RBM45 homo-oligomerization mediates association with ALS-linked proteins and stress granules

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Li, Yang ^a   Collins, Mahlon ^a,b   Geiser, Rachel ^a   Bakkar, Nadine ^a   Riascos, David ^a   Bowser, Robert ^a,b  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; DNA BINDING PROTEIN; NERVE PROTEIN; NUCLEAR LOCALIZATION SIGNAL; PROTEIN BINDING; RBM45 PROTEIN, HUMAN; RNA BINDING PROTEIN; RNA BINDING PROTEIN FUS;

ACTIVE TRANSPORT; AMINO ACID SEQUENCE; CELL INCLUSION; CELL LINE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR LOCALIZATION SIGNAL; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEINOSIS; SEQUENCE ALIGNMENT;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL LINE; DNA-BINDING PROTEINS; HUMANS; INCLUSION BODIES; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPS; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RNA-BINDING PROTEIN FUS; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT;

EID: 84942155885     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14262     Document Type: Article

References (48)

1. Ferraiuolo, L., Kirby, J., Grierson, A. J., Sendtner, M. & Shaw, P. J. Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nature reviews. Neurology 7, 616-630, doi: 10.1038/nrneurol.2011.152 (2011).
2. Robberecht, W. & Philips, T. The changing scene of amyotrophic lateral sclerosis. Nat Rev Neurosci 14, 248-264, doi: 10.1038/ nrn3430 (2013).
3. Gitcho, M. A. et al. TDP-43 A315T mutation in familial motor neuron disease. Annals of neurology 63, 535-538, doi: 10.1002/ ana.21344 (2008).
4. Kabashi, E. et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nature genetics 40, 572-574, doi: 10.1038/ng.132 (2008).
5. Sreedharan, J. et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319, 1668-1672, doi: 10.1126/science.1154584 (2008).
6. Kwiatkowski, T. J., Jr. et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323, 1205-1208, doi: 10.1126/science.1166066 (2009).
7. Vance, C. et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323, 1208-1211, doi: 10.1126/science.1165942 (2009).
8. Lagier-Tourenne, C., Polymenidou, M. & Cleveland, D. W. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Human molecular genetics 19, R46-64, doi: 10.1093/hmg/ddq137 (2010).
9. Colombrita, C. et al. TDP-43 is recruited to stress granules in conditions of oxidative insult. Journal of neurochemistry 111, 1051-1061, doi: 10.1111/j.1471-4159.2009.06383.x (2009).
10. Liu-Yesucevitz, L. et al. Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PloS one 5, e13250, doi: 10.1371/journal.pone.0013250 (2010).
11. Bosco, D. A. et al. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Human molecular genetics 19, 4160-4175, doi: 10.1093/hmg/ddq335 (2010).
12. Parker, S. J. et al. Endogenous TDP-43 localized to stress granules can subsequently form protein aggregates. Neurochemistry international 60, 415-424, doi: 10.1016/j.neuint.2012.01.019 (2012).
13. Lagier-Tourenne, C. & Cleveland, D. W. Rethinking ALS: the FUS about TDP-43. Cell 136, 1001-1004, doi: 10.1016/j. cell.2009.03.006 (2009).
14. Dormann, D. & Haass, C. TDP-43 and FUS: a nuclear affair. Trends in neurosciences, doi: 10.1016/j.tins.2011.05.002 (2011).
15. Dormann, D. et al. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. The EMBO journal 29, 2841-2857, doi: 10.1038/emboj.2010.143 (2010).
16. Winton, M. J. et al. Disturbance of nuclear and cytoplasmic TAR DNA-binding protein (TDP-43) induces disease-like redistribution, sequestration, and aggregate formation. The Journal of biological chemistry 283, 13302-13309, doi: 10.1074/jbc. M800342200 (2008).
17. Johnson, B. S. et al. TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. The Journal of biological chemistry 284, 20329-20339, doi: 10.1074/jbc.M109.010264 (2009).
18. Bentmann, E. et al. Requirements for stress granule recruitment of fused in sarcoma (FUS) and TAR DNA-binding protein of 43 kDa (TDP-43). The Journal of biological chemistry 287, 23079-23094, doi: 10.1074/jbc.M111.328757 (2012).
19. Lee, E. B., Lee, V. M. & Trojanowski, J. Q. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nature reviews. Neuroscience 13, 38-50, doi: 10.1038/nrn3121 (2012).
20. Collins, M. et al. The RNA-binding motif 45 (RBM45) protein accumulates in inclusion bodies in amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration with TDP-43 inclusions (FTLD-TDP) patients. Acta neuropathologica 124, 717-732, doi: 10.1007/s00401-012-1045-x (2012).
21. Tamada, H. et al. cDNA cloning and characterization of Drb1, a new member of RRM-type neural RNA-binding protein. Biochemical and biophysical research communications 297, 96-104 (2002).
22. Hans, F. et al. UBE2E ubiquitin-conjugating enzymes and ubiquitin isopeptidase Y regulate TDP-43 protein ubiquitination. The Journal of biological chemistry 289, 19164-19179, doi: 10.1074/jbc.M114.561704 (2014).
23. Kosugi, S., Hasebe, M., Tomita, M. & Yanagawa, H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA 106, 10171-10176, doi: 10.1073/pnas.0900604106 (2009).
24. Dingwall, C., Robbins, J., Dilworth, S. M., Roberts, B. & Richardson, W. D. The nucleoplasmin nuclear location sequence is larger and more complex than that of SV-40 large T antigen. The Journal of cell biology 107, 841-849 (1988).
25. King, O. D., Gitler, A. D. & Shorter, J. The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain research 1462, 61-80, doi: 10.1016/j.brainres.2012.01.016 (2012).
26. Shiina, Y., Arima, K., Tabunoki, H. & Satoh, J. TDP-43 dimerizes in human cells in culture. Cellular and molecular neurobiology 30, 641-652, doi: 10.1007/s10571-009-9489-9 (2010).
27. Wang, Y. T. et al. The truncated C-terminal RNA recognition motif of TDP-43 protein plays a key role in forming proteinaceous aggregates. The Journal of biological chemistry 288, 9049-9057, doi: 10.1074/jbc.M112.438564 (2013).
28. Zhang, Y. J. et al. The dual functions of the extreme N-terminus of TDP-43 in regulating its biological activity and inclusion formation. Hum Mol Genet 22, 3112-3122, doi: 10.1093/hmg/ddt166 (2013).
29. Dettmer, U., Newman, A. J., Luth, E. S., Bartels, T. & Selkoe, D. In vivo cross-linking reveals principally oligomeric forms of alpha-synuclein and beta-synuclein in neurons and non-neural cells. The Journal of biological chemistry 288, 6371-6385, doi: 10.1074/jbc.M112.403311 (2013).
30. Da Cruz, S. & Cleveland, D. W. Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr Opin Neurobiol 21, 904-919, doi: 10.1016/j.conb.2011.05.029 (2011).
31. Johnson, J. O. et al. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat Neurosci 17, 664-666, doi: 10.1038/nn.3688 (2014).
32. Soderberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3, 995-1000, doi: 10.1038/nmeth947 (2006).
33. Bentmann, E., Haass, C. & Dormann, D. Stress granules in neurodegeneration - lessons learnt from TAR DNA binding protein of 43 kDa and fused in sarcoma. FEBS J 280, 4348-4370, doi: 10.1111/febs.12287 (2013).
34. Li, Y. R., King, O. D., Shorter, J. & Gitler, A. D. Stress granules as crucibles of ALS pathogenesis. The Journal of cell biology 201, 361-372, doi: 10.1083/jcb.201302044 (2013).
35. Bakkar, N., Kousari, A., Kovalik, T., Li, Y. & Bowser, R. RBM45 Modulates the Antioxidant Response in Amyotrophic Lateral Sclerosis through Interactions with KEAP1. Molecular and cellular biology 35, 2385-2399, doi: 10.1128/MCB.00087-15 (2015).
36. Hussain, R. H., Zawawi, M. & Bayfield, M. A. Conservation of RNA chaperone activity of the human La-related proteins 4, 6 and 7. Nucleic acids research 41, 8715-8725, doi: 10.1093/nar/gkt649 (2013).
37. Song, Y. et al. Evidence for an RNA chaperone function of polypyrimidine tract-binding protein in picornavirus translation. Rna 11, 1809-1824, doi: 10.1261/rna.7430405 (2005).
38. Xu, T., Han, J. H. & Kang, H. Structural features important for the RNA chaperone activity of zinc finger-containing glycine-rich RNA-binding proteins from wheat (Triticum avestivum) and rice (Oryza sativa). Phytochemistry 94, 28-35, doi: 10.1016/j. phytochem.2013.05.019 (2013).
39. Ivanyi-Nagy, R., Davidovic, L., Khandjian, E. W. & Darlix, J. L. Disordered RNA chaperone proteins: from functions to disease. Cellular and molecular life sciences: CMLS 62, 1409-1417, doi: 10.1007/s00018-005-5100-9 (2005).
40. Collins, B. M. et al. Homomeric ring assemblies of eukaryotic Sm proteins have affinity for both RNA and DNA. Crystal structure of an oligomeric complex of yeast SmF. The Journal of biological chemistry 278, 17291-17298, doi: 10.1074/jbc.M211826200 (2003).
41. Buratti, E. et al. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. The Journal of biological chemistry 280, 37572-37584, doi: 10.1074/jbc.M505557200 (2005).
42. Lagier-Tourenne, C. et al. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nature neuroscience 15, 1488-1497, doi: 10.1038/nn.3230 (2012).
43. Gitler, A. D. T. D. P.-4. 3. and FUS/TLS yield a target-rich haul in ALS. Nature neuroscience 15, 1467-1469, doi: 10.1038/nn.3243 (2012).
44. Polymenidou, M. et al. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 14, 459-468, doi: 10.1038/nn.2779 (2011).
45. Tollervey, J. R. et al. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 14, 452-458, doi: 10.1038/nn.2778 (2011).
46. Aiyar, A., Xiang, Y. & Leis, J. Site-directed mutagenesis using overlap extension PCR. Methods Mol Biol 57, 177-191, doi: 10.1385/0-89603-332-5:177 (1996).
47. Ponti, A., Gulati, A., Bäcker, V. & Schwarb, P. Huygens Remote Manager, a Web Interface for High-Volume Batch Deconvolution. Imaging & Microscopy 9, 57-58 (2007).
48. Klockenbusch, C. & Kast, J. Optimization of formaldehyde cross-linking for protein interaction analysis of non-tagged integrin beta1. J Biomed Biotechnol 2010, 927585, doi: 10.1155/2010/927585 (2010).