Error-Prone DNA Polymerase IV Is Regulated by the Heat Shock Chaperone GroE in
            <i>Escherichia coli</i>

Layton, Jill; Foster, Patricia L.

doi:10.1128/jb.187.2.449-457.2005

Cited by 56 publications

(58 citation statements)

References 64 publications

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“…Previous results have demonstrated that complex cellular pathways regulate both the amount and activity of Pol IV (6,8,12,19,25,26,38,42). The results presented here clarify that RpoS regulates Pol IV directly by altering its amount and indirectly by altering its activity and that these regulatory modes are in effect at different times during the cell cycle.…”

Section: Discussionsupporting

confidence: 57%

RpoS, the Stress Response Sigma Factor, Plays a Dual Role in the Regulation of Escherichia coli 's Error-Prone DNA Polymerase IV

Storvik

Foster

2010

J Bacteriol

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RpoS, Escherichia coli's general stress response sigma factor, regulates error-prone DNA polymerase IV (Pol IV) (encoded by the dinB gene). Pol IV is induced in stationary-phase cells, and thereafter, levels of the protein remain elevated for several days of continuous incubation. This induction and persistence in stationary-phase cells are dependent on RpoS. Data presented here show that this regulation is direct via the RpoS-directed transcription of the dinB gene. However, a loss of RpoS also results in a decrease in Pol IV-dependent mutation when Pol IV is overexpressed from an RpoS-independent promoter in exponentially growing cells. The loss of RpoS also increases cell sensitivity to 4-nitroquinoline-1-oxide, indicating that RpoS affects the ability of Pol IV to bypass DNA lesions. Thus, in addition to directly driving the transcription of the dinB gene in stationaryphase cells, RpoS regulates the activity of Pol IV in exponentially growing cells via a second, indirect pathway.In their natural environments bacteria are constantly assaulted by a variety of stresses that include nutritional deprivation, temperature fluctuation, desiccation, and exposure to DNA-damaging agents such as UV light and reactive oxygen species. To survive such challenges, bacteria have evolved coordinated cellular defense mechanisms, two of which are the RpoS-regulated response to nutritional deprivation and the SOS response to DNA damage.Sigma factors are the subunits of RNA polymerase that recognize the promoter regions of genes and direct the holoenzyme to them. Escherichia coli has seven sigma factors, each of which is responsible for gene regulation under specific conditions. The vegetative sigma factor RpoD (also called D and 70 ) directs the RNA polymerase holoenzyme (E D ) to transcribe housekeeping genes and the genes specifically expressed during the exponential phase. A second major sigma factor, RpoS (also called S and 38 ), regulates the cell's response to nutritional deprivation. RpoS is activated as cells enter stationary phase and is responsible, either directly or indirectly, for the regulation of as many as 500 genes (33,40,41). Because of their similar recognition sequences, RpoS and RpoD often direct the RNA polymerase holoenzyme to bind to the same promoters (17). However, promoter binding by the RpoS-containing RNA polymerase holoenzyme (E S ) is enhanced in stationary phase by the accumulation of accessory factors, such as ppGpp, and/or by changes in DNA topology (7,17,23,24).DNA damage in E. coli and its relatives results in the upregulation of more than 40 genes (11) that include the genes encoding DNA polymerase II (Pol II), Pol IV, and Pol V (8,19). Pol IV, encoded by dinB, and Pol V, encoded by umuDC, are members of the Y family of specialized DNA polymerases (for a review, see reference 30). These polymerases are found in organisms from all three domains of life and can replicate damaged DNA, a process called translesion synthesis. Because of its ability to bypass many types of DNA lesions, Pol V has a ...

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Section: Discussionsupporting

confidence: 57%

RpoS, the Stress Response Sigma Factor, Plays a Dual Role in the Regulation of Escherichia coli 's Error-Prone DNA Polymerase IV

Storvik

Foster

2010

J Bacteriol

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“…In addition, the transcription of the dinB gene is controlled by RpoS, a s-subunit of RNA polymerase, which regulates a general stress response (Layton and Foster 2003). PolIV is also regulated by the heat-shock chaperone GroE (Layton and Foster 2005). Therefore, PolIV is a component of several cellular stress responses.…”

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Involvement ofEscherichia coliDNA Polymerase IV in Tolerance of Cytotoxic Alkylating DNA Lesionsin Vivo

Dasgupta²,

et al. 2007

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Escherichia coli PolIV, a DNA polymerase capable of catalyzing synthesis past replication-blocking DNA lesions, belongs to the most ubiquitous branch of Y-family DNA polymerases. The goal of this study is to identify spontaneous DNA damage that is bypassed specifically and accurately by PolIV in vivo. We increased the amount of spontaneous DNA lesions using mutants deficient for different DNA repair pathways and measured mutation frequency in PolIV-proficient and -deficient backgrounds. We found that PolIV performs an error-free bypass of DNA damage that accumulates in the alkA tag genetic background. This result indicates that PolIV is involved in the error-free bypass of cytotoxic alkylating DNA lesions. When the amount of cytotoxic alkylating DNA lesions is increased by the treatment with chemical alkylating agents, PolIV is required for survival in an alkA tag-proficient genetic background as well. Our study, together with the reported involvement of the mammalian PolIV homolog, Polk, in similar activity, indicates that Y-family DNA polymerases from the DinB branch can be added to the list of evolutionarily conserved molecular mechanisms that counteract cytotoxic effects of DNA alkylation. This activity is of major biological relevance because alkylating agents are continuously produced endogenously in all living cells and are also present in the environment.

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“…Because of this strong phenotype, adaptive mutation in FC40 is often used as an assay for Pol IV's mutagenic activity (e.g., see reference 23). Several factors existent in stationary-phase cells contribute to this high rate of Pol IV-dependent adaptive mutation: (i) transcription of the dinB gene is induced approximately 3-fold under the control of the stationary-phase sigma factor RpoS (42,63), (ii) the Pol IV protein is stabilized by the chaperone GroEL (43), (iii) Pol IV activity is enhanced by cellular polyphosphate (65), and (iv) proposed inhibitors of Pol IV activity, such as UmuD, may be less active or abundant in stationary-phase cells (23). This growth phase regulation suggests that Pol IV's mutagenic activity may serve an important function during nutrient-limited conditions.…”

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The SMC-Like Protein Complex SbcCD Enhances DNA Polymerase IV-Dependent Spontaneous Mutation inEscherichia coli

Storvik

Foster

2011

J Bacteriol

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In Escherichia coli, RpoS, the general stress response sigma factor, regulates the activity of the specialized DNA polymerase DNA polymerase IV (Pol IV) both in stationary-phase and in exponential-phase cells. In Escherichia coli and its relatives, DNA damage results in the induction of about 40 genes as part of the SOS response. Three of these genes encode specialized DNA polymerases: DNA polymerase II (Pol II; encoded by the polB gene), DNA Pol IV (encoded by the dinB gene), and DNA Pol V (encoded by the umuDC genes) (11,35). Pol IV and Pol V are members of the Y family of DNA polymerases that are widely distributed in all domains of life. Y family polymerases can replicate damaged DNA, a process called translesion synthesis, but they replicate undamaged DNA with fidelities that are typically orders of magnitude lower than those achieved by replicative DNA polymerases (20,48

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Error-Prone DNA Polymerase IV Is Regulated by the Heat Shock Chaperone GroE in Escherichia coli

Cited by 56 publications

References 64 publications

RpoS, the Stress Response Sigma Factor, Plays a Dual Role in the Regulation of Escherichia coli 's Error-Prone DNA Polymerase IV

RpoS, the Stress Response Sigma Factor, Plays a Dual Role in the Regulation of Escherichia coli 's Error-Prone DNA Polymerase IV

Involvement ofEscherichia coliDNA Polymerase IV in Tolerance of Cytotoxic Alkylating DNA Lesionsin Vivo

The SMC-Like Protein Complex SbcCD Enhances DNA Polymerase IV-Dependent Spontaneous Mutation inEscherichia coli

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