The intrinsic ATPase activity of Mycobacterium tuberculosis DnaA promotes rapid oligomerization of DnaA on oriC

Molecular Microbiology

Volumn 59, Issue 6, 2006, Pages 1876-1890

  Madiraju, Murty V V S ^c   Moomey, Meredith ^c   Neuenschwander, Pierre F ^c   Muniruzzaman, Syed ^a,c   Yamamoto, Kohji ^b,c   Grimwade, Julia E ^d   Rajagopalan, Malini ^a  

^a XAVIER UNIVERSITY OF LOUISIANA   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

^d Florida Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA A;

ARTICLE; DNA REPLICATION ORIGIN; ENZYME ACTIVITY; ENZYME BINDING; ESCHERICHIA COLI; GENE MUTATION; MUTANT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; SURFACE PLASMON RESONANCE;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; BASE SEQUENCE; CHROMOSOMES, BACTERIAL; DNA FOOTPRINTING; DNA REPLICATION; DNA-BINDING PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; MYCOBACTERIUM TUBERCULOSIS; REPLICATION ORIGIN; SURFACE PLASMON RESONANCE;

ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS;

EID: 33645462018     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05068.x     Document Type: Article

References (48)

1. Bondeson K. Frostell-Karlsson A. Fagerstam L. Magnusson G. 1993 Lactose repressor-operator DNA interactions: kinetic analyses by a surface plasmon resonance biosensor. Anal Biochem 214 245 251.
2. Bramhill D. Kornberg A. 1988a A model for initiation at origins of DNA replication. Cell 54 915 918.
3. Bramhill D. Kornberg A. 1988b Duplex opening by dnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52 743 755.
4. Camara J.E. Skarstad K. Crooke E. 2003 Controlled initiation of chromosomal replication in Escherichia coli requires functional Hda protein. J Bacteriol 185 3244 3248.
5. Camara J.E. Breier A.M. Brendler T. Austin S. Cozzarelli N.R. Crooke E. 2005 Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep 6 736 741.
6. Castuma C.E. Crooke E. Kornberg A. 1993 Fluid membranes with acidic domains activate DnaA, the initiator protein of replication in Escherichia coli. J Biol Chem 268 24665 24668.
7. Cole S.T. Brosch R. Parkhill J. Garnier T. Churcher C. Harris D. et al. 1998 Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393 537 544.
8. Crooke E. Castuma C.E. Kornberg A. 1992 The chromosome origin of Escherichia coli stabilizes DnaA protein during rejuvenation by phospholipids. J Biol Chem 267 16779 16782.
9. Crooke E. Thresher R. Hwang D.S. Griffith J. Kornberg A. 1993 Replicatively active complexes of DnaA protein and the Escherichia coli chromosomal origin observed in the electron microscope. J Mol Biol 233 16 24.
10. Dziadek J. Rajagopalan M. Parish T. Kurepina N. Greendyke R. Kreiswirth B.N. Madiraju M.V. 2002 Mutations in the CCGTTCACA DnaA box of Mycobacterium tuberculosis oriC that abolish replication of oriC plasmids are tolerated on the chromosome. J Bacteriol 184 3848 3855.
11. Erzberger J.P. Pirruccello M.M. Berger J.M. 2002 The structure of bacterial DnaA: implications for general mechanisms underlying DNA replication initiation. EMBO J 21 4763 4773.
12. Fukuoka T. Moriya S. Yoshikawa H. Ogasawara N. 1990 Purification and characterization of an initiation protein for chromosomal replication, DnaA, in Bacillus subtilis. J Biochem (Tokyo) 107 732 739.
13. Greendyke R. Rajagopalan M. Parish T. Madiraju M.V. 2002 Conditional expression of Mycobacterium smegmatis dnaA, an essential DNA replication gene. Microbiology 148 3887 3900.
14. Grimwade J.E. Ryan V.T. Leonard A.C. 2000 IHF redistributes bound initiator protein, DnaA, on supercoiled oriC of Escherichia coli. Mol Microbiol 35 835 844.
15. Guo L. Katayama T. Seyama Y. Sekimizu K. Miki T. 1999 Isolation and characterization of novel cold-sensitive dnaA mutants of Escherichia coli. FEMS Microbiol Lett 176 357 366.
16. Jacob F. Brenner S. Cuzin F. 1963 On the regulation of replication in bacteria. Cold Spring Harbor Symnp Quant Biol 28 329 348.
17. Katayama T. 2001 Feedback controls restrain the initiation of Escherichia coli chromosomal replication. Mol Microbiol 41 9 17.
18. Katayama T. Sekimizu K. 1999 Inactivation of Escherichia coli DnaA protein by DNA polymerase III and negative regulations for initiation of chromosomal replication. Biochimie 81 835 840.
19. Katayama T. Kubota T. Kurokawa K. Crooke E. Sekimizu K. 1998 The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94 61 71.
20. Kato J. Katayama T. 2001 Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20 4253 4262.
21. Kawakami H. Keyamura K. Katayama T. 2005 Formation of an ATP-DnaA-specific initiation complex requires DnaA Arginine 285, a conserved motif in the AAA+ protein family. J Biol Chem 280 27420 27430.
22. Lee D.G. Bell S.P. 2000 ATPase switches controlling DNA replication initiation. Curr Opin Cell Biol 12 280 285.
23. Leonard A.C. Grimwade J.E. 2005 Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Mol Microbiol 55 978 985.
24. Li Z. Crooke E. 1999 Functional analysis of affinity-purified polyhistidine-tagged DnaA protein. Protein Expr Purif 17 41 48.
25. McGarry K.C. Ryan V.T. Grimwade J.E. Leonard A.C. 2004 Two discriminatory binding sites in the Escherichia coli replication origin are required for DNA strand opening by initiator DnaA-ATP. Proc Natl Acad Sci USA 101 2811 2816.
26. Margulies C. Kaguni J.M. 1996 Ordered and sequential binding of DnaA protein to oriC, the chromosomal origin of Escherichia coli. J Biol Chem 271 17035 17040.
27. Messer W. 2002 The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol Rev 26 355 374.
28. Messer W. Blaesing F. Jakimowicz D. Krause M. Majka J. Nardmann J. et al. 2001 Bacterial replication initiator DnaA. Rules for DnaA binding and roles of DnaA in origin unwinding and helicase loading. Biochimie 83 5 12.
29. Munoz-Elias E.J. Timm J. Botha T. Chan W.T. Gomez J.E. McKinney J.D. 2005 Replication dynamics of Mycobacterium tuberculosis in chronically infected mice. Infect Immun 73 546 551.
30. Nishida S. Fujimitsu K. Sekimizu K. Ohmura T. Ueda T. Katayama T. 2002 A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: evidence from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo. J Biol Chem 277 14986 14995.
31. Parish T. Stoker N.G. 2000 Use of a flexible cassette method to generate a double unmarked Mycobacterium tuberculosis tlyA plcABC mutant by gene replacement. Microbiology 146 1969 1975.
32. Qin M.H. Madiraju M.V. Zachariah S. Rajagopalan M. 1997 Characterization of the oriC region of Mycobacterium smegmatis. J Bacteriol 179 6311 6317.
33. Qin M.H. Madiraju M.V. Rajagopalan M. 1999 Characterization of the functional replication origin of Mycobacterium tuberculosis. Gene 233 121 130.
34. Rajagopalan M. Qin M.H. Nash D.R. Madiraju M.V. 1995 Mycobacterium smegmatis dnaA region and autonomous replication activity. J Bacteriol 177 6527 6535.
35. Ryan V.T. Grimwade J.E. Camara J.E. Crooke E. Leonard A.C. 2004 Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA. Mol Microbiol 51 1347 1359.
36. Salazar L. Fsihi H. de Rossi E. Riccardi G. Rios C. Cole S.T. Takiff H.E. 1996 Organization of the origins of replication of the chromosomes of Mycobacterium smegmatis, Mycobacterium leprae and Mycobacterium tuberculosis and isolation of a functional origin from M. smegmatis. Mol Microbiol 20 283 293.
37. Sasse-Dwight S. Gralla J.D. 1991 Footprinting protein-DNA complexes in vivo. Methods Enzymol 208 146 168.
38. Schaper S. Messer W. 1995 Interaction of the initiator protein DnaA of Escherichia coli with its DNA target. J Biol Chem 270 17622 17626.
39. Sekimizu K. Bramhill D. Kornberg A. 1987 ATP activates dnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50 259 265.
40. Simmons L.A. Felczak M. Kaguni J.M. 2003 DnaA protein of Escherichia coli: oligomerization at the E. coli chromosomal origin is required for initiation and involves specific N-terminal amino acids. Mol Microbiol 49 849 858.
41. Speck C. Messer W. 2001 Mechanism of origin unwinding: sequential binding of DnaA to double- and single-stranded DNA. EMBO J 20 1469 1476.
42. Speck C. Weigel C. Messer W. 1999 ATP- and ADP-dnaA protein, a molecular switch in gene regulation. EMBO J 18 6169 6176.
43. Stover C.K. de la Cruz V.F. Fuerst T.R. Burlein J.E. Benson L.A. Bennett L.T. et al. 1991 New use of BCG for recombinant vaccines. Nature 351 456 460.
44. Takata M. Guo L. Katayama T. Hase M. Seyama Y. Miki T. Sekimizu K. 2000 Mutant DnaA proteins defective in duplex opening of oriC, the origin of chromosomal DNA replication in Escherichia coli. Mol Microbiol 35 454 462.
45. Wayne L.G. 1994 Dormancy of Mycobacterium tuberculosis and latency of disease. Eur J Clin Microbiol Infect Dis 13 908 914.
46. Yamamoto K. Muniruzzaman S. Rajagopalan M. Madiraju M.V. 2002 Modulation of Mycobacterium tuberculosis DnaA protein-adenine-nucleotide interactions by acidic phospholipids. Biochem J 363 305 311.
47. Zawilak A. Kois A. Konopa G. Smulczyk-Krawczyszyn A. Zakrzewska- Czerwinska J. 2004 Mycobacterium tuberculosis DnaA initiator protein: purification and DNA-binding requirements. Biochem J 382 247 252.
48. Zawilak-Pawlik A. Kois A. Majka J. Jakimowicz D. Smulczyk-Krawczyszyn A. Messer W. Zakrzewska-Czerwinska J. 2005 Architecture of bacterial replication initiation complexes - orisomes from four unrelated bacteria. Biochem J 389 471 481.