DNA Damage Triggers Genetic Exchange in
Many organisms respond to DNA damage by inducing expression of DNA repair genes. We find that the human stomach pathogen Helicobacter pylori instead induces transcription and translation of natural competence genes, thus increasing transformation frequency. Transcription of a lysozyme-like protein that promotes DNA donation from intact cells is also induced. Exogenous DNA modulates the DNA damage response, as both recA and the ability to take up DNA are required for full induction of the response. This feedback loop is active during stomach colonization, indicating a role in the pathogenesis of the bacterium. As patients can be infected with multiple genetically distinct clones of H. pylori, DNA damage induced genetic exchange may facilitate spread of antibiotic resistance and selection of fitter variants through re-assortment of preexisting alleles in this important human pathogen.
Vyšlo v časopise:
DNA Damage Triggers Genetic Exchange in. PLoS Pathog 6(7): e32767. doi:10.1371/journal.ppat.1001026
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001026
Souhrn
Many organisms respond to DNA damage by inducing expression of DNA repair genes. We find that the human stomach pathogen Helicobacter pylori instead induces transcription and translation of natural competence genes, thus increasing transformation frequency. Transcription of a lysozyme-like protein that promotes DNA donation from intact cells is also induced. Exogenous DNA modulates the DNA damage response, as both recA and the ability to take up DNA are required for full induction of the response. This feedback loop is active during stomach colonization, indicating a role in the pathogenesis of the bacterium. As patients can be infected with multiple genetically distinct clones of H. pylori, DNA damage induced genetic exchange may facilitate spread of antibiotic resistance and selection of fitter variants through re-assortment of preexisting alleles in this important human pathogen.
Zdroje
1. PeekRMJr
BlaserMJ
2002 Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2 28 37
2. CheyWD
WongBC
2007 American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol 102 1808 1825
3. GrahamDY
2009 Efficient identification and evaluation of effective Helicobacter pylori therapies. Clin Gastroenterol Hepatol 7 145 148
4. SuerbaumS
SmithJM
BapumiaK
MorelliG
SmithNH
1998 Free recombination within Helicobacter pylori. Proc Natl Acad Sci U S A 95 12619 12624
5. AlmRA
LingLS
MoirDT
KingBL
BrownED
1999 Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397 176 180
6. GressmannH
LinzB
GhaiR
PleissnerKP
SchlapbachR
2005 Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 1 e43
7. SalamaN
GuilleminK
McDanielTK
SherlockG
TompkinsL
2000 A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc Natl Acad Sci U S A 97 14668 14673
8. BaltrusDA
GuilleminK
PhillipsPC
2008 Natural transformation increases the rate of adaptation in the human pathogen Helicobacter pylori. Evolution 62 39 49
9. LuriaSE
DelbruckM
1943 Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics 28 491 511
10. BjörkholmB
SjolundM
FalkPG
BergOG
EngstrandL
2001 Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci U S A 98 14607 14612
11. KangJM
IovineNM
BlaserMJ
2006 A paradigm for direct stress-induced mutation in prokaryotes. FASEB J 20 2476 2485
12. TaylorNS
FoxJG
AkopyantsNS
BergDE
ThompsonN
1995 Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J Clin Microbiol 33 918 923
13. BergDE
GilmanRH
Lelwala-GurugeJ
SrivastavaK
ValdezY
1997 Helicobacter pylori populations in Peruvian patients. Clin Infect Dis 25 996 1002
14. SchwarzS
MorelliG
KusecekB
ManicaA
BallouxF
2008 Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog 4 e1000180
15. SalamaNR
Gonzalez-ValenciaG
DeatherageB
Aviles-JimenezF
AthertonJC
2007 Genetic analysis of Helicobacter pylori strain populations colonizing the stomach at different times postinfection. J Bacteriol 189 3834 3845
16. TalaricoS
GoldBD
FeroJ
ThompsonDT
GuarnerJ
2009 Pediatric Helicobacter pylori isolates display distinct gene coding capacities and virulence gene marker profiles. J Clin Microbiol In Press
17. IsraelDA
SalamaN
KrishnaU
RiegerUM
AthertonJC
2001 Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc Natl Acad Sci U S A 98 14625 14630
18. YehYC
ChangKC
YangJC
FangCT
WangJT
2002 Association of metronidazole resistance and natural competence in Helicobacter pylori. Antimicrob Agents Chemother 46 1564 1567
19. HofreuterD
OdenbreitS
HaasR
2001 Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol Microbiol 41 379 391
20. Alvarez-MartinezCE
ChristiePJ
2009 Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73 775 808
21. BaltrusDA
GuilleminK
2006 Multiple phases of competence occur during the Helicobacter pylori growth cycle. FEMS Microbiol Lett 255 148 155
22. AmundsenSK
FeroJ
HansenLM
CromieGA
SolnickJV
2008 Helicobacter pylori AddAB helicase-nuclease and RecA promote recombination-related DNA repair and survival during stomach colonization. Mol Microbiol 69 994 1007
23. AmundsenSK
FeroJ
SalamaNR
SmithGR
2009 Dual Nuclease and Helicase Activities of Helicobacter pylori AddAB Are Required for DNA Repair, Recombination, and Mouse Infectivity. J Biol Chem 284 16759 16766
24. GalhardoRS
HastingsPJ
RosenbergSM
2007 Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 42 399 435
25. CirzRT
JonesMB
GinglesNA
MinogueTD
JarrahiB
2007 Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J Bacteriol 189 531 539
26. CirzRT
O'NeillBM
HammondJA
HeadSR
RomesbergFE
2006 Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J Bacteriol 188 7101 7110
27. TombJF
WhiteO
KerlavageAR
ClaytonRA
SuttonGG
1997 The complete genome sequence of the gastric pathogen Helicobacter pylori [see comments] [published erratum appears in Nature 1997 Sep 25;389(6649):412]. Nature 388 539 547
28. HanJ
SahinO
BartonYW
ZhangQ
2008 Key role of Mfd in the development of fluoroquinolone resistance in Campylobacter jejuni. PLoS Pathog 4 e1000083
29. PrudhommeM
AttaiechL
SanchezG
MartinB
ClaverysJP
2006 Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313 89 92
30. MooreRA
BecktholdB
WongS
KureishiA
BryanLE
1995 Nucleotide sequence of the gyrA gene and characterization of ciprofloxacin-resistant mutants of Helicobacter pylori. Antimicrob Agents Chemother 39 107 111
31. TusherVG
TibshiraniR
ChuG
2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 5116 5121
32. MarsinS
MathieuA
KortulewskiT
GueroisR
RadicellaJP
2008 Unveiling novel RecO distant orthologues involved in homologous recombination. PLoS Genet 4 e1000146
33. MiyagishimaSY
WolkCP
OsteryoungKW
2005 Identification of cyanobacterial cell division genes by comparative and mutational analyses. Mol Microbiol 56 126 143
34. PerezJC
GroismanEA
2009 Evolution of transcriptional regulatory circuits in bacteria. Cell 138 233 244
35. da RochaRP
PaquolaAC
Marques MdoV
MenckCF
GalhardoRS
2008 Characterization of the SOS regulon of Caulobacter crescentus. J Bacteriol 190 1209 1218
36. KarnholzA
HoeflerC
OdenbreitS
FischerW
HofreuterD
2006 Functional and topological characterization of novel components of the comB DNA transformation competence system in Helicobacter pylori. J Bacteriol 188 882 893
37. SharmaCM
HoffmannS
DarfeuilleF
ReignierJ
FindeissS
The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464 250 5
38. ClaverysJP
PrudhommeM
MartinB
2006 Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Microbiol 60 451 475
39. KangJ
HuangS
BlaserMJ
2005 Structural and functional divergence of MutS2 from bacterial MutS1 and eukaryotic MSH4-MSH5 homologs. J Bacteriol 187 3528 3537
40. MarsichE
ZuccatoP
RizziS
VetereA
ToninE
2002 Helicobacter pylori expresses an autolytic enzyme: gene identification, cloning, and theoretical protein structure. J Bacteriol 184 6270 6279
41. SalamaNR
OttoG
TompkinsL
FalkowS
2001 Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection. Infect Immun 69 730 736
42. JazayeriA
BalestriniA
GarnerE
HaberJE
CostanzoV
2008 Mre11-Rad50-Nbs1-dependent processing of DNA breaks generates oligonucleotides that stimulate ATM activity. EMBO J 27 1953 1962
43. BaldwinDN
ShepherdB
KraemerP
HallMK
SycuroLK
2007 Identification of Helicobacter pylori genes that contribute to stomach colonization. Infect Immun 75 1005 1016
44. MerrellDS
ThompsonLJ
KimCC
MitchellH
TompkinsLS
2003 Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect Immun 71 6510 6525
45. ThompsonLJ
MerrellDS
NeilanBA
MitchellH
LeeA
2003 Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect Immun 71 2643 2655
46. BaltrusDA
AmievaMR
CovacciA
LoweTM
MerrellDS
2008 The Complete Genome Sequence of Helicobacter pylori strain G27. J Bacteriol
47. HahneF
HuberW
GentlemanR
FalconS
2008 Bioconductor Case Studies: Springer Verlag
48. LangfordML
ZabaletaJ
OchoaAC
TestermanTL
McGeeDJ
2006 In vitro and in vivo complementation of the Helicobacter pylori arginase mutant using an intergenic chromosomal site. Helicobacter 11 477 493
49. RoscheWA
FosterPL
2000 Determining mutation rates in bacterial populations. Methods 20 4 17
50. HachemCY
ClarridgeJE
ReddyR
FlammR
EvansDG
1996 Antimicrobial susceptibility testing of Helicobacter pylori. Comparison of E-test, broth microdilution, and disk diffusion for ampicillin, clarithromycin, and metronidazole. Diagn Microbiol Infect Dis 24 37 41
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 7
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- RNA Virus Replication Complexes
- Virus-Infection or 5′ppp-RNA Activates Antiviral Signal through Redistribution of IPS-1 Mediated by MFN1
- Functional Genetic Diversity among Complex Clinical Isolates: Delineation of Conserved Core and Lineage-Specific Transcriptomes during Intracellular Survival
- Extreme CD8 T Cell Requirements for Anti-Malarial Liver-Stage Immunity following Immunization with Radiation Attenuated Sporozoites