Ribonucleoprotein complexes in neurologic diseases

Current Opinion in Neurobiology

Volumn 18, Issue 5, 2008, Pages 516-523

  Ule, Jernej ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; DNA BINDING PROTEIN; FRAGILE X MENTAL RETARDATION PROTEIN; MESSENGER RNA; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SURVIVAL MOTOR NEURON PROTEIN; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

BRAIN REGION; CENTRAL NERVOUS SYSTEM; CODING; DNA BINDING MOTIF; DNA SPLICING; HUMAN; NERVE FIBER TRANSPORT; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW;

ALTERNATIVE SPLICING; ANIMALS; DNA-BINDING PROTEINS; FRAGILE X MENTAL RETARDATION PROTEIN; HUMANS; NERVOUS SYSTEM DISEASES; RIBONUCLEOPROTEINS; RNA TRANSPORT; SMN COMPLEX PROTEINS;

EID: 56249119910     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2008.09.018     Document Type: Review

References (69)

1. Handwerger K.E., and Gall J.G. Subnuclear organelles: new insights into form and function. Trends Cell Biol 16 1 (2006) 19-26
2. Kiebler M.A., and Bassell G.J. Neuronal RNA granules: movers and makers. Neuron 51 6 (2006) 685-690
3. Neumann M., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314 5796 (2006) 130-133. ALS and FTLD patients often share some common symptoms, which suggested that the two disorders may share a mechanistic link. This study found the molecular link between the two disorders by the observation that the cytoplasmic ubiquitinated inclusions in both disorders contain TDP-43 RNA-binding protein, which is associated with its loss from the nucleus.
4. Sreedharan J., et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319 5870 (2008) 1668-1672. This study identified several ALS patients with mutations in TDP-43. The mutant proteins showed increased tendency to cleavage and were toxic to the embryonic chick spinal cord neurons causing marked apoptosis and developmental delay.
5. Lefebvre S., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80 1 (1995) 155-165
6. Garber K., et al. Transcription, translation and fragile X syndrome. Curr Opin Genet Dev 16 3 (2006) 270-275
7. Forman M.S., Trojanowski J.Q., and Lee V.M. Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat Med 10 10 (2004) 1055-1063
8. Higashi S., et al. Concurrence of TDP-43, tau and alpha-synuclein pathology in brains of Alzheimer's disease and dementia with Lewy bodies. Brain Res 1184 (2007) 284-294
9. Amador-Ortiz C., et al. TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer's disease. Ann Neurol 61 5 (2007) 435-445
10. Buratti E., and Baralle F.E. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front Biosci 13 (2008) 867-878
11. Ayala Y.M., Misteli T., and Baralle F.E. TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc Natl Acad Sci U S A 105 10 (2008) 3785-3789. The authors analyzed mRNA levels in the TDP-43 knockdown cells to find an increase in the levels of Cdk6 mRNA and protein, accompanied by an increase in phosphorylation of two of its major protein targets.
12. Strong M.J., et al. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol Cell Neurosci 35 2 (2007) 320-327
13. Kabashi E., et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 40 5 (2008) 572-574
14. Setola V., et al. Axonal-SMN (a-SMN), a protein isoform of the survival motor neuron gene, is specifically involved in axonogenesis. Proc Natl Acad Sci U S A 104 6 (2007) 1959-1964
15. Briese M., Esmaeili B., and Sattelle D.B. Is spinal muscular atrophy the result of defects in motor neuron processes?. Bioessays 27 9 (2005) 946-957
16. Gavrilina T.O., et al. Neuronal SMN expression corrects spinal muscular atrophy in severe SMA mice while muscle-specific SMN expression has no phenotypic effect. Hum Mol Genet 17 8 (2008) 1063-1075. This is the first study showing in an animal model of SMA that neuronal expression of SMN can rescue the phenotype, suggesting that the decreased amount of SMN in the non-neuronal tissues does not play a major role in SMA.
17. Pellizzoni L. Chaperoning ribonucleoprotein biogenesis in health and disease. EMBO Rep 8 4 (2007) 340-345
18. Pellizzoni L., Charroux B., and Dreyfuss G. SMN mutants of spinal muscular atrophy patients are defective in binding to snRNP proteins. Proc Natl Acad Sci U S A 96 20 (1999) 11167-11172
19. Wan L., et al. The survival of motor neurons protein determines the capacity for snRNP assembly: biochemical deficiency in spinal muscular atrophy. Mol Cell Biol 25 13 (2005) 5543-5551
20. Shpargel K.B., and Matera A.G. Gemin proteins are required for efficient assembly of Sm-class ribonucleoproteins. Proc Natl Acad Sci U S A 102 48 (2005) 17372-17377
21. Buhler D., et al. Essential role for the tudor domain of SMN in spliceosomal U snRNP assembly: implications for spinal muscular atrophy. Hum Mol Genet 8 13 (1999) 2351-2357
22. Gabanella F., et al. Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS ONE 2 9 (2007) e921. This is the first study to report defective snRNP assembly in the spinal cord of an SMA mouse model.
23. Winkler C., et al. Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy. Genes Dev 19 19 (2005) 2320-2330
24. Zhang Z., et al. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 133 4 (2008) 585-600
25. Butchbach M.E., Edwards J.D., and Burghes A.H. Abnormal motor phenotype in the SMNDelta7 mouse model of spinal muscular atrophy. Neurobiol Dis 27 2 (2007) 207-219
26. Ronesi J.A., and Huber K.M. Metabotropic glutamate receptors and fragile X mental retardation protein: partners in translational regulation at the synapse. Sci Signal 1 5 (2008) pe6
27. Piper M., and Holt C. RNA translation in axons. Annu Rev Cell Dev Biol 20 (2004) 505-523
28. Rossoll W., et al. Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 163 4 (2003) 801-812
29. Rossoll W., et al. Specific interaction of Smn, the spinal muscular atrophy determining gene product, with hnRNP-R and gry-rbp/hnRNP-Q: a role for Smn in RNA processing in motor axons?. Hum Mol Genet 11 1 (2002) 93-105
30. Tadesse H., et al. KH-type splicing regulatory protein interacts with survival motor neuron protein and is misregulated in spinal muscular atrophy. Hum Mol Genet 17 4 (2008) 506-524
31. Oprea G.E., et al. Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science 320 5875 (2008) 524-527. A search for SMA modifier genes has found that overexpression of plastin 3, a protein that bundles actin filaments, can rescue the aberrant axonal outgrowth in severe SMA mouse motor neurons.
32. Huber K.M., Kayser M.S., and Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288 5469 (2000) 1254-1257
33. Nosyreva E.D., and Huber K.M. Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. J Neurophysiol 95 5 (2006) 3291-3295
34. Hou L., et al. Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 51 4 (2006) 441-454
35. Darnell J.C., et al. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107 4 (2001) 489-499
36. Brown V., et al. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107 4 (2001) 477-487
37. Todd P.K., Mack K.J., and Malter J.S. The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc Natl Acad Sci U S A 100 24 (2003) 14374-14378
38. Napoli I., et al. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134 6 (2008) 1042-1054. This study reports that FMRP-binding protein CYFIP1 inhibits translation by binding eIF4E. Formation of FMRP/CYFIP1/eIF4E complex is shown to be increased by cap-Arc mRNA and BC1 RNA and decreased by transient mGluR activation.
39. Park S., et al. Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59 1 (2008) 70-83. The authors report that eEF2 and arc are both required for mGluR-LTD, which is also impaired in Fmr1/Arc double KO mice. Interestingly, Fmr1 KO mice lack the mGluR-dependent synthesis of Arc mRNA, suggesting that misregulated Arc protein translation may contribute to the abnormal mGluR-LTD in Fmr1 KO mice.
40. Waung M.W., et al. Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59 1 (2008) 84-97
41. Antar L.N., et al. Metabotropic glutamate receptor activation regulates fragile-X mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J Neurosci 24 11 (2004) 2648-2655
42. Dictenberg J.B., et al. A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev Cell 14 6 (2008) 926-939. Analysis of mRNA transport in FMRP knockout neurons found that several FMRP-target mRNAs do not localize to neurons in response to mGluR-LTD, whereas in wild-type neurons both FMRP and its target mRNAs do, showing for the first time that in addition to regulating RNA translation, FMRP might also play a role in activity-dependent transport of specific mRNAs.
43. Narayanan U., et al. FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J Neurosci 27 52 (2007) 14349-14357
44. Weiler I.J., et al. Fragile X mental retardation protein is necessary for neurotransmitter-activated protein translation at synapses. Proc Natl Acad Sci U S A 101 50 (2004) 17504-17509
45. Huttelmaier S., et al. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438 7067 (2005) 512-515
46. Wang G.S., and Cooper T.A. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 8 10 (2007) 749-761
47. Cartegni L., and Krainer A.R. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat Genet 30 4 (2002) 377-384
48. Hofmann Y., and Wirth B. hnRNP-G promotes exon 7 inclusion of survival motor neuron (SMN) via direct interaction with Htra2-beta1. Hum Mol Genet 11 17 (2002) 2037-2049
49. Kashima T., and Manley J.L. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat Genet 34 4 (2003) 460-463
50. Kashima T., et al. hnRNP A1 functions with specificity in repression of SMN2 exon 7 splicing. Hum Mol Genet 16 24 (2007) 3149-3159
51. Cartegni L., et al. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am J Hum Genet 78 1 (2006) 63-77
52. Licatalosi DD, Darnell RB: Splicing regulation in neurologic disease. Neuron, in press.
53. Orr H.T., and Zoghbi H.Y. Trinucleotide repeat disorders. Annu Rev Neurosci 30 (2007) 575-621
54. Ule J., et al. CLIP identifies Nova-regulated RNA networks in the brain. Science 302 5648 (2003) 1212-1215
55. Ule J., et al. Nova regulates brain-specific splicing to shape the synapse. Nat Genet 37 8 (2005) 844-852
56. Ule J., et al. An RNA map predicting Nova-dependent splicing regulation. Nature 444 7119 (2006) 580-586. This study shows that a set of positional rules can distinguish the splicing silencing and enhancing action of Nova against a large set of its target mRNAs and can be used to predict the activity of Nova. In addition, analysis of partially spliced pre-mRNAs in Nova2 knockout brain shows that splicing of sequential introns proceeds in a preferential order, allowing Nova to act by regulating splicing of only one of the two introns flanking an alternative exon.
57. Mackenzie I.R., et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 61 5 (2007) 427-434
58. Rizzardini M., et al. Low levels of ALS-linked Cu/Zn superoxide dismutase increase the production of reactive oxygen species and cause mitochondrial damage and death in motor neuron-like cells. J Neurol Sci 232 1-2 (2005) 95-103
59. Wan L., et al. Inactivation of the SMN complex by oxidative stress. Mol Cell 31 2 (2008) 244-254. The authors developed a high-throughput screen for snRNP assembly modifiers and discovered that ROS inhibit SMN-complex activity in a dose-dependent manner. This suggests that the SMN complex may a role in oxidative stress pathophysiology, which is associated with many degenerative diseases.
60. van der Brug M.P., et al. RNA binding activity of the recessive parkinsonism protein DJ-1 supports involvement in multiple cellular pathways. Proc Natl Acad Sci U S A 105 29 (2008) 10244-10249
61. Faghihi M.A., et al. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat Med 14 7 (2008) 723-730
62. Sofola O.A., et al. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 55 4 (2007) 565-571. This study reports that hnRNP A2 directly binds to the CGG RNA repeat and thereby also recruits CUGBP1, and either protein can suppress the phenotype of the FXTAS Drosophila model.
63. Iwahashi C.K., et al. Protein composition of the intranuclear inclusions of FXTAS. Brain 129 Pt 1 (2006) 256-271
64. Bermejo-Pareja F., et al. Incidence and subtypes of dementia in three elderly populations of central Spain. J Neurol Sci 264 1-2 (2008) 63-72
65. Hyman B.T., et al. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225 4667 (1984) 1168-1170
66. Josephs K.A., et al. Abnormal TDP-43 immunoreactivity in AD modifies clinicopathologic and radiologic phenotype. Neurology 70 19 Pt 2 (2008) 1850-1857
67. Pasinelli P., and Brown R.H. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7 9 (2006) 710-723
68. Kumar-Singh S., and Van Broeckhoven C. Frontotemporal lobar degeneration: current concepts in the light of recent advances. Brain Pathol 17 1 (2007) 104-114
69. Parsons D.W., et al. Intragenic telSMN mutations: frequency, distribution, evidence of a founder effect, and modification of the spinal muscular atrophy phenotype by cenSMN copy number. Am J Hum Genet 63 6 (1998) 1712-1723