publication . Article . 2019

Gadd45α modulates aversive learning through post‐transcriptional regulation of memory‐related mRNAs

Aparisi Rey, Alejandro; Karaulanov, Emil; Sharopov, Salim; Arab, Khelifa; Schäfer, Andrea; Gierl, Mathias; Guggenhuber, Stephan; Brandes, Caroline; Pennella, Luigi; Gruhn, Wolfram H; ...
Open Access English
  • Published: 01 Apr 2019 Journal: EMBO Reports, volume 20, issue 6 (issn: 1469-221X, eissn: 1469-3178, Copyright policy)
  • Publisher: John Wiley and Sons Inc.
Abstract
Abstract Learning is essential for survival and is controlled by complex molecular mechanisms including regulation of newly synthesized mRNAs that are required to modify synaptic functions. Despite the well‐known role of RNA‐binding proteins (RBPs) in mRNA functionality, their detailed regulation during memory consolidation is poorly understood. This study focuses on the brain function of the RBP Gadd45α (growth arrest and DNA damage‐inducible protein 45 alpha, encoded by the Gadd45a gene). Here, we find that hippocampal memory and long‐term potentiation are strongly impaired in Gadd45a‐deficient mice, a phenotype accompanied by reduced levels of memory‐related ...
Subjects
free text keywords: Article, Articles, Gadd45a, Grin2a, memory, RNA stability, Neuroscience, RNA Biology
77 references, page 1 of 6

1 Nainar S, Marshall PR, Tyler CR, Spitale RC, Bredy TW (2016) Evolving insights into RNA modifications and their functional diversity in the brain. Nat Neurosci 19: 1292–1298 27669990 [OpenAIRE] [PubMed]

2 Fukuchi M, Tsuda M (2010) Involvement of the 3′‐untranslated region of the brain‐derived neurotrophic factor gene in activity‐dependent mRNA stabilization. J Neurochem 115: 1222–1233 20874756 [PubMed]

3 Swanger SA, He YA, Richter JD, Bassell GJ (2013) Dendritic GluN2A synthesis mediates activity‐induced NMDA receptor insertion. J Neurosci 33: 8898–8908 23678131 [OpenAIRE] [PubMed]

4 Fornace AJ Jr, Nebert DW, Hollander MC, Luethy JD, Papathanasiou M, Fargnoli J, Holbrook NJ (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA‐damaging agents. Mol Cell Biol 9: 4196–4203 2573827 [OpenAIRE] [PubMed]

5 Takekawa M, Saito H (1998) A family of stress‐inducible GADD45‐like proteins mediate activation of the stress‐responsive MTK1/MEKK4 MAPKKK. Cell 95: 521–530 9827804 [OpenAIRE] [PubMed]

6 Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, Handa V, Döderlein G, Maltry N, Wu W, Lyko F et al (2007) Gadd45a promotes epigenetic gene activation by repair‐mediated DNA demethylation. Nature 445: 671–675 17268471 [OpenAIRE] [PubMed]

7 Jarome TJ, Butler AA, Nichols JN, Pacheco NL, Lubin FD (2015) NF‐kappaB mediates Gadd45beta expression and DNA demethylation in the hippocampus during fear memory formation. Front Mol Neurosci 8: 54 26441517 [OpenAIRE] [PubMed]

8 Gavin DP, Kusumo H, Sharma RP, Guizzetti M, Guidotti A, Pandey SC (2015) Gadd45b and N‐methyl‐D‐aspartate induced DNA demethylation in postmitotic neurons. Epigenomics 7: 567–579 26111030 [OpenAIRE] [PubMed]

9 Sytnikova YA, Kubarenko AV, Schäfer A, Weber AN, Niehrs C (2011) Gadd45a is an RNA binding protein and is localized in nuclear speckles. PLoS ONE 6: e14500 21249130 [OpenAIRE] [PubMed]

10 Matsunaga E, Nambu S, Oka M, Iriki A (2015) Comparative analysis of developmentally regulated expressions of Gadd45a, Gadd45b, and Gadd45g in the mouse and marmoset cerebral cortex. Neuroscience 284: 566–580 25450958 [PubMed]

11 Leach PT, Poplawski SG, Kenney JW, Hoffman B, Liebermann DA, Abel T, Gould TJ (2012) Gadd45b knockout mice exhibit selective deficits in hippocampus‐dependent long‐term memory. Learn Mem 19: 319–324 22802593 [OpenAIRE] [PubMed]

12 Sultan FA, Wang J, Tront J, Liebermann DA, Sweatt JD (2012) Genetic deletion of Gadd45b, a regulator of active DNA demethylation, enhances long‐term memory and synaptic plasticity. J Neurosci 32: 17059–17066 23197699 [OpenAIRE] [PubMed]

13 Hollander MC, Sheikh MS, Bulavin DV, Lundgren K, Augeri‐Henmueller L, Shehee R, Molinaro TA, Kim KE, Tolosa E, Ashwell JD et al (1999) Genomic instability in Gadd45a‐deficient mice. Nat Genet 23: 176–184 10508513 [PubMed]

14 Hoffman B, Liebermann DA (2013) Gadd45 in modulation of solid tumors and leukemia. Adv Exp Med Biol 793: 21–33 24104471 [OpenAIRE] [PubMed]

15 Liebermann DA, Tront JS, Sha X, Mukherjee K, Mohamed‐Hadley A, Hoffman B (2011) Gadd45 stress sensors in malignancy and leukemia. Crit Rev Oncog 16: 129–140 22150313 [OpenAIRE] [PubMed]

77 references, page 1 of 6
Abstract
Abstract Learning is essential for survival and is controlled by complex molecular mechanisms including regulation of newly synthesized mRNAs that are required to modify synaptic functions. Despite the well‐known role of RNA‐binding proteins (RBPs) in mRNA functionality, their detailed regulation during memory consolidation is poorly understood. This study focuses on the brain function of the RBP Gadd45α (growth arrest and DNA damage‐inducible protein 45 alpha, encoded by the Gadd45a gene). Here, we find that hippocampal memory and long‐term potentiation are strongly impaired in Gadd45a‐deficient mice, a phenotype accompanied by reduced levels of memory‐related ...
Subjects
free text keywords: Article, Articles, Gadd45a, Grin2a, memory, RNA stability, Neuroscience, RNA Biology
77 references, page 1 of 6

1 Nainar S, Marshall PR, Tyler CR, Spitale RC, Bredy TW (2016) Evolving insights into RNA modifications and their functional diversity in the brain. Nat Neurosci 19: 1292–1298 27669990 [OpenAIRE] [PubMed]

2 Fukuchi M, Tsuda M (2010) Involvement of the 3′‐untranslated region of the brain‐derived neurotrophic factor gene in activity‐dependent mRNA stabilization. J Neurochem 115: 1222–1233 20874756 [PubMed]

3 Swanger SA, He YA, Richter JD, Bassell GJ (2013) Dendritic GluN2A synthesis mediates activity‐induced NMDA receptor insertion. J Neurosci 33: 8898–8908 23678131 [OpenAIRE] [PubMed]

4 Fornace AJ Jr, Nebert DW, Hollander MC, Luethy JD, Papathanasiou M, Fargnoli J, Holbrook NJ (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA‐damaging agents. Mol Cell Biol 9: 4196–4203 2573827 [OpenAIRE] [PubMed]

5 Takekawa M, Saito H (1998) A family of stress‐inducible GADD45‐like proteins mediate activation of the stress‐responsive MTK1/MEKK4 MAPKKK. Cell 95: 521–530 9827804 [OpenAIRE] [PubMed]

6 Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, Handa V, Döderlein G, Maltry N, Wu W, Lyko F et al (2007) Gadd45a promotes epigenetic gene activation by repair‐mediated DNA demethylation. Nature 445: 671–675 17268471 [OpenAIRE] [PubMed]

7 Jarome TJ, Butler AA, Nichols JN, Pacheco NL, Lubin FD (2015) NF‐kappaB mediates Gadd45beta expression and DNA demethylation in the hippocampus during fear memory formation. Front Mol Neurosci 8: 54 26441517 [OpenAIRE] [PubMed]

8 Gavin DP, Kusumo H, Sharma RP, Guizzetti M, Guidotti A, Pandey SC (2015) Gadd45b and N‐methyl‐D‐aspartate induced DNA demethylation in postmitotic neurons. Epigenomics 7: 567–579 26111030 [OpenAIRE] [PubMed]

9 Sytnikova YA, Kubarenko AV, Schäfer A, Weber AN, Niehrs C (2011) Gadd45a is an RNA binding protein and is localized in nuclear speckles. PLoS ONE 6: e14500 21249130 [OpenAIRE] [PubMed]

10 Matsunaga E, Nambu S, Oka M, Iriki A (2015) Comparative analysis of developmentally regulated expressions of Gadd45a, Gadd45b, and Gadd45g in the mouse and marmoset cerebral cortex. Neuroscience 284: 566–580 25450958 [PubMed]

11 Leach PT, Poplawski SG, Kenney JW, Hoffman B, Liebermann DA, Abel T, Gould TJ (2012) Gadd45b knockout mice exhibit selective deficits in hippocampus‐dependent long‐term memory. Learn Mem 19: 319–324 22802593 [OpenAIRE] [PubMed]

12 Sultan FA, Wang J, Tront J, Liebermann DA, Sweatt JD (2012) Genetic deletion of Gadd45b, a regulator of active DNA demethylation, enhances long‐term memory and synaptic plasticity. J Neurosci 32: 17059–17066 23197699 [OpenAIRE] [PubMed]

13 Hollander MC, Sheikh MS, Bulavin DV, Lundgren K, Augeri‐Henmueller L, Shehee R, Molinaro TA, Kim KE, Tolosa E, Ashwell JD et al (1999) Genomic instability in Gadd45a‐deficient mice. Nat Genet 23: 176–184 10508513 [PubMed]

14 Hoffman B, Liebermann DA (2013) Gadd45 in modulation of solid tumors and leukemia. Adv Exp Med Biol 793: 21–33 24104471 [OpenAIRE] [PubMed]

15 Liebermann DA, Tront JS, Sha X, Mukherjee K, Mohamed‐Hadley A, Hoffman B (2011) Gadd45 stress sensors in malignancy and leukemia. Crit Rev Oncog 16: 129–140 22150313 [OpenAIRE] [PubMed]

77 references, page 1 of 6
Powered by OpenAIRE Research Graph
Any information missing or wrong?Report an Issue