RNA quality control and protein aggregates in amyotrophic lateral sclerosis: A review

Muscle and Nerve

Volumn 47, Issue 3, 2013, Pages 330-338

  Verma, Ashok ^a   Tandan, Rup ^b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

ALS; FUS TLS; Protein aggregates; RNA metabolism; TDP 43

Indexed keywords

CELL NUCLEUS DNA; FUSED IN SARCOMA PROTEIN; MICRORNA; RNA; SURVIVAL MOTOR NEURON PROTEIN; TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; CELL INCLUSION; CELLULAR DISTRIBUTION; CHROMOSOME TRANSLOCATION; CYTOSOL; DENDRITIC SPINE; EUCHROMATIN; EXON; GENE MUTATION; HUMAN; IMMUNOPRECIPITATION; MOLECULAR PATHOLOGY; MOTONEURON; NERVE CELL PLASTICITY; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN RNA BINDING; QUALITY CONTROL; REVIEW; RNA METABOLISM; RNA PROCESSING; RNA SPLICING; RNA TRANSCRIPTION; SPINAL MUSCULAR ATROPHY; SPLICEOSOME; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CYTOSOL; DISEASE PROGRESSION; HUMANS; MICRORNAS; MUSCLE PROTEINS; MUTATION; QUALITY CONTROL; RNA; RNA SPLICING; RNA-BINDING PROTEIN FUS; TDP-43 PROTEINOPATHIES; TRANSCRIPTION, GENETIC;

EID: 84874284405     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.23673     Document Type: Review

References (76)

1. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993;362:59-62.
2. Chen YZ, Bennett CL, Huynh HM, Blair IP, Puls I, Irobi J, et al. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am J Hum Genet 2004;74:1128-1135.
3. Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, et al. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat Genet 2006;38:411-413.
4. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008;319:1668-1672.
5. Maruyama H, Morino H, Ito H, Izumi Y, Kato H, Watanabe Y, et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 2010;465:223-226.
6. Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009;323:1205-1208.
7. Deng HX, Chen W, Hong ST, Boycott KM, Gorrie GH, Siddique N, et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011;477:211-215.
8. Johnson JO, Mandrioli J, Benatar M, Abramzon Y, Van Deerlin VM, Trojanowski JQ, et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010;68:857-864. Erratum in: Neuron 2011;69:397.
9. Renton AE, Majounie E, Waite A, Simon-Sanchez J, Rollinson S, Gibbs JR, et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011;72:257-268.
10. Malpas K. Motor neuron disease: functional screening identifies novel candidate risk genes in amyotrophic lateral sclerosis. Nat Rev Neurol 2011;8:1.
11. Couthouis J, Hart MP, Shorter J, DeJesus-Hernandez M, Erion R, Oristano R, et al. A yeast functional screen predicts new candidate ALS disease genes. Proc Natl Acad Sci U S A 2011;108:20881-20890.
12. Fecto F, Yan J, Vemula SP, Liu E, Yang Y, Chen W, et al. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch Neurol 2011;68:1440-1446.
13. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006;312:1389-1392.
14. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 2008;11:251-253.
15. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006;314:130-133.
16. Da Cruz S, Cleveland DW. Understanding the role of TDP-43 and FUS/TLS in ALS and beyond. Curr Opin Neurobiol 2011;21:904-919.
17. Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, VandeVelde C, et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 2008;40:572-574.
18. Mackenzie IR, Rademakers R, Neumann M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol 2010;9:995-1007.
19. Lanson NA Jr, Pandey UB. FUS-related proteinopathies: lessons from animal models. Brain Res 2012;1462:44-60.
20. Lefebvre S, Burglen L, Reboullet S, Clermont O, Burlet P, Viollet L, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995;80:155-165.
21. Ticozzi N, Tiloca C, Morelli C, Colombrita C, Poletti B, Doretti A, et al. Genetics of familial Amyotrophic lateral sclerosis. Arch Ital Biol 2011;149:65-82.
22. Verma A. RNA processing errors in amyotrophic lateral sclerosis. Ann Ind Aca Neurol 2011;14:231-236.
23. Kumari D, Biacsi RE, Usdin K. Repeat expansion affects both transcription initiation and elongation in friedreich ataxia cells. J Biol Chem 2011;286:4209-4215.
24. Lee JE, Cooper TA. Pathogenic mechanisms of myotonic dystrophy. Biochem Soc Trans 2009;37:1281-1286.
25. Lagier-Tourenne C, Polymenidou M, Cleveland DW. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 2010;19:46-64.
26. Thorpe JR, Tang H, Atherton J, Cairns NJ. Fine structural analysis of the neuronal inclusions of frontotemporal lobar degeneration with TDP-43 proteinopathy. J Neural Transm 2008;115:1661-1671.
27. Van Deerlin VM, Leverenz JB, Bekris LM, Bird TD, Yuan W, Elman LB, et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol 2008;7:409-416.
28. Giordana MT, Piccinini M, Grifoni S, De Marco G, Vercellino M, Magistrello M, et al. TDP-43 redistribution is an early event in sporadic amyotrophic lateral sclerosis. Brain Pathol 2010;20:351-360.
29. Huang EJ, Zhang J, Geser F, Trojanowski JQ, Strober JB, Dickson DW, et al. Extensive FUS-immunoreactive pathology in juvenile amyotrophic lateral sclerosis with basophilic inclusions. Brain Pathol 2010;20:1069-1076.
30. Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009;323:1208-1211.
31. Corrado L, Del Bo R, Castellotti B, Ratti A, Cereda C, Penco S, et al. Mutations of FUS gene in sporadic amyotrophic lateral sclerosis. J Med Genet 2010;47:190-194.
32. van Blitterswijk M, Landers JE. RNA processing pathways in amyotrophic lateral sclerosis. Neurogenetics 2010;11:275-290.
33. Tateishi T, Hokonohara T, Yamasaki R, Miura S, Kikuchi H, Iwaki A, et al. Multiple system degeneration with basophilic inclusions in Japanese ALS patients with FUS mutation. Acta Neuropathol 2010;119:355-364.
34. Ou SH, Wu F, Harrich D, Garcia-Martinez LF, Gaynor RB. Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J Virol 1995;69:3584-3596.
35. Ayala YM, Zago P, D'Ambrogio A, Xu YF, Petrucelli L, Buratti E, et al. Structural determinants of the cellular localization and shuttling of TDP-43. J Cell Sci 2008;121:3778-3785.
36. Morohoshi F, Ootsuka Y, Arai K, Ichikawa H, Mitani S, Munakata N, et al. Genomic structure of the human RBP56/hTAFII68 and FUS/TLS genes. Gene 1998;221:191-198.
37. Law WJ, Cann KL, Hicks GG. TLS, EWS and TAF15: a model for transcriptional integration of gene expression. Brief Funct Genomic Proteomic 2006;5:8-14.
38. Powers CA, Mathur M, Raaka BM, Ron D, Samuels HH. TLS (translocated-in-liposarcoma) is a high-affinity interactor for steroid, thyroid hormone, and retinoid receptors. Mol Endocrinol 1998;12:4-18.
39. Buratti E, Baralle FE. 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 2001;276:36337-36343.
40. D'Ambrogio A, Buratti E, Stuani C, Guarnaccia C, Romano M, Ayala YM, et al. Functional mapping of the interaction between TDP-43 and hnRNP A2 in vivo. Nucleic Acids Res 2009;37:4116-4126.
41. Bose JK, Wang IF, Hung L, Tarn WY, Shen CK. TDP-43 overexpression enhances exon 7 inclusion during the survival of motor neuron pre-mRNA splicing. J Biol Chem 2008;283:28852-28859.
42. Fujii R, Okabe S, Urushido T, Inoue K, Yoshimura A, Tachibana T, et al. The RNA binding protein TLS is translocated to dendritic spines by mGluR5 activation and regulates spine morphology Curr Biol 2005;15:587-593.
43. Feiguin F, Godena VK, Romano G, D'Ambrogio A, Klima R, Baralle FE. Depletion of TDP-43 affects Drosophila motoneurons terminal synapsis and locomotive behavior. FEBS Lett 2009;583:1586-1592.
44. Kawahara Y, Mieda-Sato A. TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc Natl Acad Sci U S A 2012;109:3347-3352.
45. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, Liang TY, et al. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 2011;14:459-468.
46. Tollervey JR, Curk T, Rogelj B, Briese M, Cereda M, Kayikci M, et al. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 2011;14:452-458.
47. Sephton CF, Cenik C, Kucukural A, Dammer EB, Cenik B, Han Y, et al. Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J Biol Chem 2011;286:1204-1215.
48. Xiao S, Sanelli T, Dib S, Sheps D, Findlater J, Bilbao J, et al. RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol Cell Neurosci 2011;47:167-171.
49. Elden AC, Kim HJ, Hart MP, Chen-Plotkin AS, Johnson BS, Fang X, et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 2010;466:1069-1075.
50. Kim SH, Shanware NP, Bowler MJ, Tibbetts RS. Amyotrophic lateral sclerosis-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to co-regulate HDAC6 mRNA. J Biol Chem 2010;285:34097-34105.
51. Strong MJ, Volkening K, Hammond R, Yang W, Strong W, Leystra-Lantz C, et al. TDP43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Mol Cell Neurosci 2007;35:320-327.
52. Fujii R, Takumi T. TLS facilitates transport of mRNA encoding an actin-stabilizing protein to dendritic spines. J Cell Sci 2005;118:5755-5765.
53. Hoell JI, Larsson E, Runge S, Nusbaum JD, Duggimpudi S, Farazi TA, et al. RNA targets of wild-type and mutant FET family proteins. Nat Struct Mol Biol 2011;18:1428-1431.
54. Bosco DA, Lemay N, Ko HK, Zhou H, Burke C, Kwiatkowski TJ Jr, et al. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum Mol Genet 2010;19:4160-4175.
55. Polymenidou M, Cleveland DW. The seeds of neurodegeneration: prion-like spreading in ALS. Cell 2011;147:498-508.
56. Fecto F, Siddique T. UBQLN2/P62 cellular recycling pathways in amyotrophic lateral sclerosis and frontotemporal dementia. Muscle Nerve 2012;45:157-162.
57. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, et al. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 2007;10:615-622.
58. Chia R, Tattum MH, Jones S, Collinge J, Fisher EM, Jackson GS. Superoxide dismutase 1 and tgSOD1 mouse spinal cord seed fibrils, suggesting a propagative cell death mechanism in amyotrophic lateral sclerosis. PLoS One 2010;5:e10627.
59. Haidet-Phillips AM, Hester ME, Miranda CJ, Meyer K, Braun L, Frakes A, et al. Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol 2011;29:824-828.
60. Fuentealba RA, Udan M, Bell S, Wegorzewska I, Shao J, Diamond MI, et al. Interaction with polyglutamine aggregates reveals a Q/N-rich domain in TDP-43. J Biol Chem 2010;285:26304-26314.
61. Cushman M, Johnson BS, King OD, Gitler AD, Shorter J. Prion-like disorders: blurring the divide between transmissibility and infectivity. J Cell Sci 2010;123:1191-1201.
62. Furukawa Y, Kaneko K, Watanabe S, Yamanaka K, Nukina N. A seeding reaction recapitulates intracellular formation of Sarkosyl-insoluble transactivation response element (TAR) DNA-binding protein-43 inclusions. J Biol Chem 2011;286:18664-18672.
63. Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, Hruscha A, et al. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. EMBO J 2010;29:2841-2857.
64. Alberti S, Halfmann R, King O, Kapila A, Lindquist S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 2009;137:146-158.
65. Dormann D, Haass C. TDP-43 and FUS: a nuclear affair. Trends Neurosci 2011;34:339-348.
66. Huang C, Zhou H, Tong J, Chen H, Liu YJ, Wang D, et al. FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS Genet 2011;7:e1002011.
67. Fiesel FC, Voigt A, Weber SS, Van den Haute C, Waldenmaier A, Gorner K, et al. Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J 2010;29:209-321.
68. Li Y, Ray P, Rao EJ, Shi C, Guo W, Chen X, et al. A Drosophila model for TDP-43 proteinopathy. Proc Natl Acad Sci U S A 2010;107:3169-3174.
69. Kabashi E, Lin L, Tradewell ML, Dion PA, Bercier V, Bourgouin P, et al. Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum Mol Genet 2010;19:671-683.
70. Kraemer BC, Schuck T, Wheeler JM, Robinson LC, Trojanowski JQ, Lee VM, et al. Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathol 2010;119:409-419.
71. Ash PE, Zhang YJ, Roberts CM, Saldi T, Hutter H, Buratti E, et al. Neurotoxic effects of TDP-43 overexpression in C. elegans. Hum Mol Genet 2010;19:3206-3218.
72. Wils H, Kleinberger G, Janssens J, Pereson S, Joris G, Cuijt I, et al. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A 2010;107:3858-3863.
73. Dennis JS, Citron BA. Wobbler mice modeling motor neuron disease display elevated transactive response DNA binding protein. Neuroscience 2009;158:745-750.
74. Stallings NR, Puttaparthi K, Luther CM, Burns DK, Elliott JL. Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol Dis 2010;40:404-414.
75. Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A 2009;106:18809-18814.
76. Zhou H, Huang C, Chen H, Wang D, Landel CP, Xia PY, et al. Transgenic rat model of neurodegeneration caused by mutation in the TDP gene. PLoS Genet 2010;6:e1000887.