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AU-rich element-binding protein negatively regulates CCAAT enhancer-binding protein mRNA stability during long-term synaptic plasticity in Aplysia.

ABSTRACT: The consolidation of long-term memory for sensitization and synaptic facilitation in Aplysia requires synthesis of new mRNA including the immediate early gene Aplysia CCAAT enhancer-binding protein (ApC/EBP). After the rapid induction of ApC/EBP expression in response to repeated treatments of 5-hydroxytryptamine (5-HT), ApC/EBP mRNA is temporarily expressed in sensory neurons of sensory-to-motor synapses. However, the molecular mechanism underlying the rapid degradation of ApC/EBP transcript is not known. Here, we cloned an AU-rich element (ARE)-binding protein, ApAUF1, which functions as a destabilizing factor for ApC/EBP mRNA. ApAUF1 was found to bind to the 3' UTR of ApC/EBP mRNA that contains AREs and subsequently reduces the expression of ApC/EBP 3' UTR-containing reporter genes. Moreover, overexpression of ApAUF1 inhibited the induction of ApC/EBP mRNA in sensory neurons and also impaired long-term facilitation of sensory-to-motor synapses by repetitive 5-HT treatments. These results provide evidence for a critical role of the posttranscriptional modification of ApC/EBP mRNA during the consolidation of synaptic plasticity.

SUBMITTER: Lee YS

PROVIDER: S-EPMC3458389 | biostudies-literature | 2012 Sep

REPOSITORIES: biostudies-literature

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AU-rich element-binding protein negatively regulates CCAAT enhancer-binding protein mRNA stability during long-term synaptic plasticity in Aplysia.

Lee Yong-Seok YS Choi Sun-Lim SL Jun Heejung H Yim Se-Jeong SJ Lee Jin-A JA Kim Hyoung F HF Lee Seung-Hee SH Shim Jaehoon J Lee Kyungmin K Jang Deok-Jin DJ Kaang Bong-Kiun BK

Proceedings of the National Academy of Sciences of the United States of America 20120904 38

The consolidation of long-term memory for sensitization and synaptic facilitation in Aplysia requires synthesis of new mRNA including the immediate early gene Aplysia CCAAT enhancer-binding protein (ApC/EBP). After the rapid induction of ApC/EBP expression in response to repeated treatments of 5-hydroxytryptamine (5-HT), ApC/EBP mRNA is temporarily expressed in sensory neurons of sensory-to-motor synapses. However, the molecular mechanism underlying the rapid degradation of ApC/EBP transcript is ...[more]

PMID: 22949683

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Project description:The yeast M-NM-6-crystallin Zta1p interacts specifically with RNA sequences rich in adenine and uracil (AU-rich element). We have looked for possible targets of Zta1p through a comparative transcriptional analysis of the yeast defective in ZTA1 (M-NM-^Tzta1) versus the wild-type by microarray. This revealed that a group of genes implicated on amino acid biosynthesis are affected by the lack of ZTA1. The effect on one of the targets ARG4 was studied in more detail, revealing a clear positive correlation between ZTA1 and ARG4 expression at the mRNA level. We demonstrate that Zta1p is able to bind specifically to the 3M-bM-^@M-^YUTR AU-rich elements of ARG4 mRNA in vitro, suggesting that the mechanism by which ZTA1 modulates the expression of ARG4 is probably mediated by this mRNA binding ability. Moreover, the expression of ZTA1 is also under the control of the TOR pathway, and under Gcn4p, which regulates genes implicated in the response to nutrient availability and the general amino acid control (GAAC). In summary, our results shed light on the functional role of the M-NM-6-crystallin family as stress response proteins, with a conserved functional role, from yeast to humans, in the post-transcriptional regulation of genes that need to be rapidly activated for cell defense. Triplicate biological replicate experiments were performed, where the two strains, M-bM-^HM-^Fzta1 and wild-type, were grown in the presence or absence of hydrogen peroxide. The experimental design was defined to directly compare the M-bM-^HM-^Fzta1 versus the wild-type strain in either of the two hydrogen peroxide treatment conditions (i.e. treated M-bM-^HM-^Fzta1 versus treated wt, or untreated M-bM-^HM-^Fzta1 versus untreated wt). A duplicate hybridization on a separate array with dye swapping was performed in each case to correct for dye bias effects. Thus, a total of 12 array data sets were produced as a result of processing three experimental pairs of samples, for each of two treatment conditions, with dye swap duplicates.

Dataset Information

AU-rich element-binding protein negatively regulates CCAAT enhancer-binding protein mRNA stability during long-term synaptic plasticity in Aplysia.

Publications

AU-rich element-binding protein negatively regulates CCAAT enhancer-binding protein mRNA stability during long-term synaptic plasticity in Aplysia.

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