Online citations, reference lists, and bibliographies.
← Back to Search

The Escherichia Coli Histone-like Protein HU Has A Role In Stationary Phase Adaptive Mutation

A. B. Williams, P. Foster
Published 2007 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
Stationary phase adaptive mutation in Escherichia coli is thought to be a mechanism by which mutation rates are increased during stressful conditions, increasing the possibility that fitness-enhancing mutations arise. Here we present data showing that the histone-like protein, HU, has a role in the molecular pathway by which adaptive Lac+ mutants arise in E. coli strain FC40. Adaptive Lac+ mutations are largely but not entirely due to error-prone DNA polymerase IV (Pol IV). Mutations in either of the HU subunits, HUα or HUβ, decrease adaptive mutation to Lac+ by both Pol IV-dependent and Pol IV-independent pathways. Additionally, HU mutations inhibit growth-dependent mutations without a reduction in the level of Pol IV. These effects of HU mutations on adaptive mutation and on growth-dependent mutations reveal novel functions for HU in mutagenesis.
This paper references
10.1016/0378-1119(89)90175-3
Participation of hup gene product in replicative transposition of Mu phage in Escherichia coli.
Y. Kano (1989)
10.1128/JB.186.15.4846-4852.2004
Adaptive mutation in Escherichia coli.
P. Foster (2000)
Population dynamics of a Lac- strain of Escherichia coli during selection for lactose utilization.
P. Foster (1994)
10.1126/SCIENCE.8023164
Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs.
P. Foster (1994)
10.1046/j.1365-2958.2003.03704.x
Error‐prone DNA polymerase IV is controlled by the stress‐response sigma factor, RpoS, in Escherichia coli
J. C. Layton (2003)
10.1016/S0300-9084(01)01331-1
The looped domain organization of the nucleoid in histone-like protein defective Escherichia coli strains.
R. Brunetti (2001)
10.1073/PNAS.92.12.5487
Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation.
P. Foster (1995)
Selection was for zeomycin resistance (Zeo). PFB673 and PFB674 were constructed by first transducing either the DhupATKn or DhupBTKn alleles into PFB236 using P1vir bacteriophage selecting for Kn
Borden (2002)
RpoS is required to maintain normal levels of Pol IV during stationary phase (Layton and Foster
Lombardo (2004)
10.1016/0022-2836(81)90525-8
Genetic and sequence analysis of frameshift mutations induced by ICR-191.
M. Calos (1981)
10.1126/SCIENCE.8023163
Adaptive mutation by deletions in small mononucleotide repeats.
S. Rosenberg (1994)
10.1128/JB.184.18.5077-5087.2002
Role of ppGpp in rpoS stationary-phase regulation in Escherichia coli.
M. Hirsch (2002)
10.1017/S001667230003175X
A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria . By Jeffrey H. Miller. Cold Spring Harbor Laboratory Press. 1992. 876 pages. Price $95.00. ISBN 0 87969 349 5.
D. Leach (1993)
10.1038/nrmicro1340
Long-term survival during stationary phase: evolution and the GASP phenotype
S. Finkel (2006)
10.1128/JB.179.5.1550-1554.1997
Nonadaptive mutations occur on the F' episome during adaptive mutation conditions in Escherichia coli.
P. Foster (1997)
10.1534/GENETICS.166.2.669
General stress response regulator RpoS in adaptive mutation and amplification in Escherichia coli.
M. Lombardo (2004)
BW25113 Host strain for PCR-mediated gene inactivation
HUISMAN (1989)
10.1016/0003-2697(74)90440-0
Visualization of catalase on acrylamide gels.
E. D. Gregory (1974)
10.1128/JB.173.14.4482-4492.1991
Stationary-phase-inducible "gearbox" promoters: differential effects of katF mutations and role of sigma 70.
D. Bohannon (1991)
Image Processing with ImageJ. Biophotonics International
Abramoff (2004)
10.1016/0378-1119(88)90443-x
Genetic characterization of the gene hupA encoding the HU-2 protein of Escherichia coli.
Y. Kano (1988)
10.1074/jbc.M201978200
The Bacterial Histone-like Protein HU Specifically Recognizes Similar Structures in All Nucleic Acids
A. Balandina (2002)
pression of the seqA gene is negatively modulated by the HU protein in Escherichia coli
S. A dhya (2002)
The dinB gene encodes a novel Escherichia coli DNA polymerase
J Wagner (1999)
10.1016/0014-5793(79)80518-9
Native Escherichia coli HU protein is a heterotypic dimer
J. Rouvière-Yaniv (1979)
Adaptive reversion of a frameshift mutation in Escherichia coli.
J. Cairns (1991)
10.1146/ANNUREV.MICRO.60.080805.142238
Environmental stress and lesion-bypass DNA polymerases.
T. Nohmi (2006)
10.1016/S0022-2836(64)80049-8
SPECIFICITY OF THE INDUCTION OF THE ENZYMES OF THE LAC OPERON IN ESCHERICHIA COLI.
B. Müller-hill (1964)
10.1109/EMPDP.1994.592460
Image Processing
E. Pissaloux (1994)
Population dynamics of a Lac strain of Escherichia coli during selection for lactose utilization
P. L. Foster (1994)
10.1073/PNAS.0508032102
Nucleoid remodeling by an altered HU protein: reorganization of the transcription program.
S. Kar (2005)
10.1073/PNAS.0308230101
Dual architectural roles of HU: formation of flexible hinges and rigid filaments.
J. van Noort (2004)
WI) and developed using the Westernlight chemiluminescence reagent (Applied Biosystems, Foster City, CA). Densitometric analysis was performed using ImageJ software (version 1.36b
Promega (2004)
10.1128/JB.01706-06
Amplification of lac cannot account for adaptive mutation to Lac+ in Escherichia coli.
J. Stumpf (2007)
10.1006/JMBI.1997.1310
Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival.
L. Claret (1997)
10.1046/j.1365-2443.1996.d01-236.x
Histone‐like protein HU as a specific transcriptional regulator: co‐factor role in repression of gal transcription by GAL repressor
T. Aki (1996)
10.1128/JB.186.15.4838-4843.2004
Adaptive point mutation and adaptive amplification pathways in the Escherichia coli Lac system: stress responses producing genetic change.
S. Rosenberg (2004)
Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol
R Hengge-Aronis (2002)
As shown in Figure 1A, cells with the hupATCm or hupBTKn alleles had an 70% reduction in adaptive mutation. During this experiment the numbers of viable Lac cells on the minimal lactose plates
Kn Huisman (1989)
A defect in RpoS activity would reduce or eliminate katE expression, resulting in a decrease in the katE-encoded HPII catalase activity in cell-free extracts
Schellhorn (1997)
10.1016/S1097-2765(00)80376-7
The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis.
J. Wagner (1999)
10.1111/j.1365-2958.2005.04724.x
Polyphosphate kinase regulates error‐prone replication by DNA polymerase IV in Escherichia coli
J. Stumpf (2005)
10.1021/BI047720T
Gal repressor-operator-HU ternary complex: pathway of repressosome formation.
Siddhartha Roy (2005)
10.1074/JBC.M400021200
Reconstitution of F Factor DNA Replication in Vitro with Purified Proteins*
S. Zzaman (2004)
10.1128/JB.180.15.3750-3756.1998
Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination.
S. Li (1998)
10.1073/PNAS.120163297
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
K. Datsenko (2000)
10.1128/JB.170.9.4286-4292.1988
Transcriptional regulation of katE in Escherichia coli K-12.
H. Schellhorn (1988)
10.1073/pnas.092269199
SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness
Bethany Yeiser (2002)
Immunoblots Standard molecular biology
Ausubel (1988)
A second high affinity HU binding site in the phage Mu transpososome.
B. D. Lavoie (1994)
10.1007/s004380000384
Expression of the seqA gene is negatively modulated by the HU protein in Escherichia coli
H. Lee (2001)
10.1006/ABIO.2000.4668
An easy and accurate agarose gel assay for quantitation of bacterial plasmid copy numbers.
E. Pushnova (2000)
10.1016/J.DNAREP.2006.06.008
Replication arrest-stimulated recombination: Dependence on the RecA paralog, RadA/Sms and translesion polymerase, DinB.
S. Lovett (2006)
recombination intermediates independently of the major Holliday junction resolution complex, RuvABC (Briggs et al
Harris (2004)
10.1093/emboj/16.12.3666
Repressor induced site‐specific binding of HU for transcriptional regulation
T. Aki (1997)
10.1073/PNAS.92.9.3958
Increased sensitivity to gamma irradiation in bacteria lacking protein HU.
F. Boubrik (1995)
10.1016/S1097-2765(01)00204-0
SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification.
G. Mckenzie (2001)
10.1016/0003-2697(84)90204-5
Effects of molecular oxygen on detection of superoxide radical with nitroblue tetrazolium and on activity stains for catalase.
D. Clare (1984)
10.1046/j.1365-2958.2001.02305.x
The Escherichia coli histone‐like protein HU regulates rpoS translation
A. Balandina (2001)
10.1073/PNAS.81.14.4490
Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation.
O. Huisman (1984)
Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli.
P. Foster (1996)
10.1128/jb.177.22.6670-6671.1995
Conjugation is not required for adaptive reversion of an episomal frameshift mutation in Escherichia coli.
P. Foster (1995)
10.1016/S0076-6879(05)09012-9
Methods for determining spontaneous mutation rates.
P. Foster (2006)
10.1128/JB.173.3.1004-1011.1991
Genetic analysis of the recG locus of Escherichia coli K-12 and of its role in recombination and DNA repair.
R. G. Lloyd (1991)
10.1128/JB.172.9.5402-5407.1990
Subunit-specific phenotypes of Salmonella typhimurium HU mutants.
D. Hillyard (1990)
WI) and developed using the Westernlight chemiluminescence reagent (Applied Biosystems, Foster City, CA). Densitometric analysis was performed using ImageJ software (version 1.36b
Promega (2004)
10.1128/JB.186.15.4855-4860.2004
Adaptive mutation: how growth under selection stimulates Lac(+) reversion by increasing target copy number.
J. Roth (2004)
Genetic characterization of the gene hupB encoding the HU-1 protein of Escherichia coli.
Y. Kano (1986)
however, in our model adaptive mutation in E. coli involves upregulation of mutation rates during stressful conditions, thus increasing the possibility that fitness-enhancing mutations
Rosenberg (2004)
Current Protocols in Molecular Biology
Ausubel (1988)
10.1016/0923-2508(91)90094-Q
Are appR and katF the same Escherichia coli gene encoding a new sigma transcription initiation factor?
E. Touati (1991)
10.1006/JMBI.1999.2631
Differential binding of the Escherichia coli HU, homodimeric forms and heterodimeric form to linear, gapped and cruciform DNA.
V. Pinson (1999)
The dinB gene encodes a novel Escherichia coli DNA polymerase, DNA Pol IV, involved in mutagenesis
J. Wagner (1999)
Opposing roles of the holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation.
R. S. Harris (1996)
10.1098/RSTB.2003.1364
Interplay between DNA replication, recombination and repair based on the structure of RecG helicase.
G. S. Briggs (2004)
10.1111/J.1574-6968.1995.TB07764.X
Regulation of hydroperoxidase (catalase) expression in Escherichia coli.
H. Schellhorn (1995)
10.1128/JB.171.7.3704-3712.1989
Multiple defects in Escherichia coli mutants lacking HU protein.
O. Huisman (1989)
10.1128/JB.177.14.4121-4130.1995
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
L. M. Guzmán (1995)
10.1128/JB.184.10.2674-2681.2002
Escherichia coli DNA polymerase III can replicate efficiently past a T-T cis-syn cyclobutane dimer if DNA polymerase V and the 3' to 5' exonuclease proofreading function encoded by dnaQ are inactivated.
A. Borden (2002)
10.1016/S0300-9084(01)01254-8
HU-GFP and DAPI co-localize on the Escherichia coli nucleoid.
M. Wery (2001)
Image processing with ImageJ. Biophotonics Intl
M D Abramoff (2004)
Image processing with ImageJ
M. Abràmoff (2004)
10.1073/PNAS.75.10.4824
beta-Galactosidase chimeras: primary structure of a lac repressor-beta-galactosidase protein.
A. Brake (1978)
Current Protocols in Molecular Biology
F M Ausubel (1988)
10.1128/MMBR.66.3.373-395.2002
Signal Transduction and Regulatory Mechanisms Involved in Control of the σS (RpoS) Subunit of RNA Polymerase
R. Hengge-Aronis (2002)
10.1073/PNAS.94.25.13792
Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA.
S. Kim (1997)
10.1093/emboj/cdg568
Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the β‐clamp
K. Bunting (2003)
10.1074/JBC.M108456200
In Vitro Repression of the gal Promoters by GalR and HU Depends on the Proper Helical Phasing of the Two Operators*
D. Lewis (2002)
10.1016/S0167-4781(97)00044-4
Identification and analysis of the rpoS-dependent promoter of katE, encoding catalase HPII in Escherichia coli.
K. Tanaka (1997)
10.1016/S0092-8674(00)81000-4
A Molecular Switch in a Replication Machine Defined by an Internal Competition for Protein Rings
V. Naktinis (1996)
Effects of molecular oxygen on detection of superoxide radical with nitroblue tetrazolium and on activity stains for catalase
J. R ouviere-Y aniv (1984)
10.1074/JBC.M204826200
Fidelity of Escherichia coli DNA Polymerase IV
S. Kobayashi (2002)
10.1046/j.1365-2958.2002.02868.x
Selective expression of the β‐subunit of nucleoid‐associated protein HU during cold shock in Escherichia coli
M. Giangrossi (2002)
10.1016/J.JMB.2006.02.022
Three-stage regulation of the amphibolic gal operon: from repressosome to GalR-free DNA.
Szabolcs Semsey (2006)
Overexpressing Pol IV
Lopez De Saro (2003)
b-galactosidase chimeras: primary structure of a lac repressor-b-galactosidase protein
A J Brake (1978)
10.1093/emboj/cdg603
Competitive processivity‐clamp usage by DNA polymerases during DNA replication and repair
F. J. López de Saro (2003)



This paper is referenced by
10.1128/JB.00358-10
RpoS, the stress response sigma factor, plays a dual role in the regulation of Escherichia coli's error-prone DNA polymerase IV.
Kimberly A M Storvik (2010)
10.1534/genetics.115.186163
Salvador Luria and Max Delbrück on Random Mutation and Fluctuation Tests
A. Murray (2016)
10.1111/j.1574-6976.2008.00142.x
A global view of antibiotic resistance.
J. Martínez (2009)
Role of translesion DNA polymerases in mutagenesis and DNA damage tolerance in Pseudomonads
Tatjana Jatsenko (2018)
10.21775/cimb.013.001
Functional evolution of bacterial histone-like HU proteins.
A. Grove (2011)
10.1111/j.1365-2958.2011.07590.x
Escherichia coli Rep DNA helicase and error‐prone DNA polymerase IV interact physically and functionally
Thomas E Sladewski (2011)
10.1007/s00284-008-9340-4
HU Participates in Expression of a Specific Set of Genes Required for Growth and Survival at Acidic pH in Escherichia coli
Hongkai Bi (2008)
10.1002/9780470015902.A0023608
Stress-induced Mutagenesis in Bacteria
P. Foster (2011)
10.1111/j.1365-2958.2008.06117.x
Promoter specificity for 6S RNA regulation of transcription is determined by core promoter sequences and competition for region 4.2 of σ70
Amy T. Cavanagh (2008)
10.1534/g3.111.001057
Double-Strand Break Repair and Holliday Junction Processing Are Required for Chromosome Processing in Stationary-Phase Escherichia coli Cells
Ashley B. Williams (2011)
Development of acetic-acid tolerant Zymomonas mobilis strains through adaptation
Y. Wang (2008)
10.26180/5BBFF8E0455A2
Investigating members of the Omp85 protein superfamily in Klebsiella pneumoniae
Von Vergal Ligutum Torres (2019)
10.1128/JB.00101-15
Interactions and Localization of Escherichia coli Error-Prone DNA Polymerase IV after DNA Damage.
Sarita Mallik (2015)
10.1128/JB.01166-10
The SMC-like protein complex SbcCD enhances DNA polymerase IV-dependent spontaneous mutation in Escherichia coli.
Kimberly A M Storvik (2011)
10.1016/j.dnarep.2019.102745
Integration Host Factor IHF facilitates homologous recombination and mutagenic processes in Pseudomonas putida.
Katren Mikkel (2019)
10.1534/genetics.115.178970
Roles of Nucleoid-Associated Proteins in Stress-Induced Mutagenic Break Repair in Starving Escherichia coli
J. M. Moore (2015)
One-step purification of histone-like protein ( HU ) from Halobacillus litoralis
P. Ghadam (2015)
10.3390/microorganisms8010025
Mutation and Recombination Rates Vary Across Bacterial Chromosome
M. Kivisaar (2019)
10.1128/ecosalplus.7.2.3
Stress-Induced Mutagenesis.
Ashley B. Williams (2012)
Semantic Scholar Logo Some data provided by SemanticScholar