Distinct partitioning of ALS associated TDP-43, FUS and SOD1 mutants into cellular inclusions

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Farrawell, Natalie E ^a,b   Lambert Smith, Isabella A ^a,b   Warraich, Sadaf T ^d   Blair, Ian P ^d   Saunders, Darren N ^e,f   Hatters, Danny M ^c   Yerbury, Justin J ^a,b  

^a ILLAWARRA HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF WOLLONGONG   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MACQUARIE UNIVERSITY   (Australia)

^e GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^f ST VINCENT'S CLINIC   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; MUTANT PROTEIN; PROTEIN AGGREGATE; RNA BINDING PROTEIN FUS; SUPEROXIDE DISMUTASE; TDP-43 PROTEIN, HUMAN; UBIQUITIN;

AMYOTROPHIC LATERAL SCLEROSIS; CELL INCLUSION; ENZYME SPECIFICITY; GENETIC TRANSFECTION; HUMAN; METABOLISM; MICROTUBULE; TUMOR CELL LINE; UBIQUITINATION;

AMYOTROPHIC LATERAL SCLEROSIS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; HUMANS; INCLUSION BODIES; MICROTUBULES; MUTANT PROTEINS; PROTEIN AGGREGATES; RNA-BINDING PROTEIN FUS; SUBSTRATE SPECIFICITY; SUPEROXIDE DISMUTASE; TRANSFECTION; UBIQUITIN; UBIQUITINATION;

EID: 84940185085     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13416     Document Type: Article

References (70)

1. Rosen, D. R. et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62 (1993).
2. Kwiatkowski, T. J. Jr et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 323, 1205-1208 (2009).
3. Vance, C. et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 323, 1208-1211 (2009).
4. Nishimura, A. L. et al. A mutation in the vesicle-trafcking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. American Journal of Human Genetics 75, 822-831 (2004).
5. Kabashi, E. et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nature Genetics 40, 572-574 (2008).
6. Sreedharan, J. et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 319, 1668-1672 (2008).
7. Maruyama, H. et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 465, 223-226 (2010).
8. Johnson, J. O. et al. Exome Sequencing Reveals VCP Mutations as a Cause of Familial ALS. Neuron 68, 857-864 (2010).
9. Rea, S. L., Majcher, V., Searle, M. S. & Layfeld, R. SQSTM1 mutations-Bridging Paget disease of bone and ALS/FTLD. Experimental Cell Research 325, 27-37 (2014).
10. Deng, H. X. et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 477, 211-215 (2011).
11. Wu, C. H. et al. Mutations in the proflin 1 gene cause familial amyotrophic lateral sclerosis. Nature 488, 499-503 (2012).
12. Johnson, J. O. et al. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat Neurosci 17, 664-666 (2014).
13. DeJesus-Hernandez, M. et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72, 245-256 (2011).
14. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75, 333-366 (2006).
15. Giordana, M. T. et al. TDP-43 redistribution is an early event in sporadic amyotrophic lateral sclerosis. Brain Pathol 20, 351-360 (2010).
16. Brettschneider, J. et al. TDP-43 pathology and neuronal loss in amyotrophic lateral sclerosis spinal cord. Acta neuropathologica 128, 423-437 (2014).
17. Ticozzi, N., Ratti, A. & Silani, V. Protein aggregation and deffective RNA metabolism as mechanisms for motor neuron damage. CNS and Neurological Disorders-Drug Targets 9, 285-296 (2010).
18. Leigh, P. N. et al. Ubiquitin-immunoreactive intraneuronal inclusions in amyotrophic lateral sclerosis. Morphology, distribution, and specifcity. Brain 114, 775-788 (1991).
19. Strong, M. J., Kesavapany, S. & Pant, H. C. The pathobiology of amyotrophic lateral sclerosis: A proteinopathy? Journal of Neuropathology and Experimental Neurology 64, 649-664 (2005).
20. Grad, L. I. et al. Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and-independent mechanisms. Proc Natl Acad Sci USA 111, 3620-3625 (2014).
21. Sherman, M. Y. & Goldberg, A. L. Cellular Defences against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron 29, 15-32 (2001).
22. Yerbury, J. J. & Kumita, J. R. Protein chemistry of amyloid fbrils and chaperones: Implications for amyloid formation and disease. Current Chemical Biology 4, 89-98 (2010).
23. Huang, Q. & Figueiredo-Pereira, M. E. Ubiquitin/proteasome pathway impairment in neurodegeneration: Terapeutic implications. Apoptosis 15, 1292-1311 (2010).
24. Yerbury, J. J. et al. The small heat shock proteins alphaB-crystallin and Hsp27 suppress SOD1 aggregation in vitro. Cell stress & chaperones 18, 251-257 (2013).
25. Kwong, L. K., Neumann, M., Sampathu, D. M., Lee, V. M. Y. & Trojanowski, J. Q. TDP-43 proteinopathy: The neuropathology underlying major forms of sporadic and familial frontotemporal lobar degeneration and motor neuron disease. Acta Neuropathologica 114, 63-70 (2007).
26. Liscic, R. M., Grinberg, L. T., Zidar, J., Gitcho, M. A. & Cairns, N. J. ALS and FTLD: Two faces of TDP-43 proteinopathy. European Journal of Neurology 15, 772-780 (2008).
27. Mackenzie, I. R. A. et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Annals of Neurology 61, 427-434 (2007).
28. Bolognesi, B. et al. ANS binding reveals common features of cytotoxic amyloid species. ACS chemical biology 5, 735-740 (2010).
29. Johnston, J. A., Ward, C. L. & Kopito, R. R. Aggresomes: a cellular response to misfolded proteins. The Journal of cell biology 143, 1883-1898 (1998).
30. Kaganovich, D., Kopito, R. & Frydman, J. Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095 (2008).
31. Weisberg, S. J. et al. Compartmentalization of superoxide dismutase 1 (SOD1G93A) aggregates determines their toxicity. Proceedings of the National Academy of Sciences of the United States of America 109, 15811-15816 (2012).
32. Hipp, M. S. et al. Indirect inhibition of 26S proteasome activity in a cellular model of Huntington's disease. The Journal of cell biology 196, 573-587 (2012).
33. Polling, S. et al. Misfolded polyglutamine, polyalanine, and superoxide dismutase 1 aggregate via distinct pathways in the cell. J Biol Chem 289, 6669-6680 (2014).
34. Yang, C. et al. The C-terminal TDP-43 fragments have a high aggregation propensity and harm neurons by a dominant-negative mechanism. PloS one 5, e15878 (2010).
35. Che, M. X., Jiang, Y. J., Xie, Y. Y., Jiang, L. L. & Hu, H. Y. Aggregation of the 35-kDa fragment of TDP-43 causes formation of cytoplasmic inclusions and alteration of RNA processing. FASEB journal: ofcial publication of the Federation of American Societies for Experimental Biology 25, 2344-2353 (2011).
36. Deng, H. X. et al. FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis. Annals of Neurology 67, 739-748 (2010).
37. Blair, I. P. et al. FUS mutations in amyotrophic lateral sclerosis: clinical, pathological, neurophysiological and genetic analysis. Journal of neurology, neurosurgery, and psychiatry 81, 639-645 (2010).
38. Sun, Z. et al. Molecular determinants and genetic modifers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS Biol 9, e1000614 (2011).
39. Maekawa, S. et al. TDP-43 is consistently co-localized with ubiquitinated inclusions in sporadic and Guam amyotrophic lateral sclerosis but not in familial amyotrophic lateral sclerosis with and without SOD1 mutations. Neuropathology: ofcial journal of the Japanese Society of Neuropathology 29, 672-683 (2009).
40. Pesiridis, G. S., Tripathy, K., Tanik, S., Trojanowski, J. Q. & Lee, V. M. A "two-hit" hypothesis for inclusion formation by carboxyl-terminal fragments of TDP-43 protein linked to RNA depletion and impaired microtubule-dependent transport. J Biol Chem 286, 18845-18855 (2011).
41. Shelkovnikova, T. A., Robinson, H. K., Connor-Robson, N. & Buchman, V. L. Recruitment into stress granules prevents irreversible aggregation of FUS protein mislocalized to the cytoplasm. Cell Cycle 12, 3194-3202 (2013).
42. Muchowski, P. J., Ning, K., D'Souza-Schorey, C. & Fields, S. Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc Natl Acad Sci USA 99, 727-732 (2002).
43. Johnston, J. A., Dalton, M. J., Gurney, M. E. & Kopito, R. R. Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America 97, 12571-12576 (2000).
44. Meriin, A. B. et al. Intracellular aggregation of polypeptides with expanded polyglutamine domain is stimulated by stress-activated kinase MEKK1. J Cell Biol 153, 851-864 (2001).
45. Ben-Gedalya, T. et al. Cyclosporin-A-induced prion protein aggresomes are dynamic quality-control cellular compartments. J Cell Sci 124, 1891-1902 (2011).
46. Scotter, E. L. et al. Diferential roles of the ubiquitin proteasome system and autophagy in the clearance of soluble and aggregated TDP-43 species. J Cell Sci 127, 1263-1278 (2014).
47. Knowles, T. P., Vendruscolo, M. & Dobson, C. M. The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 15, 384-396 (2014).
48. Kato, M. et al. Cell-free Formation of RNA Granules: Low Complexity Sequence Domains Form Dynamic Fibers within Hydrogels. Cell 149, 753-767 (2012).
49. Buchan, J. R., Kolaitis, R. M., Taylor, J. P. & Parker, R. Eukaryotic Stress Granules Are Cleared by Autophagy and Cdc48/VCP Function. Cell 153, 1461-1474 (2013).
50. Niwa, J. et al. Dorfn Ubiquitylates Mutant SOD1 and Prevents Mutant SOD1-mediated Neurotoxicity. Journal of Biological Chemistry 277, 36793-36798 (2002).
51. Arima, K. et al. Immunohistochemical and ultrastructural characterization of ubiquitinated eosinophilic fbrillary neuronal inclusions in sporadic amyotrophic lateral sclerosis Acta Neuropathologica 96, 75-85 (1998).
52. Tada, M. et al. Coexistence of Huntington's disease and amyotrophic lateral sclerosis: a clinicopathological study. Acta Neuropathologica 124, 749-760 (2012).
53. Doi, H., Koyano, S., Susuki, Y., Nukina, N. & Kuroiwa, Y. The RNA-binding protein FUS/TLS is a common aggregate-interacting protein in polyglutamine diseases. Neuroscience Research 66, 131-133 (2010).
54. Johnson, B. S. et al. TDP-43 is intrinsically aggregation-prone, and amyotrophic lateral sclerosis-linked mutations accelerate aggregation and increase toxicity. Journal of Biological Chemistry 284, 20329-20339 (2009).
55. Kim, H. J. et al. Analysis of hnRNPA1, A2/B1, and A3 genes in patients with amyotrophic lateral sclerosis. Nature 495, 467-473 (2013).
56. Wang, Q., Johnson, J. L., Agar, N. Y. R. & Agar, J. N. Protein aggregation and protein instability govern familial amyotrophic lateral sclerosis patient survival. PLoS Biology 6, 1508-1526 (2008).
57. Johnson, B. S., McCafery, J. M., Lindquist, S. & Gitler, A. D. A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proc Natl Acad Sci USA 105, 6439-6444 (2008).
58. Halliday, G. et al. Mechanisms of disease in frontotemporal lobar degeneration: gain of function versus loss of function effects. Acta Neuropathol 124, 373-382 (2012).
59. Schwartz, J. C. et al. FUS is sequestered in nuclear aggregates in ALS patient fbroblasts. Mol Biol Cell 25, 2571-2578 (2014).
60. Tsuiji, H. et al. Spliceosome integrity is deffective in the motor neuron diseases ALS and SMA. EMBO molecular medicine 5, 221-234 (2013).
61. Kabashi, E. et al. FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic lateral sclerosis. PLoS genetics 7, e1002214 (2011).
62. Kopito, R. Aggresomes, inclusion bodies and protein aggregation. Trends in Cell Biology 10, 524-530 (2000).
63. Szeto, J. et al. ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2, 189-199 (2006).
64. Kamhi-Nesher, S. et al. A Novel Quality Control Compartment Derived from the Endoplasmic Reticulum. Molecular Biology of the Cell 12, 1711-1723 (2001).
65. Turner, B. J. et al. Impaired extracellular secretion of mutant superoxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis. J Neurosci 25, 108-117 (2005).
66. Bergink, S. et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes and Development 20, 1343-1352 (2006).
67. Kimura, S., Noda, T. & Yoshimori, T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fuorescent-tagged LC3. Autophagy 3, 452-460 (2007).
68. Ramdzan, Y. M. et al. Conformation sensors that distinguish monomeric proteins from oligomers in live cells. Chemistry & biology 17, 371-379 (2010).
69. Cashman, N. R. et al. Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev Dyn 194, 209-221, doi: 10.1002/aja.1001940306 (1992).
70. Wanker, E. E. et al. Membrane flter assay for detection of amyloid-like polyglutamine-containing protein aggregates. Methods in Enzymology 309, 375-386 (1999).