P., Ha, T. and Patel, S.S. (2009) Real-time observation of the transition from transcription initiation to elongation of the RNA polymerase. Proc. Natl Acad. Sci. USA, 106, 22175-22180.
35. Tang, G.-Q., Roy, R., Ha, T. and Patel, S.S. (2008) Transcription initiation in a single-subunit RNA polymerase proceeds through DNA scrunching and rotation of the N-terminal subdomains. Mol. Cell, 30, 567-577. (Pubitemid 351755060)
36. Cisse, I., Okumus, B., Joo, C. and Ha, T. (2007) Fueling protein? DNA interactions inside porous nanocontainers. Proc. Natl Acad. Sci. USA, 104, 12646-12650. (Pubitemid 47255208)
37. Mangus, D.A., Jang, S.H. and Jaehning, J.A. (1994) Release of the yeast mitochondrial RNA polymerase specificity factor from transcription complexes. J. Biol. Chem., 269, 26568-26574. (Pubitemid 24328486)
38. Biswas, T.K., Edwards, J.C., Rabinowitz, M. and Getz, G.S. (1985) Characterization of a yeast mitochondrial promoter by deletion mutagenesis. Proc. Natl Acad. Sci. USA, 82, 1954-1958. (Pubitemid 15060819)
39. Gaspari, M., Falkenberg, M., Larsson, N.-G. and Gustafsson, C.M. (2004) The mitochondrial RNA polymerase contributes critically to promoter specificity in mammalian cells. EMBO J., 23, 4606-4614. (Pubitemid 39657860)
40. Bonawitz, N.D., Clayton, D.A. and Shadel, G.S. (2006) Initiation and beyond: multiple functions of the human mitochondrial transcription machinery. Mol. Cell, 24, 813-825. (Pubitemid 46001607)
41. Sologub, M., Litonin, D., Anikin, M., Mustaev, A. and Temiakov, D. (2009) TFB2 Is a transient component of the catalytic site of the human mitochondrial RNA polymerase. Cell, 139, 934-944.
42. Litonin, D., Sologub, M., Shi, Y., Savkina, M., Anikin, M., Falkenberg, M., Gustafsson, C.M. and Temiakov, D. Human mitochondrial transcription revisited. J. Biol. Chem., 285, 18129-18133.
43. Dairaghi, D.J., Shadel, G.S. and Clayton, D.A. (1995) Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim. Biophys. Acta, 1271, 127-134.
44. Diffley, J.F. and Stillman, B. (1991) A close relative of the nuclear, chromosomal high-mobility group protein HMG1 in yeast mitochondria. Proc. Natl Acad. Sci. USA, 88, 7864-7868. (Pubitemid 21915255)
45. Dairaghi, D.J., Shadel, G.S. and Clayton, D.A. (1995) Addition of a 29 residue carboxyl-terminal tail converts a simple HMG box-containing protein into a transcriptional activator. J. Mol. Biol., 249, 11-28.