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SREBP controls oxygen-dependent mobilization of retrotransposons in fission yeast.

Sehgal A, Lee CY, Espenshade PJ - PLoS Genet. (2007)

Bottom Line: Transposons do not encode transcription factors and thus rely on host factors for mRNA expression and survival.Sre1 binds to DNA sequences in the Tf2 long terminal repeat that functions as an oxygen-dependent promoter.We find that Tf2 solo long terminal repeats throughout the genome direct oxygen-dependent expression of adjacent coding and noncoding sequences, providing a potential mechanism for the generation of oxygen-dependent gene expression.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, Maryland, Unites States of America.

ABSTRACT
Retrotransposons are mobile genetic elements that proliferate through an RNA intermediate. Transposons do not encode transcription factors and thus rely on host factors for mRNA expression and survival. Despite information regarding conditions under which elements are upregulated, much remains to be learned about the regulatory mechanisms or factors controlling retrotransposon expression. Here, we report that low oxygen activates the fission yeast Tf2 family of retrotransposons. Sre1, the yeast ortholog of the mammalian membrane-bound transcription factor sterol regulatory element binding protein (SREBP), directly induces the expression and mobilization of Tf2 retrotransposons under low oxygen. Sre1 binds to DNA sequences in the Tf2 long terminal repeat that functions as an oxygen-dependent promoter. We find that Tf2 solo long terminal repeats throughout the genome direct oxygen-dependent expression of adjacent coding and noncoding sequences, providing a potential mechanism for the generation of oxygen-dependent gene expression.

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Sre1 Controls Low Oxygen Expression of Multiple Tf2 Elements(A) Scheme for tagging individual Tf2 elements with ura4+. Bold arrow denotes Tf2 transcription initiation. Northern probe positions are indicated.(B) Yeast containing a single Tf2 element tagged by ura4+ or wild-type yeast were grown +/− oxygen for 8 h and processed for northern analysis using strand-specific DNA probes to detect either the tagged Tf2 element (ura4+ probe) or all 13 Tf2 elements (Tf2 probe).(C) Wild-type or sre1Δ yeast containing a tagged Tf2 element were grown +/− oxygen for 6 h and processed for northern analysis. All Tf2 elements tested (Tf2–4, Tf2–7, and Tf2–10) gave results identical to Tf2–3.
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pgen-0030131-g002: Sre1 Controls Low Oxygen Expression of Multiple Tf2 Elements(A) Scheme for tagging individual Tf2 elements with ura4+. Bold arrow denotes Tf2 transcription initiation. Northern probe positions are indicated.(B) Yeast containing a single Tf2 element tagged by ura4+ or wild-type yeast were grown +/− oxygen for 8 h and processed for northern analysis using strand-specific DNA probes to detect either the tagged Tf2 element (ura4+ probe) or all 13 Tf2 elements (Tf2 probe).(C) Wild-type or sre1Δ yeast containing a tagged Tf2 element were grown +/− oxygen for 6 h and processed for northern analysis. All Tf2 elements tested (Tf2–4, Tf2–7, and Tf2–10) gave results identical to Tf2–3.

Mentions: Fission yeast contains 13 full-length Tf2 transposons whose coding sequences are 99% identical at the DNA level and thus cannot be distinguished by hybridization [30]. To analyze the expression of individual transposons, we designed a strategy to tag each transposon with ura4+ (Figure 2A). We generated 13 different strains (Tf2–1 to Tf2–13), each carrying a single, tagged Tf2 element. These 13 strains and an untagged wild-type strain were grown in the presence or absence of oxygen for 8 h and processed for northern analysis using a strand-specific ura4+ probe. Expression of 12 out of 13 transposons increased under low oxygen (Figure 2B, upper panel). Notably, Tf2–11 was not induced despite low oxygen expression of other Tf2 elements in this strain (Figure 2B, lanes 21–22). Hereafter, we refer to the 12 coregulated elements collectively as Tf2. To test if low oxygen induction required Sre1, we deleted sre1+ from five Tf2-ura4+ tagged strains (Tf2–3, 4, 7, 10, and 11). Low oxygen induction of Tf2 transposons required Sre1 (Figure 2C), while deletion of sre1+ had no effect on Tf2–11 expression. These data demonstrate that with the exception of Tf2–11, Sre1 controls low oxygen expression of Tf2 transposons.


SREBP controls oxygen-dependent mobilization of retrotransposons in fission yeast.

Sehgal A, Lee CY, Espenshade PJ - PLoS Genet. (2007)

Sre1 Controls Low Oxygen Expression of Multiple Tf2 Elements(A) Scheme for tagging individual Tf2 elements with ura4+. Bold arrow denotes Tf2 transcription initiation. Northern probe positions are indicated.(B) Yeast containing a single Tf2 element tagged by ura4+ or wild-type yeast were grown +/− oxygen for 8 h and processed for northern analysis using strand-specific DNA probes to detect either the tagged Tf2 element (ura4+ probe) or all 13 Tf2 elements (Tf2 probe).(C) Wild-type or sre1Δ yeast containing a tagged Tf2 element were grown +/− oxygen for 6 h and processed for northern analysis. All Tf2 elements tested (Tf2–4, Tf2–7, and Tf2–10) gave results identical to Tf2–3.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC1941750&req=5

pgen-0030131-g002: Sre1 Controls Low Oxygen Expression of Multiple Tf2 Elements(A) Scheme for tagging individual Tf2 elements with ura4+. Bold arrow denotes Tf2 transcription initiation. Northern probe positions are indicated.(B) Yeast containing a single Tf2 element tagged by ura4+ or wild-type yeast were grown +/− oxygen for 8 h and processed for northern analysis using strand-specific DNA probes to detect either the tagged Tf2 element (ura4+ probe) or all 13 Tf2 elements (Tf2 probe).(C) Wild-type or sre1Δ yeast containing a tagged Tf2 element were grown +/− oxygen for 6 h and processed for northern analysis. All Tf2 elements tested (Tf2–4, Tf2–7, and Tf2–10) gave results identical to Tf2–3.
Mentions: Fission yeast contains 13 full-length Tf2 transposons whose coding sequences are 99% identical at the DNA level and thus cannot be distinguished by hybridization [30]. To analyze the expression of individual transposons, we designed a strategy to tag each transposon with ura4+ (Figure 2A). We generated 13 different strains (Tf2–1 to Tf2–13), each carrying a single, tagged Tf2 element. These 13 strains and an untagged wild-type strain were grown in the presence or absence of oxygen for 8 h and processed for northern analysis using a strand-specific ura4+ probe. Expression of 12 out of 13 transposons increased under low oxygen (Figure 2B, upper panel). Notably, Tf2–11 was not induced despite low oxygen expression of other Tf2 elements in this strain (Figure 2B, lanes 21–22). Hereafter, we refer to the 12 coregulated elements collectively as Tf2. To test if low oxygen induction required Sre1, we deleted sre1+ from five Tf2-ura4+ tagged strains (Tf2–3, 4, 7, 10, and 11). Low oxygen induction of Tf2 transposons required Sre1 (Figure 2C), while deletion of sre1+ had no effect on Tf2–11 expression. These data demonstrate that with the exception of Tf2–11, Sre1 controls low oxygen expression of Tf2 transposons.

Bottom Line: Transposons do not encode transcription factors and thus rely on host factors for mRNA expression and survival.Sre1 binds to DNA sequences in the Tf2 long terminal repeat that functions as an oxygen-dependent promoter.We find that Tf2 solo long terminal repeats throughout the genome direct oxygen-dependent expression of adjacent coding and noncoding sequences, providing a potential mechanism for the generation of oxygen-dependent gene expression.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, Maryland, Unites States of America.

ABSTRACT
Retrotransposons are mobile genetic elements that proliferate through an RNA intermediate. Transposons do not encode transcription factors and thus rely on host factors for mRNA expression and survival. Despite information regarding conditions under which elements are upregulated, much remains to be learned about the regulatory mechanisms or factors controlling retrotransposon expression. Here, we report that low oxygen activates the fission yeast Tf2 family of retrotransposons. Sre1, the yeast ortholog of the mammalian membrane-bound transcription factor sterol regulatory element binding protein (SREBP), directly induces the expression and mobilization of Tf2 retrotransposons under low oxygen. Sre1 binds to DNA sequences in the Tf2 long terminal repeat that functions as an oxygen-dependent promoter. We find that Tf2 solo long terminal repeats throughout the genome direct oxygen-dependent expression of adjacent coding and noncoding sequences, providing a potential mechanism for the generation of oxygen-dependent gene expression.

Show MeSH
Related in: MedlinePlus