Nuclear Fragile X Mental Retardation Protein Is localized to Cajal Bodies

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Dury, Alain Y ^a,b   El Fatimy, Rachid ^a,b   Tremblay, Sandra ^a   Rose, Timothy M ^c   Côté, Jocelyn ^d   De Koninck, Paul ^a,b   Khandjian, Edouard W ^a,b  

^a Centre de recherche   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; ISOPROTEIN; MESSENGER RIBONUCLEOPROTEIN; MESSENGER RNA; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COILED BODY; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FRAGILE X SYNDROME; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MICROTUBULE; MISSENSE MUTATION; MOLECULAR WEIGHT; OPEN READING FRAME; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RNA METABOLISM; SEQUENCE ALIGNMENT; ANIMAL; BIOSYNTHESIS; CELL NUCLEUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; NERVE CELL; PATHOLOGY; ULTRASTRUCTURE;

ANIMALS; CELL NUCLEUS; COILED BODIES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE EXPRESSION REGULATION; HUMANS; MICE; NEURONS; PROTEIN ISOFORMS; RIBONUCLEOPROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84887308928     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003890     Document Type: Article

References (67)

1. O'Donnell WT, Warren ST, (2002) A decade of molecular studies of fragile X syndrome. Annu Rev Neurosci 25: 315-338.
2. Bardoni B, Davidovic L, Bensaid M, Khandjian EW, (2006) The fragile X syndrome: exploring its molecular basis and seeking a treatment. Expert Rev Mol Med 8: 1-16.
3. Bassell GJ, Warren ST, (2008) Fragile X Syndrome: Loss of local mRNA regulation alters synaptic development and function. Neuron 60: 201-214.
4. Devys D, Lutz Y, Rouyer N, Bellocq J-P, Mandel J-L, (1993) The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation. Nat Genet 4: 335-340.
5. Siomi H, Siomi MC, Nussbaum RL, Dreyfuss G, (1993) The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74: 291-298.
6. Corbin F, Bouillon M, Fortin A, Morin S, Rousseau F, et al. (1997) The fragile X mental retardation protein is associated with poly(A)+ mRNA in actively translating polyribosomes. Hum Mol Genet 6: 1465-1472.
7. Khandjian EW, Huot ME, Tremblay S, Davidovic L, Mazroui R, et al. (2004) Biochemical evidence for the association of fragile X mental retardation protein with brain polyribosomal ribonucleoparticles. Proc Natl Acad Sci USA 101: 13357-13362.
8. Stefani G, Fraser CE, Darnell JC, Darnell RB, (2004) Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J Neurosci 24: 7272-7276.
9. Antar LN, Dictenberg JB, Plociniak M, Afroz R, Bassell GJ, (2005) Localization of FMRP-associated mRNA granules and requirement of microtubules for activity-dependent trafficking in hippocampal neurons. Genes Brain Behav 4: 350-359.
10. Khandjian EW, Tournier B, Séguin S, Tremblay S, De Koninck P, et al. (2009) RNA Granules: Functions within Presynaptic Terminals and Postsynaptic Spines. Encyclopedia of Neuroscience 8: 389-395.
11. Darnell JC, (2011) Defects in translational regulation contributing to human cognitive and behavioral disease. Curr Opin Genet Dev 21: 465-473.
12. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, et al. (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146: 247-261.
13. Eberhart DE, Malter HE, Feng Y, Warren ST, (1996) The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum Mol Genet 5: 1083-1091.
14. Fridell RA, Benson RE, Hua J, Bogerd HP, Cullen BR, (1996) A nuclear role for the Fragile X mental retardation protein. EMBO J 15: 5408-5414.
15. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST, et al. (1997) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J Neurosci 17: 1539-1547.
16. Verheij C, Bakker CE, de Graaff E, Keulemans J, Willemsen R, et al. (1993) Characterization and localization of the FMR-1 gene product associated with fragile X syndrome. Nature 363: 722-724.
17. Sittler A, Devys D, Weber C, Mandel J-L, (1996) Alternative splicing of exon 14 determines nuclear or cytoplasmic localisation of fmr1 protein isoforms. Hum Mol Genet 5: 95-102.
18. El Fatimy R, Tremblay S, Dury AY, Solomon S, De Koninck P, et al. (2012) Fragile X mental retardation protein interacts with the RNA-binding protein Caprin1 in neuronal ribonucleoprotein complexes. PLoS One 7 (6) (): e39338.
19. Liu Q, Dreyfuss G, (1996) A novel nuclear structure containing the survival of motor neurons protein. EMBO J 15: 3555-3565.
20. Nizami ZF, Deryusheva S, Gall JG (2010) Cajal bodies and histone locus bodies in Drosophila and Xenopus. In: Nuclear organization and function. Cold Spring Harbor symposia on quantitative biology. Vol LXXV. pp313-320. Cold Spring Harbor Laboratory Press.
21. Gall JG, (2000) Cajal Bodies: The First 100 Years. Annu Rev Cell Dev Biol 16: 273-300.
22. Cioce M, Lamond AI, (2005) Cajal Bodies: A Long History of Discovery. Annu Rev Cell Dev Biol 21: 105-131.
23. Hebert MD, (2010) Phosphorylation and the Cajal body: modification in search of function. Arch Biochem Biophys 496: 69-76.
24. Ben-Ze'ev A, Duerr A, Solomon F, Penman S, (1979) The outer boundary of the cytoskeleton: a lamina derived from plasma membrane proteins. Cell 17: 859-865.
25. Staufenbiel M, Deppert W, (1982) Intermediate filament systems are collapsed onto the nuclear surface after isolation of nuclei from tissue culture cells. Exp Cell Res 138: 207-214.
26. Fey EG, Wan KM, Penman S, (1984) Epithelial cytoskeletal framework and nuclear matrix-intermediate filament scaffold: three-dimensional organization and protein composition. J Cell Biol 98: 1973-1984.
27. Kuersten S, Ohno M, Mattaj IW, (2001) Nucleocytoplasmic transport: Ran, beta and beyond. Trends Cell Biol 11: 497-503.
28. Tamanini F, Bontekoe C, Bakker CE, van Unen L, Anar B, et al. (1999) Different targets for the fragile X-related proteins revealed by their distinct nuclear localizations. Hum Mol Genet 8: 863-869.
29. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, et al. (2002) Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11: 3007-3017.
30. Carvalho T, Almeida F, Calapez A, Lafarga M, Berciano MT, Carmo-Fonseca M, (1999) The spinal muscular atrophy disease gene product, SMN: A link between snRNP biogenesis and the Cajal (coiled) body. J Cell Biol 147: 715-728.
31. Sleeman JE, Ajuh P, Lamond AI, (2001) snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J Cell Sci 114: 4407-4419.
32. Ashley CT, Sutcliffe JS, Kunst CB, Leiner HA, Eichler EE, et al. (1993) Human and murine FMR-1: alternative splicing and translational initiation downstream of the CGG-repeat. Nature Genet 4: 244-251.
33. Verkerk AJMH, de Graaf E, De Boulle K, Eichler EE, Koonecki DS, et al. (1993) Alternative splicing in the fragile X gene FMR1. Hum Mol Genet 2: 399-404.
34. Eichler EE, Richards S, Gibbs RA, Nelson DL, (1993) Fine structure of the human FMR1 gene. Hum Mol Genet 2: 1147-1153.
35. Brackett DM, Qing F, Amieux PS, Sellers DL, Horner PJ, et al. (2013) Fmr1 transcript isoforms: association with polyribosomes; regional and developmental expression in mouse brain. PLoS ONE 8 (3) (): e58296.
36. Valverde R, Pozdnyakova I, Kajander T, Venkatraman J, Regan L, (2007) Fragile X mental retardation syndrome: structure of the KH1-KH2 domains of fragile X mental retardation protein. Structure 15: 1090-1098.
37. Kosugi S, Hasebe M, Tomita M, Yanagawa H, (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA 106: 10171-10176.
38. Lam YW, Lyon CE, Lamond AI, (2002) Large-scale isolation of Cajal bodies from HeLa cells. Mol Biol Cell 13: 2461-2473.
39. Lam YW. Cajal Body Isolation Protocol. http://www.lamondlab.com/f7cbprotocol.htm.
40. Gabel LA, Won S, Kawai H, McKinney M, Tartakoff AM, et al. (2004) Visual experience regulates transient expression and dendritic localization of fragile X mental retardation protein. J Neurosci 24: 10579-10583.
41. Walker MP, Rajendra TK, Saieva L, Fuentes JL, Pellizzoni L, et al. (2008) SMN complex localizes to the sarcomeric Z-disc and is proteolytic target of calpain. Hum Mol Genet 17: 3399-3410.
42. Fuentes JL, Strayer MS, Matera AG, (2010) Molecular determinants of Survival Motor Neuron (SMN) protein cleavage by the calcium-activated protease, Calpain. PLoS ONE 5 (12) (): e15769.
43. Velma V, Broome HJ, Hebert MD, (2012) Regulated specific proteolysis of the Cajal body marker protein coilin. Chromosoma 121: 629-642.
44. DuVerle DA, Ono Y, Sorimachi H, Mamitsuka H, (2011) Calpain cleavage prediction using multiple kernel learning. PLoS ONE 6 (5) (): e19035.
45. Swanson MS, Dreyfuss G, (1988) Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol Cell Biol 8: 2237-2241.
46. DeBoulle K, Verkerk AJ, Reyniers E, Vits L, Hendrickx J, et al. (1993) A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nature Genet 3: 31-35.
47. Feng Y, Absher D, Eberhart DE, Brown V, Malter HE, et al. (1997) FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol Cell 1: 109-118.
48. Darnell JC, Fraser CE, Mostovetsky O, Stefani G, Jones TA, et al. (2005) Kissing complex RNAs mediate interaction between the Fragile-X mental retardation protein KH2 domain and brain polyribosomes. Genes Dev 19: 903-918.
49. Zang JB, Nosyreva ED, Spencer CM, Volk LJ, Musunuru K, et al. (2009) A Mouse Model of the Human Fragile X Syndrome I304N Mutation. PLoS Genet 5 (12) (): e1000758.
50. Dundr M, Hebert MD, Karpova TS, Stanek D, Xu H, et al. (2004) In vivo kinetics of Cajal body components. J Cell Biol 164: 831-842.
51. Kim M, Bellini M, Ceman S, (2009) Fragile X mental retardation protein FMRP binds mRNAs in the nucleus. Mol Cell Biol 29: 214-228.
52. Siomi MC, Zhang Y, Siomi H, Dreyfuss G, (1996) Specific sequences in the fragile X syndrome protein FMR1 and the FXR proteins mediate their binding to 60S ribosomal subunits and the interactions among them. Mol Cell Biol 16: 3825-3832.
53. Ramos A, Hollingworth D, Adinolfi S, Castets M, Kelly G, et al. (2006) The structure of the N-terminal domain of the fragile X mental retardation protein: a platform for protein-protein interaction. Structure 14: 21-31.
54. Schenck A, Bardoni B, Moro A, Bagni C, Mandel J-L, (2001) A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc Natl Acad Sci USA 98: 8844-8849.
55. Davidovic L, Bechara E, Gravel M, Jaglin XH, Tremblay S, et al. (2006) The nuclear microspherule protein 58 is a novel RNA-binding protein that interacts with fragile X mental retardation protein in polyribosomal mRNPs from neurons. Hum Mol Genet 15: 1525-1538.
56. Bardoni B, Castets M, Huot ME, Schenck A, Adinolfi S, et al. (2003) 82-FIP, a novel FMRP (fragile X mental retardation protein) interacting protein, shows a cell cycle-dependent intracellular localization. Hum Mol Genet 12: 1689-1698.
57. Piazzon N, Rage F, Schlotter F, Moine H, Branlant C, et al. (2008) In vitro and in cellulo evidences for association of the survival of motor neuron complex with the fragile X mental retardation protein. J Biol Chem 283: 5598-5610.
58. Menon RP, Gibson TJ, Pastore A, (2004) The C terminus of fragile X mental retardation protein interacts with the multi-domain Ran-binding protein in the microtubule-organising centre. J Mol Biol 343: 43-53.
59. Bardoni B, Schenck A, Mandel JL, (1999) A novel RNA-binding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum Mol Genet 8: 2557-2566.
60. Bardoni B, Willemsen R, Weiler IJ, Schenck A, Severijnen LA, et al. (2003) NUFIP1 (nuclear FMRP interacting protein 1) is a nucleocytoplasmic shuttling protein associated with active synaptoneurosomes. Exp Cell Res 289: 95-107.
61. Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, et al. (2008) The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 180: 579-595.
62. Garcia-Lopez P, Garcia-Marin V, Freire M, (2010) The histological slides and drawings of Cajal. Front Neuroanat 4: 1-16.
63. Platani M, Goldberg I, Swedlow JR, Lamond AI, (2000) In vivo analysis of Cajal body movement, separation, and joining in live human cells. J Cell Biol 151: 1561-1574.
64. Broome HJ, Hebert MD, (2013) Coilin displays differential affinity for specific RNAs in vivo and is linked to telomerase RNA biogenesis. J Mol Biol 425: 713-724.
65. Hubers L, Valderrama-Carvajal H, Laframboise J, Timbers J, Sanchez G, et al. (2011) HuD interacts with survival motor neuron protein and can rescue spinal muscular atrophy-like neuronal defects. Hum Mol Genet 20: 553-579.
66. Chamousset D, De Wever V, Moorhead GB, Chen Y, Boisvert FM, et al. (2010) RRP1B targets PP1 to mammalian cell nucleoli and is associated with Pre-60S ribosomal subunits. Mol Biol Cell 21: 4212-4226.
67. Zacharias DA, Violin JD Newton AC, Tsien RY, (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296: 913-916.