DNA Adenine Methylation Is Required to Replicate Both Chromosomes Once per Cell Cycle

English version České info

DNA adenine methylation is widely used to control many DNA transactions, including replication. In Escherichia coli, methylation serves to silence newly synthesized (hemimethylated) sister origins. SeqA, a protein that binds to hemimethylated DNA, mediates the silencing, and this is necessary to restrict replication to once per cell cycle. The methylation, however, is not essential for replication initiation per se but appeared so when the origins (oriI and oriII) of the two Vibrio cholerae chromosomes were used to drive plasmid replication in E. coli. Here we show that, as in the case of E. coli, methylation is not essential for oriI when it drives chromosomal replication and is needed for once-per-cell-cycle replication in a SeqA-dependent fashion. We found that oriII also needs SeqA for once-per-cell-cycle replication and, additionally, full methylation for efficient initiator binding. The requirement for initiator binding might suffice to make methylation an essential function in V. cholerae. The structure of oriII suggests that it originated from a plasmid, but unlike plasmids, oriII makes use of methylation for once-per-cell-cycle replication, the norm for chromosomal but not plasmid replication.

Vyšlo v časopise: DNA Adenine Methylation Is Required to Replicate Both Chromosomes Once per Cell Cycle. PLoS Genet 6(5): e32767. doi:10.1371/journal.pgen.1000939
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000939

Souhrn

Zdroje

1. SuzukiMM

BirdA

2008 DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9 465 476

2. MarinusMG

1987 DNA methylation in Escherichia coli. Annu Rev Genet 21 113 131

3. LowDA

CasadesusJ

2008 Clocks and switches: bacterial gene regulation by DNA adenine methylation. Curr Opin Microbiol 11 106 112

4. Lφbner-OlesenA

SkovgaardO

MarinusMG

2005 Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8 154 160

5. CasadesusJ

LowD

2006 Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70 830 856

6. EngelJD

von HippelPH

1978 Effects of methylation on the stability of nucleic acid conformations. Studies at the polymer level. J Biol Chem 253 927 934

7. CollinsM

MyersRM

1987 Alterations in DNA helix stability due to base modifications can be evaluated using denaturing gradient gel electrophoresis. J Mol Biol 198 737 744

8. PolaczekP

KwanK

CampbellJL

1998 GATC motifs may alter the conformation of DNA depending on sequence context and N6-adenine methylation status: possible implications for DNA-protein recognition. Mol Gen Genet 258 488 493

9. CollierJ

McAdamsHH

ShapiroL

2007 A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc Natl Acad Sci U S A 104 17111 17116

10. AbelesA

BrendlerT

AustinS

1993 Evidence of two levels of control of P1 oriR and host oriC replication origins by DNA adenine methylation. J Bacteriol 175 7801 7807

11. NielsenO

Lφbner-OlesenA

2008 Once in a lifetime: strategies for preventing re-replication in prokaryotic and eukaryotic cells. EMBO Rep 9 151 156

12. WaldminghausT

SkarstadK

2009 The Escherichia coli SeqA protein. Plasmid 61 141 150

13. Lφbner-OlesenA

HansenFG

RasmussenKV

MartinB

KuempelPL

1994 The initiation cascade for chromosome replication in wild-type and Dam methyltransferase deficient Escherichia coli cells. EMBO J 13 1856 1862

14. Lφbner-OlesenA

von FreieslebenU

1996 Chromosomal replication incompatibility in Dam methyltransferase deficient Escherichia coli cells. EMBO J 15 5999 6008

15. SkarstadK

Lφbner-OlesenA

2003 Stable co-existence of separate replicons in Escherichia coli is dependent on once-per-cell-cycle initiation. EMBO J 22 140 150

16. PaulssonJ

ChattorajDK

2006 Origin inactivation in bacterial DNA replication control. Mol Microbiol 61 9 15

17. JulioSM

HeithoffDM

ProvenzanoD

KloseKE

SinsheimerRL

2001 DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69 7610 7615

18. EganES

WaldorMK

2003 Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell 114 521 530

19. DuigouS

KnudsenKG

SkovgaardO

EganES

Lφbner-OlesenA

2006 Independent Control of Replication Initiation of the Two Vibrio cholerae Chromosomes by DnaA and RctB. J Bacteriol 188 6419 6424

20. LeonardAC

HelmstetterCE

1988 Replication patterns of multiple plasmids coexisting in Escherichia coli. J Bacteriol 170 1380 1383

21. HeidelbergJF

EisenJA

NelsonWC

ClaytonRA

GwinnML

2000 DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406 477 483

22. LuM

CampbellJL

BoyeE

KlecknerN

1994 SeqA: a negative modulator of replication initiation in E. coli. Cell 77 413 426

23. ParkerB

MarinusMG

1988 A simple and rapid method to obtain substitution mutations in Escherichia coli: isolation of a dam deletion/insertion mutation. Gene 73 531 535

24. BatesDB

AsaiT

CaoY

ChambersMW

CadwellGW

1995 The DnaA box R4 in the minimal oriC is dispensable for initiation of Escherichia coli chromosome replication. Nucleic Acids Res 23 3119 3125

25. SkarstadK

BernanderR

BoyeE

1995 Analysis of DNA replication in vivo by flow cytometry. Methods Enzymol 262 604 613

26. BoyeE

Lφbner-OlesenA

1990 The role of dam methyltransferase in the control of DNA replication in E. coli. Cell 62 981 989

27. CampbellJL

KlecknerN

1990 E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62 967 979

28. Saint-DicD

KehrlJ

FrushourB

KahngLS

2008 Excess SeqA leads to replication arrest and a cell division defect in Vibrio cholerae. J Bacteriol 190 5870 5878

29. SlaterS

WoldS

LuM

BoyeE

SkarstadK

1995 E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82 927 936

30. NielsenHJ

LiY

YoungrenB

HansenFG

AustinS

2006 Progressive segregation of the Escherichia coli chromosome. Mol Microbiol 61 383 393

31. SrivastavaP

ChattorajDK

2007 Selective chromosome amplification in Vibrio cholerae. Mol Microbiol 66 1016 1028

32. MoriyaS

AtlungT

HansenFG

YoshikawaH

OgasawaraN

1992 Cloning of an autonomously replicating sequence (ars) from the Bacillus subtilis chromosome. Mol Microbiol 6 309 315

33. ReisenauerA

KahngLS

McCollumS

ShapiroL

1999 Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181 5135 5139

34. AbelesAL

AustinSJ

1987 P1 plasmid replication requires methylated DNA. EMBO J 6 3185 3189

35. GammieAE

CrosaJH

1991 Roles of DNA adenine methylation in controlling replication of the REPI replicon of plasmid pColV-K30. Mol Microbiol 5 495 503

36. BrendlerT

AustinS

1999 Binding of SeqA protein to DNA requires interaction between two or more complexes bound to separate hemimethylated GATC sequences. EMBO J 18 2304 2310

37. BachT

Morigen

SkarstadK

2008 The initiator protein DnaA contributes to keeping new origins inactivated by promoting the presence of hemimethylated DNA. J Mol Biol 384 1076 1085

38. NieveraC

TorgueJJ

GrimwadeJE

LeonardAC

2006 SeqA blocking of DnaA-oriC interactions ensures staged assembly of the E. coli pre-RC. Mol Cell 24 581 592

39. RasmussenT

JensenRB

SkovgaardO

2007 The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. EMBO J 26 3124 3131

40. MargolinW

2005 FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6 862 871

41. BotelloE

NordströmK

1998 Effects of chromosome underreplication on cell division in Escherichia coli. J Bacteriol 180 6364 6374

42. WrightR

StephensC

ShapiroL

1997 The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 179 5869 5877

43. RobertsonGT

ReisenauerA

WrightR

JensenRB

JensenA

2000 The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182 3482 3489

44. KahngLS

ShapiroL

2001 The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 183 3065 3075

45. CourtDL

SwaminathanS

YuD

WilsonH

BakerT

2003 Mini-lambda: a tractable system for chromosome and BAC engineering. Gene 315 63 69

46. SrivastavaP

FeketeRA

ChattorajDK

2006 Segregation of the replication terminus of the two Vibrio cholerae chromosomes. J Bacteriol 188 1060 1070

47. Venkova-CanovaT

SrivastavaP

ChattorajDK

2006 Transcriptional inactivation of a regulatory site for replication of Vibrio cholerae chromosome II. Proc Natl Acad Sci U S A 103 12051 12056

48. Le RouxF

BinesseJ

SaulnierD

MazelD

2007 Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol 73 777 784

49. BlokeschM

SchoolnikGK

2008 The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J Bacteriol 190 7232 7240

50. BlokeschM

SchoolnikGK

2007 Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog 3 e81 doi:10.1371/journal.ppat.0030081

51. LinDC

GrossmanAD

1998 Identification and characterization of a bacterial chromosome partitioning site. Cell 92 675 685

52. LeeC

KimJ

ShinSG

HwangS

2006 Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J Biotechnol 123 273 280

53. GrantSG

JesseeJ

BloomFR

HanahanD

1990 Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87 4645 4649

54. DemarreG

GueroutAM

Matsumoto-MashimoC

Rowe-MagnusDA

MarliereP

2005 A new family of mobilizable suicide plasmids based on broad host range R388 plasmid (IncW) and RP4 plasmid (IncPalpha) conjugative machineries and their cognate Escherichia coli host strains. Res Microbiol 156 245 255

55. GuzmanLM

BelinD

CarsonMJ

BeckwithJ

1995 Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 4121 4130

56. PhilippeN

AlcarazJP

CoursangeE

GeiselmannJ

SchneiderD

2004 Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51 246 255

57. EganES