Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS)

Brain Research

Volumn 1305, Issue , 2009, Pages 168-182

  Volkening, Kathryn ^a   Leystra Lantz, Cheryl ^a   Yang, Wenchang ^a   Jaffee, Howard ^b   Strong, Michael J ^a,c  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

(SOD1); 14 3 3; Amyotrophic lateral sclerosis; Copper zinc superoxide dismutase 1; RNA binding protein; TDP 43

Indexed keywords

DNA BINDING PROTEIN; MESSENGER RNA; NEUROFILAMENT PROTEIN; NEUROFILAMENT PROTEIN L; PROTEIN 14 3 3; PROTEIN TDP-43; RNA BINDING PROTEIN; SUPEROXIDE DISMUTASE; TAR DNA BINDING PROTEIN;

3' UNTRANSLATED REGION; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; IMMUNOPRECIPITATION; METABOLISM; MOTONEURON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; RNA TRANSPORT; SPINAL CORD; WESTERN BLOTTING;

14-3-3 PROTEINS; 3' UNTRANSLATED REGIONS; AMYOTROPHIC LATERAL SCLEROSIS; BLOTTING, WESTERN; CELLS, CULTURED; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MOTOR NEURONS; NEUROFILAMENT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 73949134014     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.09.105     Document Type: Article

References (52)

1. Anderson, P., Kedersha, N., 2006. RNA granules. J. Cell Biol. 172, 803-808.
2. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., Mann, D., Tsuchiya, K., Yoshida, M., Hashizume, Y., Oda, T., 2006. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 351, 602-611. (Pubitemid 44708852)
3. Beaulieu, J.M., Jacomy, H., Julien, J.P., 2000. Formation of intermediate filament protein aggregates with disparate effects in two transgenic mouse models lacking the neurofilament light subunit. J. Neurosci. 20, 5321-5328. (Pubitemid 30457729)
4. Bergeron, C., Beric-Maskarel, K., Muntasser, S., Weyer, L., Somerville, M.J., Percy, M.E., 1994. Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J. Neuropathol. Exp. Neurol. 53, 221-230. (Pubitemid 24146859)
5. Bonifaci, N., Moroianu, J., Radu, A., Blobel, G., 1997. Karyopherin beta2 mediates nuclear import of a mRNA binding protein. Proc. Natl. Acad. Sci. U. S. A 94, 5055-5060. (Pubitemid 27214735)
6. Buratti, E., Baralle, F.E., 2001. Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J. Biol. Chem. 276, 36337-36343.
7. Burston, S.G., Clarke, A.R., 1995. Molecular chaperones: physical and mechanistic properties. Essays Biochem. 29, 125-136.
8. Canete-Soler, R., Wu, J., Zhai, J., Shamim, M., Schlaepfer, W.W., 2001. p190RhoGEF Binds to a destabilizing element in the 3′ untranslated region of light neurofilament subunit mRNA and alters the stability of the transcript. J. Biol. Chem. 276, 32046-32050.
9. Canete-Soler, R., Reddy, K.S., Tolan, D.R., Zhai, J., 2005. Aldolases A and C are ribonucleolytic components of a neuronal complex that regulates the stability of the light-neurofilament mRNA. J. Neurosci. 25, 4353-4364. (Pubitemid 40628779)
10. Elvira, G., Wasiak, S., Blandford, V., Tong, X.K., Serrano, A., Fan, X., del, R.S.-C., Servant, F., Bell, A.W., Boismenu, D., Lacaille, J.C., McPherson, P.S., DesGroseillers, L., Sossin, W.S., 2006. Characterization of an RNA granule from developing brain. Mol. Cell. Proteomics. 5, 635-651.
11. Fillman, C., Lykke-Andersen, J., 2005. RNA decapping inside and outside of processing bodies. Curr. Opin. Cell Biol. 17, 326-331. (Pubitemid 40719924)
12. Ge, W., Wu, J., Zhai, J., Nie, Z., Lin, H., Schlaepfer, W.W., Canete-Soler, R., 2002. Binding of p190RhoGEF to a destabilizing element on the light neurofilament mRNA is competed by BC1 RNA. J. Biol. Chem. 277, 42701-42705. (Pubitemid 35285640)
13. Ge, W.W., Wen, W., Strong, W., Leystra-Lantz, C., Strong, M.J., 2005. Mutant copper-zinc superoxide dismutase binds to and destabilizes human low molecular weight neurofilament mRNA. J. Biol. Chem. 280, 118-124. (Pubitemid 40164972)
14. Ge, W.W., Volkening, K., Leystra-Lantz, C., Jaffe, H., Strong, M.J., 2007. 14-3-3 protein binds to the low molecular weight neurofilament (NFL) mRNA 3′ UTR. Mol. Cell. Neurosci. 34, 80-87. (Pubitemid 46026930)
15. Gilks, N., Kedersha, N., Ayodele, M., Shen, L., Stoecklin, G., Dember, L.M., Anderson, P., 2004. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15, 5383-5398. (Pubitemid 39564732)
16. Hirokawa, N., 2006. mRNA transport in dendrites: RNA granules, motors, and tracks. J. Neurosci. 26, 7139-7142.
17. Jeong, J.H., Nam, Y.J., Kim, S.Y., Kim, E.G., Jeong, J., Kim, H.K., 2007. The transport of Staufen 2-containing ribonucleoprotein complexes involves kinesin motor protein and is modulated by mitogen-activated protein kinase pathway. J. Neurochem. 102, 2073-2084. (Pubitemid 47329284)
18. Julien, J.P., 1999. Neurofilament functions in health and disease. Curr. Opin. Neurobiol. 9, 554-560.
19. Kanai, Y., Dohmae, N., Hirokawa, N., 2004. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525. (Pubitemid 39094678)
20. Kedersha, N., Anderson, P., 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30, 963-969. (Pubitemid 36002389)
21. Kedersha, N., Cho, M.R., Li, W., Yacono, P.W., Chen, S., Gilks, N., Golan, D.E., Anderson, P., 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151, 1257-1268.
22. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D., Kaufman, R.J., Golan, D.E., Anderson, P., 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169, 871-884. (Pubitemid 41002864)
23. Kedersha, N.L., Gupta, M., Li, W., Miller, I., Anderson, P., 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147, 1431-1442.
24. Kim, K.C., Kim, H.K., 2006. Role of Staufen in dendritic mRNA transport and its modulation. Neurosci. Lett. 397, 48-52. (Pubitemid 43340457)
25. Li, X., Lu, L., Bush, D.J., Zhang, X., Zheng, L., Suswam, E.A., King, P.H., 2009. Mutant copper-zinc superoxide dismutase associated with amyotrophic lateral sclerosis binds to adenine/uridine-rich stability elements in the vascular endothelial growth factor 3′-untranslated region. J. Neurochem. 108, 1032-1044.
26. Li, Y., Jiang, Z., Chen, H., Ma, W.J., 2004. A modified quantitative EMSA and its application in the study of RNA-protein interactions. J. Biochem. Biophys. Methods 60, 85-96. (Pubitemid 38953054)
27. Mackenzie, I.R., Bigio, E.H., Ince, P.G., Geser, F., Neumann, M., Cairns, N.J., Kwong, L.K., Forman, M.S., Ravits, J., Stewart, H., Eisen, A., McClusky, L., Kretzschmar, H.A., Monoranu, C.M., Highley, J.R., Kirby, J., Siddique, T., Shaw, P.J., Lee, V.M., Trojanowski, J.Q., 2007. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann. Neurol. 61, 427-434. (Pubitemid 46878770)
28. Mallardo, M., Deitinghoff, A., Muller, J., Goetze, B., Macchi, P., Peters, C., Kiebler, M.A., 2003. Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc. Natl. Acad. Sci. U. S. A 100, 2100-2105. (Pubitemid 36254580)
29. Mathews, D.H., Sabina, J., Zuker, M., Turner, D.H., 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288, 911-940. (Pubitemid 29248642)
30. Meier, J., Couillard-Despres, S., Jacomy, H., Gravel, C., Julien, J.P., 1999. Extra neurofilament NF-L subunits rescue motor neuron disease caused by overexpression of the human NF-H gene in mice. J. Neuropathol. Exp. Neurol. 58, 1099-1110. (Pubitemid 29468271)
31. Moisse, K., Volkening, K., Leystra-Lantz, C., Welch, I., Hill, T., Strong, M.J., 2009. Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: implications for TDP-43 in the physiological response to neuronal injury. Brain Res. 1249, 202-211.
32. Moroianu, J., 1998. Distinct nuclear import and export pathways mediated by members of the karyopherin beta family. J. Cell Biochem. 70, 231-239. (Pubitemid 28308932)
33. Mulder, D.W., Kurland, L.T., Offord, K.P., Beard, C.M., 1986. Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 36, 511-517. (Pubitemid 16070005)
34. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T., Bruce, J., Schuck, T., Grossman, M., Clark, C.M., McCluskey, L.F., Miller, B.L., Masliah, E., Mackenzie, I.R., Feldman, H., Feiden, W., Kretzschmar, H.A., Trojanowski, J.Q., Lee, V.M., 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130-133. (Pubitemid 44547757)
35. Orban, T.I., Izaurralde, E., 2005. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11, 459-469. (Pubitemid 40397179)
36. Parker, R., Sheth, U., 2007. P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646. (Pubitemid 46341926)
37. Price, T.J., Flores, C.M., Cervero, F., Hargreaves, K.M., 2006. The RNA binding and transport proteins staufen and fragile X mental retardation protein are expressed by rat primary afferent neurons and localize to peripheral and central axons. Neuroscience 141, 2107-2116.
38. Ranson, N.A., White, H.E., Saibil, H.R., 1998. Chaperonins. Biochem. J. 333 (Pt. 2), 233-242. (Pubitemid 28379521)
39. Shaw, B.F., Lelie, H.L., Durazo, A., Nersissian, A.M., Xu, G., Chan, P.K., Gralla, E.B., Tiwari, A., Hayward, L.J., Borchelt, D.R., Valentine, J.S., Whitelegge, J.P., 2008. Detergent-insoluble aggregates associated with amyotrophic lateral sclerosis in transgenic mice contain primarily full-length, unmodified superoxide dismutase-1. J. Biol. Chem. 283, 8340-8350.
40. Smith, R., 2004. Moving molecules: mRNA trafficking in mammalian oligodendrocytes and neurons. Neuroscientist. 10, 495-500. (Pubitemid 39546392)
41. Stefanizzi, I., Canete-Soler, R., 2007. Coregulation of light neurofilament mRNA by poly(A)-binding protein and aldolase C: implications for neurodegeneration. Brain Res. 1139, 15-28. (Pubitemid 46335697)
42. Stoecklin, G., Mayo, T., Anderson, P., 2006. ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep. 7, 72-77.
43. Strong, M.J., 1999. Neurofilament metabolism in sporadic amyotrophic lateral sclerosis. J. Neurol. Sci. 169, 170-177. (Pubitemid 29502526)
44. Strong, M.J., Leystra-Lantz, C., Ge, W.W., 2004. Intermediate filament steady-state mRNA levels in amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 316, 317-322. (Pubitemid 38338595)
45. Strong, M.J., Volkening, K., Hammond, R., Yang, W., Strong, W., Leystra-Lantz, C., Shoesmith, C., 2007. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol. Cell. Neurosci. 35, 320-327. (Pubitemid 46843567)
46. Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M., Parker, R., 2005. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11, 371-382. (Pubitemid 40397171)
47. Thomas, M.G., Martinez Tosar, L.J., Loschi, M., Pasquini, J.M., Correale, J., Kindler, S., Boccaccio, G.L., 2005. Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Mol. Biol. Cell 16, 405-420. (Pubitemid 40024321)
48. Volkening, K., Leystra-Lantz, C., Strong, M.J., 2009. Human low molecular weight neurofilament (NFL) mRNA interacts with a predicted p190RhoGEF homologue (RGNEF) in humans. Amyotroph. Lateral Scler. 1-7.
49. Wang, I.F., Wu, L.S., Chang, H.Y., Shen, C.K., 2008. TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 105, 797-806.
50. Winton, M.J., Igaz, L.M., Wong, M.M., Kwong, L.K., Trojanowski, J.Q., Lee, V.M., 2008. Disturbance of nuclear and cytoplasmic TAR DNA-binding protein (TDP-43) induces disease-like redistribution, sequestration, and aggregate formation. J. Biol. Chem. 283, 13302-13309.
51. Zhang, Y.J., Xu, Y.F., Dickey, C.A., Buratti, E., Baralle, F., Bailey, R., Pickering-Brown, S., Dickson, D., Petrucelli, L., 2007. Progranulin mediates caspase-dependent cleavage of TAR DNA binding protein-43. J. Neurosci. 27, 10530-10534. (Pubitemid 47501990)
52. Zuker, M., 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic. Acids Res. 31, 3406-3415. (Pubitemid 37442169)