Local Protein Synthesis and Spine Morphogenesis: Fragile X Syndrome and Beyond

Overview

Journal J Neurosci

Specialty Neurology

Date 2006 Jul 11

PMID 16822971

Citations 93

Authors

Aaron W Grossman

Georgina M Aldridge

Ivan Jeanne Weiler

William T Greenough

Affiliations

Soon will be listed here.

Abstract

Behavioral experiences can modulate neural networks through changes in synaptic morphology and number. In contrast, abnormal morphogenesis of dendritic spines is associated with cognitive impairment, as in Fragile X syndrome. Dendritic or synaptic protein synthesis could provide the specificity and speed necessary for spine morphogenesis. Here, we highlight locally translated proteins shown to affect synaptic morphology (e.g., Fragile X mental retardation protein).

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References

Shiraishi Y, Mizutani A, Bito H, Fujisawa K, Narumiya S, Mikoshiba K . Cupidin, an isoform of Homer/Vesl, interacts with the actin cytoskeleton and activated rho family small GTPases and is expressed in developing mouse cerebellar granule cells. J Neurosci. 1999; 19(19):8389-400. PMC: 6783011. View

Sung Y, Conti J, Currie J, Brown W, Denman R . RNAs that interact with the fragile X syndrome RNA binding protein FMRP. Biochem Biophys Res Commun. 2000; 275(3):973-80. DOI: 10.1006/bbrc.2000.3405. View

El-Husseini A, Schnell E, Chetkovich D, Nicoll R, Bredt D . PSD-95 involvement in maturation of excitatory synapses. Science. 2000; 290(5495):1364-8. View

Laggerbauer B, Ostareck D, Keidel E, Ostareck-Lederer A, Fischer U . Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet. 2001; 10(4):329-38. DOI: 10.1093/hmg/10.4.329. View

Penzes P, Johnson R, Sattler R, Zhang X, Huganir R, Kambampati V . The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron. 2001; 29(1):229-42. DOI: 10.1016/s0896-6273(01)00193-3. View

Irwin S, Patel B, Idupulapati M, Harris J, Crisostomo R, Larsen B . Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am J Med Genet. 2001; 98(2):161-7. DOI: 10.1002/1096-8628(20010115)98:2<161::aid-ajmg1025>3.0.co;2-b. View

Li Z, Zhang Y, Ku L, Wilkinson K, Warren S, Feng Y . The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 2001; 29(11):2276-83. PMC: 55699. DOI: 10.1093/nar/29.11.2276. View

Aakalu G, Smith W, Nguyen N, Jiang C, Schuman E . Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron. 2001; 30(2):489-502. DOI: 10.1016/s0896-6273(01)00295-1. View

Sala C, Piech V, Wilson N, Passafaro M, Liu G, Sheng M . Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron. 2001; 31(1):115-30. DOI: 10.1016/s0896-6273(01)00339-7. View

10.

Brown V, Jin P, Ceman S, Darnell J, ODonnell W, Tenenbaum S . Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell. 2001; 107(4):477-87. DOI: 10.1016/s0092-8674(01)00568-2. View

11.

Vanderklish P, Edelman G . Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci U S A. 2002; 99(3):1639-44. PMC: 122243. DOI: 10.1073/pnas.032681099. View

12.

Boeckers T, Bockmann J, Kreutz M, Gundelfinger E . ProSAP/Shank proteins - a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem. 2002; 81(5):903-10. DOI: 10.1046/j.1471-4159.2002.00931.x. View

13.

Ostroff L, Fiala J, Allwardt B, Harris K . Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron. 2002; 35(3):535-45. DOI: 10.1016/s0896-6273(02)00785-7. View

14.

Sin W, Haas K, Ruthazer E, Cline H . Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature. 2002; 419(6906):475-80. DOI: 10.1038/nature00987. View

15.

Miller S, Yasuda M, Coats J, Jones Y, Martone M, Mayford M . Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron. 2002; 36(3):507-19. DOI: 10.1016/s0896-6273(02)00978-9. View

16.

Grossman A, Churchill J, Bates K, Kleim J, Greenough W . A brain adaptation view of plasticity: is synaptic plasticity an overly limited concept?. Prog Brain Res. 2002; 138:91-108. DOI: 10.1016/S0079-6123(02)38073-7. View

17.

Miyashiro K, Beckel-Mitchener A, Purk T, Becker K, Barret T, Liu L . RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice. Neuron. 2003; 37(3):417-31. DOI: 10.1016/s0896-6273(03)00034-5. View

18.

Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, Reis S . The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell. 2003; 112(3):317-27. DOI: 10.1016/s0092-8674(03)00079-5. View

19.

Tiruchinapalli D, Oleynikov Y, Kelic S, Shenoy S, Hartley A, Stanton P . Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci. 2003; 23(8):3251-61. PMC: 6742306. View

20.

Schenck A, Bardoni B, Langmann C, Harden N, Mandel J, Giangrande A . CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron. 2003; 38(6):887-98. DOI: 10.1016/s0896-6273(03)00354-4. View