Reduced activity-dependent protein levels in a mouse model of the fragile X premutation

Neurobiology of Learning and Memory

Volumn 109, Issue , 2014, Pages 160-168

  von Leden, Ramona E ^a,d   Curley, Lindsey C ^a,b   Greenberg, Gian D ^b   Hunsaker, Michael R ^a,e,f   Willemsen, Rob ^b,c   Berman, Robert F ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d Uniformed Services of the Health Sciences   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF UTAH   (United States)

Author keywords

Arc; C Fos; CGG KI mouse; Endophenotype; Fmrp; Fragile X premutation; Western blot

Indexed keywords

ARC; C-FOS; CGG KI MOUSE; ENDOPHENOTYPE; FMRP; FRAGILE X PREMUTATION; WESTERN BLOT;

ANIMALS; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE KNOCK-IN TECHNIQUES; MALE; MICE; MOTOR ACTIVITY; MOTOR CORTEX; MUTATION;

EID: 84893555489     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.01.011     Document Type: Article

References (44)

1. Antar L.N., Dictenberg J.B., Plociniak M., Afroz R., Bassell G.J. Localization of fmrp-associated mRNA granules and requirement of microtubules for activity-dependent trafficking in hippocampal neurons. Genes, Brain, and Behavior 2005, 4(6):350-359.
2. Auerbach M.D., Bear M.F. Loss of the fragile X mental retardation protein decouples metabotropic glutamate receptor dependent priming of long-term potentiation from protein synthesis. Journal of Neurophysiology 2010, 104(2):1047-1051.
3. Benjamini Y., Drai D., Elmer G., Kafkafi N., Golani I. Controlling the false discovery rate in behavior genetics research. Behavioural Brain Research 2001, 125(1-2):279-284.
4. Borthwell R.M., Hunsaker M.R., Willemsen R., Berman R.F. Spatiotemporal processing deficits in female CGG KI mice modeling the fragile X premutation. Behavioural Brain Research 2012, 233(1):29-34.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
6. Bramham C.R., Alme M.N., Bittins M., Kuipers S.D., Nair R.R., Pai B., et al. The arc of synaptic memory. Experimental Brain Research 2010, 200:125-140.
7. Bramham C.R., Worley P.F., Moore M.J., Guzowski J.F. The immediate early gene arc/arg3.1: Regulation, mechanisms, and function. Journal of Neuroscience 2008, 28(46):11760-11767.
8. Chowdhury S., Shepherd J.D., Okuno H., Lyford G., Petralia R.S., Plath N., et al. Arc/arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 2006, 52(3):445-459.
9. Darnell J.C., Van Driesche S.J., Zhang C., Hung K.Y., Mele A., Fraser C.E., et al. FMRP stalls ribosomal translocation on mRNAs linked to syaptic function and autism. Cell 2011, 146(2):247-261.
10. Diep A.A., Hunsaker M.R., Kwock R., Kim K., Willemsen R., Berman R.F. Female CGG knock-in mice modeling the fragile X premutation are impaired on a skilled forelimb reaching task. Neurobiology of Learning and Memory 2012, 97(2):229-234.
11. Dragunow M., Faull R. The use of c-Fos as a metabolic marker in neuronal pathway tracing. Journal of Neuroscience Methods 1989, 29(3):261-265.
12. Farr T.D., Whishaw I.Q. Quantitative and qualitative impairments in skilled reaching in the mouse (mus musculus) after a focal motor cortex stroke. Stroke 2002, 33(7):1869-1875.
13. Gallistel C.R., Fairhurst S., Balsam P. The learning curve: Implications of a quantitative analysis. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(36):13124-13131.
14. Garcia-Arocena D., Hagerman P.J. Advances in understanding the molecular basis of FXTAS. Human Molecular Genetics 2010, 19(R1):R83-R89.
15. Greenough W.T., Larson J.R., Withers G.S. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behavioral and Neural Biology 1985, 44(2):301-314.
16. Hagerman P.J., Hagerman R.J. The fragile-X premutation: A maturing perspective. American Journal of Human Genetics 2004, 74(5):805-816.
17. Hagerman R.J., Leehey M., Heinrichs W., Tassone F., Wilson R., Hills J., et al. Intention tremor, parkinsonism, and generalized brain atrophy in male carriers of fragile X. Neurology 2001, 57(1):127-130.
18. Hanlon E.C., Faraguna U., Vyazovskly V.V., Tononi G., Cirelli C. Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. Sleep 2009, 32(6):719-729.
19. Hosp, J. A., Mann, S., Weganast-Braun, B. M., Calhoun, M. E., & Luft, A. R. (2013). Region and taskspecific activation of Arc in primary motor cortex of rats following motor skill learning. Neuroscience, in press. doi:10.1016/j.neuroscience.2013.06.060.
20. Huber K.M., Gallagher S.M., Warren S.T., Bear M.F. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(11):7746-7750.
21. Hunsaker M.R. Comprehensive neurocognitive endophenotyping strategies for mouse models of genetic disorders. Progress in Neurobiology 2012, 96(2):220-241.
22. Hunsaker M.R., Arque G., Berman R.F., Willemsen R., Hukema R.K. Mouse models of the fragile X premutation and the fragile X associated tremor/ataxia syndrome. Results and Problems in Cell Differentiation 2012, 54:255-269.
23. Hunsaker M.R., Goodrich-Hunsaker N.J., Willemsen R., Berman R.F. Temporal ordering deficits in female CGG KI mice heterozygous for the fragile X premutation. Behavioural Brain Research 2010, 213(2):263-268.
24. Hunsaker M.R., Greco C.M., Tassone F., Berman R.F., Willemsen R., Hagerman R.J., et al. Rare intranuclear inclusions in the brains of 3 older adult males with fragile X syndrome: Implications for the spectrum of fragile X-associated disorders. Journal of Neuropathology and Experimental Neurology 2011, 70(6):462-469.
25. Hunsaker M.R., Kim K.M., Willemsen R., Berman R.F. CGG Trinucleotide repeat length modulates neural plasticity and spatiotemporal processing in a mouse model of the fragile X premutation. Hippocampus 2012, 22(12):2260-2275.
26. Hunsaker M.R., von Leden R.E., Ta B.T., Goodrich-Hunsaker N.J., Arque G., Kim K., et al. Motor deficits on a ladder rung task in male and female adolescent and adult CGG knock-in mice. Behavioural Brain Research 2011, 222(1):117-121.
27. Hunsaker M.R., Wenzel H.J., Willemsen R., Berman R.F. Progressive spatial processing deficits in a mouse model of the fragile X premutation. Behavioral Neuroscience 2009, 123(6):1315-1324.
28. Iliff A.J., Renoux A.J., Krans A., Usdin K., Sutton M.A., Todd P.K. Impaired activity-dependent FMRP translation and enhanced mGluR-dependent LTD in Fragile X premutation mice. Human Molecualr Genetics 2013, 22(6):1180-1192.
29. Irwin S.A., Christmon C.A., Grossman A.W., Galvez R., Kim S.H., DeGrush B.J., et al. Fragile X mental retardation protein levels increase following complex environment exposure in rat brain regions undergoing active synaptogenesis. Neurobiology of Learning and Memory 2005, 83(3):180-187.
30. Irwin S.A., Swain R.A., Christmon C.A., Chakravarti A., Weiler I.J., Greenough W.T. Evidence for altered fragile-X mental retardation protein expression in response to behavioral stimulation. Neurobiology of Learning and Memory 2000, 74(1):87-93.
31. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14(2):433-445.
32. McIntyre C.K., Miyashita T., Setlow B., Marjon K.D., Steward O., Guzowski J.F., et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of arc protein in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(30):10718-10723.
33. Niere F., Wilkerson J.R., Huber K.M. Evidence for a fragile X mental retardation protein-mediated translational switch in metabotropic glutamate receptor-triggered arc translation and long-term depression. Journal of Neuroscience 2012, 32(17):5924-5936.
34. Park S., Park J.M., Kim S., Kim J.A., Shepherd J.D., Smith-Hicks C.L., et al. Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 2008, 59(1):70-83.
35. Pfeiffer B.E., Huber K.M. Current advances in local protein synthesis and synaptic plasticity. Journal of Neuroscience 2006, 26(27):7147-7150.
36. R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
37. Tassone F., Hagerman P.J. Expression of the FMR1 gene. Cytogenetic and Genome Research 2003, 100(1-4):124-128.
38. Tassone F., Hagerman R.J., Chamberlain W.D., Hagerman P.J. Transcription of the FMR1 gene in individuals with fragile X syndrome. American Journal of Medical Genetics 2000, 97(3):195-203.
39. Tassone F., Hagerman R.J., Taylor A.K., Gane L.W., Godfrey T.E., Hagerman P.J. Elevated levels of FMR1 mRNA in carrier males: A new mechanism of involvement in the fragile-X syndrome. American Journal of Human Genetics 2000, 66(1):6-15.
40. Vazdarjanova A., McNaughton B.L., Barnes C.A., Worley P.F., Guzowski J.F. Experience-dependent coincident expression of the effector immediate-early genes arc and homer 1a in hippocampal and neocortical neuronal networks. Journal of Neuroscience 2002, 22(23):10067-10071.
41. Weiler I.J., Irwin S.A., Klintsova A.Y., Spencer C.M., Brazelton A.D., Miyashiro K., et al. Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proceedings of the National Academy of Sciences of the United States of America 1997, 94(10):5395-5400.
42. Whishaw I.Q., Whishaw P., Gorny B. The structure of skilled forelimb reaching in the rat: A movement rating scale. Journal of Visualized Experiments 2008, 18.
43. Willemsen R., Hoogeveen-Westerveld M., Reis S., Holstege J., Severijnen L.A., Nieuwenhuizen I.M., et al. The FMR1 CGG repeat mouse displays ubiquitin-positive intranuclear neuronal inclusions; implications for the cerebellar tremor/ataxia syndrome. Human Molecular Genetics 2003, 12(9):949-959.
44. Xu T., Yu X., Perlik A.J., Tobin W.F., Zweig J.A., Tennant K., et al. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 2009, 462(7275):915-919.