The structure of a DnaA/HobA complex from Helicobacter pylori provides insight into regulation of DNA replication in bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 50, 2009, Pages 21115-21120

  Natrajan, Ganesh ^a,d   Noirot Gros, Marie Francoise ^b   Zawilak Pawlik, Anna ^c   Kapp, Ulrike ^a   Terradot, Laurent ^a  

^a EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^b CEMAGREF   (France)

^c INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

DiaA; Isothermal titration calorimetry; Replication regulators; X ray crystallography

Indexed keywords

BACTERIAL DNA; OLIGOMER; REPLICATION INITIATOR PROTEIN DNAA;

ARTICLE; BACTERIAL MUTATION; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DNA BINDING; DNA REPLICATION; DNA STRUCTURE; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; HELICOBACTER PYLORI; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA REPLICATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; HELICOBACTER PYLORI; PROTEIN BINDING; PROTEIN MULTIMERIZATION; REPLICATION ORIGIN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER PYLORI; NEGIBACTERIA;

EID: 75849129293     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0908966106     Document Type: Article

References (39)

1. Kaguni JM, Kornberg A (1984) Replication initiated at the origin (oriC) of the E. coli chromosome reconstituted with purified enzymes. Cell 38:183-190.
2. Mott ML, Berger JM (2007) DNA replication initiation: Mechanisms and regulation in bacteria. Nat Rev Microbiol 5:343-354.
3. Kaguni JM (2006) DnaA: Controlling the initiation of bacterial DNA replication and more. Annu Rev Microbiol 60:351-371.
4. Messer W, et al. Functional domains of DnaA proteins. Biochimie 81:819-825, 1999.
5. Weigel C, et al. (1999) The N-terminus promotes oligomerization of the Escherichia coli initiator protein DnaA. Mol Microbiol 34:53-66.
6. Simmons LA, Felczak M, Kaguni JM (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.
7. Seitz H, Weigel C, Messer W (2000) The interaction domains of the DnaA and DnaB replication proteins of Escherichia coli. Mol Microbiol 37:1270-1279.
8. Sutton MD, Carr KM, Vicente M, Kaguni JM (1998) Escherichia coli DnaA protein. The N-terminal domain and loading of DnaB helicase at the E. coli chromosomal origin. J Biol Chem 273:34255-34262.
9. Lowery TJ, et al. (2007) NMR structure of the N-terminal domain of the replication initiator protein DnaA. J Struct Funct Genomics 8:11-17.
10. Abe Y, et al. (2007) Structure and function of DnaA N-terminal domains: Specific sites and mechanisms in inter-DnaA interaction and in DnaB helicase loading on oriC. J Biol Chem 282:17816-17827.
11. Erzberger JP, Pirruccello MM, Berger JM (2002) The structure of bacterial DnaA: Implications for general mechanisms underlying DNA replication initiation. EMBO J 21:4763-4773.
12. Fujikawa N, et al. (2003) Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res 31:2077-2086.
13. Erzberger JP, Mott ML, Berger JM (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat Struct Mol Biol 13:676-683.
14. Kato J, Katayama T (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20:4253-4262.
15. Chodavarapu S, Felczak MM,Yaniv JR, Kaguni JM (2008) Escherichia coliDnaAinteracts with HU in initiation at the E. coli replication origin. Mol Microbiol 67:781-792.
16. Keyamura K, et al. (2007) The interaction of DiaA and DnaA regulates the replication cycle in E. coli by directly promoting ATP DnaA-specific initiation complexes. Genes Dev 21:2083-2099.
17. Mott ML, Erzberger JP, Coons MM, Berger JM (2008) Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell 135:623-634.
18. Zakrzewska-Czerwinska J, Jakimowicz D, Zawilak-Pawlik A, Messer W (2007) Regulation of the initiation of chromosomal replication in bacteria. FEMS Microbiol Rev 31:378-387.
19. Soufo CD, et al. (2008) Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis. Dev Cell 15:935-941.
20. Noirot-Gros MF, et al. (2006) Functional dissection of YabA, a negative regulator of DNA replication initiation in Bacillus subtilis. Proc Natl Acad Sci USA 103:2368-2373.
21. Gruber S, Errington J (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137:685-696.
22. Murray H, Errington J (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135:74-84.
23. Tomb JF, et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
24. Terradot L, et al. (2004) Biochemical characterization of protein complexes from the Helicobacter pylori protein interaction map: Strategies for complex formation and evidence for novel interactions within type IV secretion systems. Mol Cell Proteomics 3:809-819.
25. Rain JC, et al. (2001) The protein-protein interactionmapof Helicobacter pylori. Nature 409:211-215.
26. Zawilak-Pawlik A, et al. (2007) HobA-a novel protein involved in initiation of chromosomal replication in Helicobacter pylori. Mol Microbiol 65:979-994.
27. Natrajan G, Hall DR, Thompson AC, Gutsche I, Terradot L (2007) Structural similarity between the DnaA-binding proteins HobA (HP1230) from Helicobacter pylori and DiaA from Escherichia coli. Mol Microbiol 65:995-1005.
28. Ishida T, et al. (2004) DiaA, a novel DnaA-binding protein, ensures the timely initiation of Escherichia coli chromosome replication. J Biol Chem 279:45546-45555.
29. Flatten I, Morigen, Skarstad K (2009) DnaA protein interacts with RNA polymerase and partially protects it from the effect of rifampicin. Mol Microbiol 71:1018-1030.
30. Chodavarapu S, Gomez R, Vicente M, Kaguni JM (2008) Escherichia coli Dps interacts with DnaA protein to impede initiation: Amodel of adaptive mutation. Mol Microbiol 67:1331-1346.
31. Ozaki S, et al. (2008) A common mechanism for the ATP-DnaA-dependent formation of open complexes at the replication origin. J Biol Chem 283:8351-8362.
32. Su'etsugu M, Shimuta TR, Ishida T, Kawakami H, Katayama T (2005) Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J Biol Chem 280:6528-6536.
33. Katayama T (2008) Roles for the AAA+ motifs of DnaA in the initiation of DNA replication. Biochem Soc Trans 36:78-82.
34. Keyamura K, Abe Y, Higashi M, Ueda T, Katayama T (2009) DiaA dynamics are coupled with changes in initial origin complexes leading to helicase loading. J Biol Chem 24:24.
35. Zawilak A, et al. (2001) Identification of a putative chromosomal replication origin from Helicobacter pylori and its interaction with the initiator protein DnaA. Nucleic Acids Res 29:2251-2259.
36. Soni RK, Mehra P, Mukhopadhyay G, Dhar SK (2005) Helicobacter pylori DnaB helicase can bypass Escherichia coli DnaC function in vivo. Biochem J 389:541-548.
37. Nitharwal RG, et al. (2007) The domain structure of Helicobacter pylori DnaB helicase: The N-terminal domain can be dispensable for helicase activity whereas the extreme C-terminal region is essential for its function. Nucleic Acids Res 35:2861-2874.
38. Felczak MM,Simmons LA, Kaguni JM (2005) An essential tryptophan of Escherichia coli DnaA protein functions in oligomerization at the E. coli replication origin. J Biol Chem 280:24627-24633.
39. Fossum S, et al. (2008) A robust screen for novel antibiotics: Specific knockout of the initiator of bacterial DNA replication. FEMS Microbiol Lett 281:210-214.