Fragile X mental retardation protein (FMRP) controls diacylglycerol kinase activity in neurons

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

Volumn 113, Issue 26, 2016, Pages E3619-E3628

  Tabet, Ricardos ^a,b,c,d   Moutin, Enora ^e   Becker, Jérôme A J ^a,b,c,d,j   Heintz, Dimitri ^d   Fouillen, Laetitia ^f   Flatter, Eric ^a,b,c,d   Krȩzel, Wojciech ^a,b,c,d   Alunni, Violaine ^a,b,c,d   Koebel, Pascale ^a,b,c,d   Dembélé, Doulaye ^a,b,c,d   Tassone, Flora ^g   Bardoni, Barbara ^h   Mandel, Jean Louis ^a,b,c,d,i   Vitale, Nicolas ^d   Muller, Dominique ^e   Merrer, Julie Le ^a,b,c,d,j   Moine, Hervé ^a,b,c,d  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b CNRS   (France)

^c INSERM   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITY OF GENEVA   (Switzerland)

^f UNIVERSITÉ DE BORDEAUX   (France)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

ⁱ Centre de Recherche Interdisciplinaire en Biologie   (France)

^j UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

more..

Author keywords

CLIP; Diacylglycerol kinase; FMRP; Fragile X syndrome; Translation control

Indexed keywords

DIACYLGLYCEROL; DIACYLGLYCEROL KINASE; FRAGILE X MENTAL RETARDATION PROTEIN; MESSENGER RNA; METABOTROPIC RECEPTOR; PHOSPHATIDIC ACID; 1,2-DIACYLGLYCEROL; FMR1 PROTEIN, HUMAN; FMR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; BRAIN CELL; CROSS LINKING; DENDRITIC SPINE; EMBRYO; ENZYME ACTIVITY; FRAGILE X SYNDROME; GENE; IMMUNOPRECIPITATION; MOUSE; NERVE CELL; NERVE CELL LESION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; AGED; ANIMAL; C57BL MOUSE; ENZYMOLOGY; GENETICS; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; MIDDLE AGED; SIGNAL TRANSDUCTION;

AGED; ANIMALS; DENDRITIC SPINES; DIACYLGLYCEROL KINASE; DIGLYCERIDES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NEURONS; SIGNAL TRANSDUCTION;

EID: 84976600655     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1522631113     Document Type: Article

References (61)

1. Nelson DL, Orr HT, Warren ST (2013) The unstable repeats-Three evolving faces of neurological disease. Neuron 77(5):825-843.
2. Santoro MR, Bray SM, Warren ST (2012) Molecular mechanisms of fragile X syndrome: A twenty-year perspective. Annu Rev Pathol 7:219-245.
3. Michalon A, et al. (2012) Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice. Neuron 74(1):49-56.
4. Khandjian EW, Corbin F, Woerly S, Rousseau F (1996) The fragile X mental retardation protein is associated with ribosomes. Nat Genet 12(1):91-93.
5. Huber KM, Gallagher SM, Warren ST, Bear MF (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 99(11): 7746-7750.
6. Sidorov MS, Auerbach BD, Bear MF (2013) Fragile X mental retardation protein and synaptic plasticity. Mol Brain 6:15.
7. Darnell JC, Klann E (2013) The translation of translational control by FMRP: Therapeutic targets for FXS. Nat Neurosci 16(11):1530-1536.
8. Qin M, Kang J, Burlin TV, Jiang C, Smith CB (2005) Postadolescent changes in regional cerebral protein synthesis: An in vivo study in the FMR1 null mouse. J Neurosci 25(20): 5087-5095.
9. Brown V, et al. (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107(4):477-487.
10. Miyashiro KY, et al. (2003) RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron 37(3):417-431.
11. Darnell JC, et al. (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146(2):247-261.
12. Ascano M, Jr, et al. (2012) FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature 492(7429):382-386.
13. Suhl JA, Chopra P, Anderson BR, Bassell GJ, Warren ST (2014) Analysis of FMRP mRNA target datasets reveals highly associated mRNAs mediated by G-quadruplex structures formed via clustered WGGA sequences. Hum Mol Genet 23(20):5479-5491.
14. Chen E, Sharma MR, Shi X, Agrawal RK, Joseph S (2014) Fragile X mental retardation protein regulates translation by binding directly to the ribosome. Mol Cell 54(3): 407-417.
15. Ule J, et al. (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302(5648):1212-1215.
16. Schaeffer C, et al. (2001) The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J 20(17):4803-4813.
17. Brindley DN, Waggoner DW (1996) Phosphatidate phosphohydrolase and signal transduction. Chem Phys Lipids 80(1-2):45-57.
18. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-237.
19. de Chaffoy de Courcelles D, et al. (1989) The role of endogenously formed diacylglycerol in the propagation and termination of platelet activation. A biochemical and functional analysis using the novel diacylglycerol kinase inhibitor, R 59 949. J Biol Chem 264(6):3274-3285.
20. Koekkoek SK, et al. (2005) Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron 47(3):339-352.
21. Hu H, et al. (2008) Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. J Neurosci 28(31):7847-7862.
22. Lauterborn JC, et al. (2007) Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J Neurosci 27(40):10685-10694.
23. Gunaydin LA, et al. (2014) Natural neural projection dynamics underlying social behavior. Cell 157(7):1535-1551.
24. Rothwell PE, et al. (2014) Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors. Cell 158(1):198-212.
25. Dahlhaus R, El-Husseini A (2010) Altered neuroligin expression is involved in social deficits in a mouse model of the fragile X syndrome. Behav Brain Res 208(1):96-105.
26. Mineur YS, Huynh LX, Crusio WE (2006) Social behavior deficits in the Fmr1 mutant mouse. Behav Brain Res 168(1):172-175.
27. Pietropaolo S, Guilleminot A, Martin B, D?Amato FR, Crusio WE (2011) Geneticbackground modulation of core and variable autistic-like symptoms in Fmr1 knockout mice. PLoS One 6(2):e17073.
28. Spencer CM, et al. (2011) Modifying behavioral phenotypes in Fmr1KO mice: Genetic background differences reveal autistic-like responses. Autism Res 4(1):40-56.
29. Comery TA, et al. (1997) Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits. Proc Natl Acad Sci USA 94(10):5401-5404.
30. He CX, Portera-Cailliau C (2013) The trouble with spines in fragile X syndrome: Density, maturity and plasticity. Neuroscience 251:120-128.
31. Imai S, Kai M, Yasuda S, Kanoh H, Sakane F (2005) Identification and characterization of a novel human type II diacylglycerol kinase, DGK kappa. J Biol Chem 280(48): 39870-39881.
32. Vasudevan S, Steitz JA (2007) AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128(6):1105-1118.
33. Kim K, et al. (2009) Synaptic removal of diacylglycerol by DGKzeta and PSD-95 regulates dendritic spine maintenance. EMBO J 28(8):1170-1179.
34. Seo J, et al. (2012) Regulation of hippocampal long-term potentiation and long-term depression by diacylglycerol kinase ζ. Hippocampus 22(5):1018-1026.
35. Shirai Y, et al. (2010) Essential role of neuron-enriched diacylglycerol kinase (DGK), DGKbeta in neurite spine formation, contributing to cognitive function. PLoS One 5(7):e11602.
36. Yang J, et al. (2011) DGKi regulates presynaptic release during mGluR-dependent LTD. EMBO J 30(1):165-180.
37. Almena M, Mérida I (2011) Shaping up the membrane: Diacylglycerol coordinates spatial orientation of signaling. Trends Biochem Sci 36(11):593-603.
38. Hama H, Hara C, Yamaguchi K, Miyawaki A (2004) PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 41(3):405-415.
39. Anwyl R (2009) Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology 56(4):735-740.
40. de Diego-Otero Y, et al. (2009) Alpha-tocopherol protects against oxidative stress in the fragile X knockout mouse: An experimental therapeutic approach for the Fmr1 deficiency. Neuropsychopharmacology 34(4):1011-1026.
41. Wang X, et al. (1998) The phosphorylation of eukaryotic initiation factor eIF4E in response to phorbol esters, cell stresses, and cytokines is mediated by distinct MAP kinase pathways. J Biol Chem 273(16):9373-9377.
42. Rush AM, Wu J, Rowan MJ, Anwyl R (2002) Group I metabotropic glutamate receptor (mGluR)-dependent long-term depression mediated via p38 mitogen-activated protein kinase is inhibited by previous high-frequency stimulation and activation of mGluRs and protein kinase C in the rat dentate gyrus in vitro. J Neurosci 22(14): 6121-6128.
43. Sharma A, et al. (2010) Dysregulation of mTOR signaling in fragile X syndrome. J Neurosci 30(2):694-702.
44. Osterweil EK, Krueger DD, Reinhold K, Bear MF (2010) Hypersensitivity to mGluR5 and ERK1/2 leads to excessive protein synthesis in the hippocampus of a mouse model of fragile X syndrome. J Neurosci 30(46):15616-15627.
45. Kim K, Yang J, Kim E (2010) Diacylglycerol kinases in the regulation of dendritic spines. J Neurochem 112(3):577-587.
46. Ishisaka M, Hara H (2014) The roles of diacylglycerol kinases in the central nervous system: Review of genetic studies in mice. J Pharmacol Sci 124(3):336-343.
47. Sakai H, Sakane F (2012) Recent progress on type II diacylglycerol kinases: The physiological functions of diacylglycerol kinase δ, η and κ and their involvement in disease. J Biochem 152(5):397-406.
48. Mientjes EJ, et al. (2006) The generation of a conditional Fmr1 knock out mouse model to study Fmrp function in vivo. Neurobiol Dis 21(3):549-555.
49. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98(9):5116-5121.
50. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911-917.
51. Shui G, et al. (2010) Characterization of substrate preference for Slc1p and Cst26p in Saccharomyces cerevisiae using lipidomic approaches and an LPAAT activity assay. PLoS One 5(8):e11956.
52. De Roo M, Klauser P, Mendez P, Poglia L, Muller D (2008) Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb Cortex 18(1):151-161.
53. Boda B, Mendez P, Boury-Jamot B, Magara F, Muller D (2014) Reversal of activitymediated spine dynamics and learning impairment in a mouse model of Fragile X syndrome. Eur J Neurosci 39(7):1130-1137.
54. Subramanian M, et al. (2011) G-quadruplex RNA structure as a signal for neurite mRNA targeting. EMBO Rep 12(7):697-704.
55. Krezel W, et al. (1998) Impaired locomotion and dopamine signaling in retinoid receptor mutant mice. Science 279(5352):863-867.
56. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates (Academic, New York).
57. Becker JA, et al. (2014) Autistic-like syndrome in mu opioid receptor null mice is relieved by facilitated mGluR4 activity. Neuropsychopharmacology 39(9):2049-2060.
58. Silverman JL, Yang M, Lord C, Crawley JN (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11(7):490-502.
59. Deacon RM (2006) Assessing nest building in mice. Nat Protoc 1(3):1117-1119.
60. Sager TN, et al. (2010) Nest building performance following MPTP toxicity in mice. Behav Brain Res 208(2):444-449.
61. Le Merrer J, Rezai X, Scherrer G, Becker JA, Kieffer BL (2013) Impaired hippocampusdependent and facilitated striatum-dependent behaviors in mice lacking the δ opioid receptor. Neuropsychopharmacology 38(6):1050-1059. E3628