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Host responses influence on the induction of lambda prophage.

Rokney A, Kobiler O, Amir A, Court DL, Stavans J, Adhya S, Oppenheim AB - Mol. Microbiol. (2008)

Bottom Line: We studied the effects of these two methods of induction on the lytic pathway by monitoring the activation of different lambda promoters, and found that the lambda genetic network co-ordinates information from the host stress response networks.Our results show that the function of the CII transcriptional activator, which facilitates the lysogenic developmental pathway, is not observed following either method of induction.We also show that, despite the common inhibitory effect on CII function, there are significant differences in the heat- and SOS-induced pathways leading to the lytic cascade.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics and Biotechnology, The Hebrew University-Hadassah Medical School, Jerusalem, Israel. assafr@ekmd.huji.ac.il

ABSTRACT
Inactivation of bacteriophage lambda CI repressor leads almost exclusively to lytic development. Prophage induction can be initiated either by DNA damage or by heat treatment of a temperature-sensitive repressor. These two treatments also cause a concurrent activation of either the host SOS or heat-shock stress responses respectively. We studied the effects of these two methods of induction on the lytic pathway by monitoring the activation of different lambda promoters, and found that the lambda genetic network co-ordinates information from the host stress response networks. Our results show that the function of the CII transcriptional activator, which facilitates the lysogenic developmental pathway, is not observed following either method of induction. Mutations in the cro gene restore the CII function irrespective of the induction method. Deletion of the heat-shock protease gene ftsH can also restore CII function following heat induction but not following SOS induction. Our findings highlight the importance of the elimination of CII function during induction as a way to ensure an efficient lytic outcome. We also show that, despite the common inhibitory effect on CII function, there are significant differences in the heat- and SOS-induced pathways leading to the lytic cascade.

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Lifestyles of phage λ.A. A cell infected with phage may follow the lytic or lysogenic response. The lysogenic state can be maintained indefinitely (prophage shown in red), occasionally cured and become non-lysogen or induced leading to lytic development.B. A schematic diagram showing the key regulatory elements in the lytic and lysogenic response. In both the lytic and lysogenic response, early transcription of N and Cro take place. In the lytic pathway, the delayed early transcripts lead to the accumulation of Q, which activates late gene expression (head and tail genes and lysis functions). CII activity is maintained below a detectable level (this work). In contrast, during the lysogenic response, CII activity dominates the network. High levels of CII, which are stabilized by CIII, lead to the activation of transcription from the pI, pE and paQ promoters. The inhibition of Q expression by the transcript initiated at the paQ promoter prevents late gene expression. Promoters are shown in green, phage functions in orange, antisense RNA in purple and lysogenic, and lytic pathways are shown in blue and red respectively (adapted from Oppenheim et al., 2005). The threshold effect on Q activity is shown as a black T.
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fig01: Lifestyles of phage λ.A. A cell infected with phage may follow the lytic or lysogenic response. The lysogenic state can be maintained indefinitely (prophage shown in red), occasionally cured and become non-lysogen or induced leading to lytic development.B. A schematic diagram showing the key regulatory elements in the lytic and lysogenic response. In both the lytic and lysogenic response, early transcription of N and Cro take place. In the lytic pathway, the delayed early transcripts lead to the accumulation of Q, which activates late gene expression (head and tail genes and lysis functions). CII activity is maintained below a detectable level (this work). In contrast, during the lysogenic response, CII activity dominates the network. High levels of CII, which are stabilized by CIII, lead to the activation of transcription from the pI, pE and paQ promoters. The inhibition of Q expression by the transcript initiated at the paQ promoter prevents late gene expression. Promoters are shown in green, phage functions in orange, antisense RNA in purple and lysogenic, and lytic pathways are shown in blue and red respectively (adapted from Oppenheim et al., 2005). The threshold effect on Q activity is shown as a black T.

Mentions: Temperate bacteriophage lambda exists in a symbiotic relationship with its host and can undergo either lytic or lysogenic development (Campbell, 2003; Livny and Friedman, 2004; Ptashne, 2004; Dodd et al., 2005) (Fig. 1A). The highly stable lysogenic state, in which the prophage replicates passively with the host genome, is maintained by the expression of the CI repressor that by binding at the oL and oR operators, blocks the cascade of phage lytic gene expression. In the repressed ‘off’ state, the CI repressor dominates the control of phage gene expression, while in the induced ‘on’ state, the CI repressor is inactivated. Treatment with DNA-damaging agents can lead to activation of the host SOS response, a DNA repair system induced by DNA damage. This results in the inactivation of the CI repressor and thus in an irreversible switch into lytic development (Campbell, 2003; Ptashne, 2004). In both the infection and induction processes, the λCro protein partially represses the pL and pR promoters, and its activity is required for efficient lytic growth (Svenningsen et al., 2005).


Host responses influence on the induction of lambda prophage.

Rokney A, Kobiler O, Amir A, Court DL, Stavans J, Adhya S, Oppenheim AB - Mol. Microbiol. (2008)

Lifestyles of phage λ.A. A cell infected with phage may follow the lytic or lysogenic response. The lysogenic state can be maintained indefinitely (prophage shown in red), occasionally cured and become non-lysogen or induced leading to lytic development.B. A schematic diagram showing the key regulatory elements in the lytic and lysogenic response. In both the lytic and lysogenic response, early transcription of N and Cro take place. In the lytic pathway, the delayed early transcripts lead to the accumulation of Q, which activates late gene expression (head and tail genes and lysis functions). CII activity is maintained below a detectable level (this work). In contrast, during the lysogenic response, CII activity dominates the network. High levels of CII, which are stabilized by CIII, lead to the activation of transcription from the pI, pE and paQ promoters. The inhibition of Q expression by the transcript initiated at the paQ promoter prevents late gene expression. Promoters are shown in green, phage functions in orange, antisense RNA in purple and lysogenic, and lytic pathways are shown in blue and red respectively (adapted from Oppenheim et al., 2005). The threshold effect on Q activity is shown as a black T.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2327240&req=5

fig01: Lifestyles of phage λ.A. A cell infected with phage may follow the lytic or lysogenic response. The lysogenic state can be maintained indefinitely (prophage shown in red), occasionally cured and become non-lysogen or induced leading to lytic development.B. A schematic diagram showing the key regulatory elements in the lytic and lysogenic response. In both the lytic and lysogenic response, early transcription of N and Cro take place. In the lytic pathway, the delayed early transcripts lead to the accumulation of Q, which activates late gene expression (head and tail genes and lysis functions). CII activity is maintained below a detectable level (this work). In contrast, during the lysogenic response, CII activity dominates the network. High levels of CII, which are stabilized by CIII, lead to the activation of transcription from the pI, pE and paQ promoters. The inhibition of Q expression by the transcript initiated at the paQ promoter prevents late gene expression. Promoters are shown in green, phage functions in orange, antisense RNA in purple and lysogenic, and lytic pathways are shown in blue and red respectively (adapted from Oppenheim et al., 2005). The threshold effect on Q activity is shown as a black T.
Mentions: Temperate bacteriophage lambda exists in a symbiotic relationship with its host and can undergo either lytic or lysogenic development (Campbell, 2003; Livny and Friedman, 2004; Ptashne, 2004; Dodd et al., 2005) (Fig. 1A). The highly stable lysogenic state, in which the prophage replicates passively with the host genome, is maintained by the expression of the CI repressor that by binding at the oL and oR operators, blocks the cascade of phage lytic gene expression. In the repressed ‘off’ state, the CI repressor dominates the control of phage gene expression, while in the induced ‘on’ state, the CI repressor is inactivated. Treatment with DNA-damaging agents can lead to activation of the host SOS response, a DNA repair system induced by DNA damage. This results in the inactivation of the CI repressor and thus in an irreversible switch into lytic development (Campbell, 2003; Ptashne, 2004). In both the infection and induction processes, the λCro protein partially represses the pL and pR promoters, and its activity is required for efficient lytic growth (Svenningsen et al., 2005).

Bottom Line: We studied the effects of these two methods of induction on the lytic pathway by monitoring the activation of different lambda promoters, and found that the lambda genetic network co-ordinates information from the host stress response networks.Our results show that the function of the CII transcriptional activator, which facilitates the lysogenic developmental pathway, is not observed following either method of induction.We also show that, despite the common inhibitory effect on CII function, there are significant differences in the heat- and SOS-induced pathways leading to the lytic cascade.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics and Biotechnology, The Hebrew University-Hadassah Medical School, Jerusalem, Israel. assafr@ekmd.huji.ac.il

ABSTRACT
Inactivation of bacteriophage lambda CI repressor leads almost exclusively to lytic development. Prophage induction can be initiated either by DNA damage or by heat treatment of a temperature-sensitive repressor. These two treatments also cause a concurrent activation of either the host SOS or heat-shock stress responses respectively. We studied the effects of these two methods of induction on the lytic pathway by monitoring the activation of different lambda promoters, and found that the lambda genetic network co-ordinates information from the host stress response networks. Our results show that the function of the CII transcriptional activator, which facilitates the lysogenic developmental pathway, is not observed following either method of induction. Mutations in the cro gene restore the CII function irrespective of the induction method. Deletion of the heat-shock protease gene ftsH can also restore CII function following heat induction but not following SOS induction. Our findings highlight the importance of the elimination of CII function during induction as a way to ensure an efficient lytic outcome. We also show that, despite the common inhibitory effect on CII function, there are significant differences in the heat- and SOS-induced pathways leading to the lytic cascade.

Show MeSH
Related in: MedlinePlus