TDP-43 high throughput screening analyses in neurodegeneration: Advantages and pitfalls

Molecular and Cellular Neuroscience

Volumn 56, Issue , 2013, Pages 465-474

  Buratti, Emanuele ^a   Romano, Maurizio ^b   Baralle, Francisco E ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MICRORNA; TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BINDING SITE; CELL SURVIVAL; DEGENERATIVE DISEASE; DNA SEQUENCE; FRONTOTEMPORAL DEMENTIA; GENE EXPRESSION; GENE TARGETING; HIGH THROUGHPUT SCREENING; HUMAN; HYPOTHESIS; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA METABOLISM; RNA PROCESSING; RNA SEQUENCE;

DNA-BINDING PROTEINS; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; SENSITIVITY AND SPECIFICITY; TDP-43 PROTEINOPATHIES;

EID: 84884820769     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.03.001     Document Type: Article

References (96)

1. Agarwal A., Koppstein D., Rozowsky J., Sboner A., Habegger L., Hillier L.W., Sasidharan R., Reinke V., Waterston R.H., Gerstein M. Comparison and calibration of transcriptome data from RNA-seq and tiling arrays. BMC Genomics 2010, 11:383.
2. Al-Chalabi A., Jones A., Troakes C., King A., Al-Sarraj S., van den Berg L.H. The genetics and neuropathology of amyotrophic lateral sclerosis. Acta Neuropathol. 2012, 124:339-352.
3. Arai T., Hasegawa M., Akiyama H., Ikeda K., Nonaka T., Mori H., Mann D., Tsuchiya K., Yoshida M., Hashizume Y., Oda T. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 2006, 351:602-611.
4. Ayala Y.M., Pantano S., D'Ambrogio A., Buratti E., Brindisi A., Marchetti C., Romano M., Baralle F.E. Human, Drosophila, and C. elegans TDP43: nucleic acid binding properties and splicing regulatory function. J. Mol. Biol. 2005, 348:575-588.
5. Ayala Y.M., Misteli T., Baralle F.E. TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3785-3789.
6. Baciu C., Thompson K.J., Mougeot J.L., Brooks B.R., Weller J.W. The LO-BaFL method and ALS microarray expression analysis. BMC Bioinforma. 2012, 13:244.
7. Bose J.K., Huang C.C., Shen C.K. Regulation of autophagy by neuropathological protein TDP-43. J. Biol. Chem. 2011, 286:44441-44448.
8. Budini M., Baralle F.E., Buratti E. Regulation of gene expression by TDP-43 and FUS/TLS in frontotemporal lobar degeneration. Curr. Alzheimer Res. 2011, 8:237-245.
9. Buratti E., Baralle F.E. 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.
10. Buratti E., Baralle F.E. The multiple roles of TDP-43 in pre-mRNA processing and gene expression regulation. RNA Biol. 2010, 7:420-429.
11. Buratti E., Baralle F.E. TDP-43: gumming up neurons through protein-protein and protein-RNA interactions. Trends Biochem. Sci. 2012, 37:237-247.
12. Buratti E., Dork T., Zuccato E., Pagani F., Romano M., Baralle F.E. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 2001, 20:1774-1784.
13. Buratti E., De Conti L., Stuani C., Romano M., Baralle M., Baralle F. Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 2010, 277:2268-2281.
14. Caputi M., Zahler A.M. Determination of the RNA binding specificity of the heterogeneous nuclear ribonucleoprotein (hnRNP) H/H'/F/2H9 family. J. Biol. Chem. 2001, 276:43850-43859.
15. Casafont I., Bengoechea R., Tapia O., Berciano M.T., Lafarga M. TDP-43 localizes in mRNA transcription and processing sites in mammalian neurons. J. Struct. Biol. 2009, 167:235-241.
16. Chen-Plotkin A.S., Geser F., Plotkin J.B., Clark C.M., Kwong L.K., Yuan W., Grossman M., Van Deerlin V.M., Trojanowski J.Q., Lee V.M. Variations in the progranulin gene affect global gene expression in frontotemporal lobar degeneration. Hum. Mol. Genet. 2008, 17:1349-1362.
17. Chiang P.M., Ling J., Jeong Y.H., Price D.L., Aja S.M., Wong P.C. Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16320-16324.
18. Colombrita C., Onesto E., Megiorni F., Pizzuti A., Baralle F.E., Buratti E., Silani V., Ratti A. TDP-43 and FUS RNA-binding proteins bind distinct sets of cytoplasmic messenger RNAs and differently regulate their post-transcriptional fate in motoneuron-like cells. J. Biol. Chem. 2012, 287:15635-15647.
19. Cooper-Knock J., Kirby J., Ferraiuolo L., Heath P.R., Rattray M., Shaw P.J. Gene expression profiling in human neurodegenerative disease. Nat. Rev. Neurol. 2012, 8:518-530.
20. Cuppens H., Lin W., Jaspers M., Costes B., Teng H., Vankeerberghen A., Jorissen M., Droogmans G., Reynaert I., Goossens M., Nilius B., Cassiman J.J. Polyvariant mutant cystic fibrosis transmembrane conductance regulator genes. The polymorphic (Tg)m locus explains the partial penetrance of the T5 polymorphism as a disease mutation. J. Clin. Invest. 1998, 101:487-496.
21. Dalma-Weiszhausz D.D., Warrington J., Tanimoto E.Y., Miyada C.G. The Affymetrix GeneChip platform: an overview. Methods Enzymol. 2006, 410:3-28.
22. Dormann D., Haass C. TDP-43 and FUS: a nuclear affair. Trends Neurosci. 2011.
23. Dreyfuss G., Matunis M.J., Pinol-Roma S., Burd C.G. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 1993, 62:289-321.
24. Dunbar S.A. Applications of Luminex xMAP technology for rapid, high-throughput multiplexed nucleic acid detection. Clin. Chim. Acta 2006, 363:71-82.
25. Egawa N., Kitaoka S., Tsukita K., Naitoh M., Takahashi K., Yamamoto T., Adachi F., Kondo T., Okita K., Asaka I., Aoi T., Watanabe A., Yamada Y., Morizane A., Takahashi J., Ayaki T., Ito H., Yoshikawa K., Yamawaki S., Suzuki S., Watanabe D., Hioki H., Kaneko T., Makioka K., Okamoto K., Takuma H., Tamaoka A., Hasegawa K., Nonaka T., Hasegawa M., Kawata A., Yoshida M., Nakahata T., Takahashi R., Marchetto M.C., Gage F.H., Yamanaka S., Inoue H. Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci. Transl. Med. 2012, 4:145ra104.
26. Fan J.B., Gunderson K.L., Bibikova M., Yeakley J.M., Chen J., Wickham Garcia E., Lebruska L.L., Laurent M., Shen R., Barker D. Illumina universal bead arrays. Methods Enzymol. 2006, 410:57-73.
27. Feiguin F., Godena V.K., Romano G., D'Ambrogio A., Klima R., Baralle F.E. Depletion of TDP-43 affects Drosophila motoneurons terminal synapsis and locomotive behavior. FEBS Lett. 2009, 583:1586-1592.
28. Fiesel F.C., Voigt A., Weber S.S., Van den Haute C., Waldenmaier A., Gorner K., Walter M., Anderson M.L., Kern J.V., Rasse T.M., Schmidt T., Springer W., Kirchner R., Bonin M., Neumann M., Baekelandt V., Alunni-Fabbroni M., Schulz J.B., Kahle P.J. Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J. 2010, 29:209-221.
29. Fiesel F.C., Weber S.S., Supper J., Zell A., Kahle P.J. TDP-43 regulates global translational yield by splicing of exon junction complex component SKAR. Nucleic Acids Res. 2012, 40:2668-2682.
30. Fukuda T., Yamagata K., Fujiyama S., Matsumoto T., Koshida I., Yoshimura K., Mihara M., Naitou M., Endoh H., Nakamura T., Akimoto C., Yamamoto Y., Katagiri T., Foulds C., Takezawa S., Kitagawa H., Takeyama K., O'Malley B.W., Kato S. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat. Cell Biol. 2007, 9:604-611.
31. Gagliardi S., Milani P., Sardone V., Pansarasa O., Cereda C. From transcriptome to noncoding rnas: implications in ALS mechanism. Neurol. Res. Int. 2012, 2012:278725.
32. Gitler A.D. TDP-43 and FUS/TLS yield a target-rich haul in ALS. Nat. Neurosci. 2012, 15:1467-1469.
33. Grabowski P. Alternative splicing takes shape during neuronal development. Curr. Opin. Genet. Dev. 2011, 21:388-394.
34. Gregory R.I., Yan K.P., Amuthan G., Chendrimada T., Doratotaj B., Cooch N., Shiekhattar R. The microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
35. Grellscheid S., Dalgliesh C., Storbeck M., Best A., Liu Y., Jakubik M., Mende Y., Ehrmann I., Curk T., Rossbach K., Bourgeois C.F., Stevenin J., Grellscheid D., Jackson M.S., Wirth B., Elliott D.J. Identification of evolutionarily conserved exons as regulated targets for the splicing activator tra2beta in development. PLoS Genet. 2011, 7:e1002390.
36. Groman J.D., Hefferon T.W., Casals T., Bassas L., Estivill X., Des Georges M., Guittard C., Koudova M., Fallin M.D., Nemeth K., Fekete G., Kadasi L., Friedman K., Schwarz M., Bombieri C., Pignatti P.F., Kanavakis E., Tzetis M., Schwartz M., Novelli G., D'Apice M.R., Sobczynska-Tomaszewska A., Bal J., Stuhrmann M., Macek M., Claustres M., Cutting G.R. Variation in a repeat sequence determines whether a common variant of the cystic fibrosis transmembrane conductance regulator gene is pathogenic or benign. Am. J. Hum. Genet. 2004, 74:176-179.
37. Guil S., Caceres J.F. The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat. Struct. Mol. Biol. 2007, 14:591-596.
38. Hallegger M., Llorian M., Smith C.W. Alternative splicing: global insights. FEBS J. 2010, 277:856-866.
39. Halliday G., Bigio E.H., Cairns N.J., Neumann M., Mackenzie I.R., Mann D.M. Mechanisms of disease in frontotemporal lobar degeneration: gain of function versus loss of function effects. Acta Neuropathol. 2012, 124:373-382.
40. Hanson K.A., Kim S.H., Tibbetts R.S. RNA-binding proteins in neurodegenerative disease: TDP-43 and beyond. Wiley Interdiscip. Rev. RNA 2012, 3:265-285.
41. Hart M.P., Gitler A.D. ALS-associated ataxin 2 polyQ expansions enhance stress-induced caspase 3 activation and increase TDP-43 pathological modifications. J. Neurosci. 2012, 32:9133-9142.
42. Hazelett D.J., Chang J.C., Lakeland D.L., Morton D.B. Comparison of parallel high-throughput RNA sequencing between knockout of TDP-43 and its overexpression reveals primarily nonreciprocal and nonoverlapping gene expression changes in the central nervous system of Drosophila. G3 (Bethesda) 2012, 2:789-802.
43. Hoell J.I., Larsson E., Runge S., Nusbaum J.D., Duggimpudi S., Farazi T.A., Hafner M., Borkhardt A., Sander C., Tuschl T. RNA targets of wild-type and mutant FET family proteins. Nat. Struct. Mol. Biol. 2011, 18:1428-1431.
44. Huelga S.C., Vu A.Q., Arnold J.D., Liang T.Y., Liu P.P., Yan B.Y., Donohue J.P., Shiue L., Hoon S., Brenner S., Ares M., Yeo G.W. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep. 2012, 1:167-178.
45. Igaz L.M., Kwong L.K., Lee E.B., Chen-Plotkin A., Swanson E., Unger T., Malunda J., Xu Y., Winton M.J., Trojanowski J.Q., Lee V.M. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest. 2011, 121:726-738.
46. Kabashi E., Lin L., Tradewell M.L., Dion P.A., Bercier V., Bourgouin P., Rochefort D., Bel Hadj S., Durham H.D., Velde C.V., Rouleau G.A., Drapeau P. 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.
47. Kaida D., Berg M.G., Younis I., Kasim M., Singh L.N., Wan L., Dreyfuss G. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 2010, 468:664-668.
48. 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.
49. King O.D., Gitler A.D., Shorter J. The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res. 2012, 1462:61-80.
50. Kocerha J., Kouri N., Baker M., Finch N., DeJesus-Hernandez M., Gonzalez J., Chidamparam K., Josephs K.A., Boeve B.F., Graff-Radford N.R., Crook J., Dickson D.W., Rademakers R. Altered microRNA expression in frontotemporal lobar degeneration with TDP-43 pathology caused by progranulin mutations. BMC Genomics 2011, 12:527.
51. Kraemer B.C., Schuck T., Wheeler J.M., Robinson L.C., Trojanowski J.Q., Lee V.M., Schellenberg G.D. Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathol. 2010, 119:409-419.
52. Lagier-Tourenne C., Polymenidou M., Hutt K.R., Vu A.Q., Baughn M., Huelga S.C., Clutario K.M., Ling S.C., Liang T.Y., Mazur C., Wancewicz E., Kim A.S., Watt A., Freier S., Hicks G.G., Donohue J.P., Shiue L., Bennett C.F., Ravits J., Cleveland D.W., Yeo G.W. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci. 2012, 15:1488-1497.
53. Larriba S., Bassas L., Gimenez J., Ramos M.D., Segura A., Nunes V., Estivill X., Casals T. Testicular CFTR splice variants in patients with congenital absence of the vas deferens. Hum. Mol. Genet. 1998, 7:1739-1743.
54. Lee E.B., Lee V.M., Trojanowski J.Q. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat. Rev. Neurosci. 2012, 13:38-50.
55. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., Chi S.W., Clark T.A., Schweitzer A.C., Blume J.E., Wang X., Darnell J.C., Darnell R.B. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
56. Luty A.A., Kwok J.B., Dobson-Stone C., Loy C.T., Coupland K.G., Karlstrom H., Sobow T., Tchorzewska J., Maruszak A., Barcikowska M., Panegyres P.K., Zekanowski C., Brooks W.S., Williams K.L., Blair I.P., Mather K.A., Sachdev P.S., Halliday G.M., Schofield P.R. Sigma nonopioid intracellular receptor 1 mutations cause frontotemporal lobar degeneration-motor neuron disease. Ann. Neurol. 2010, 68:639-649.
57. Malone J.H., Oliver B. Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol. 2011, 9:34.
58. Mattick J.S. The central role of RNA in human development and cognition. FEBS Lett. 2011, 585:1600-1616.
59. Mercado P.A., Ayala Y.M., Romano M., Buratti E., Baralle F.E. Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res. 2005, 33:6000-6010.
60. Mills J.D., Janitz M. Alternative splicing of mRNA in the molecular pathology of neurodegenerative diseases. Neurobiol. Aging 2012, 33(1012):e1011-e1024.
61. Mishra M., Paunesku T., Woloschak G.E., Siddique T., Zhu L.J., Lin S., Greco K., Bigio E.H. Gene expression analysis of frontotemporal lobar degeneration of the motor neuron disease type with ubiquitinated inclusions. Acta Neuropathol. 2007, 114:81-94.
62. Narayanan, R.K., Mangelsdorf, M., Panwar, A., Butler, T.J., Noakes, P.G., Wallace, R.H., in press. Identification of RNA bound to the TDP-43 ribonucleoprotein complex in the adult mouse brain. Amyotroph. Lateral Scler.
63. 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. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
64. Niksic M., Romano M., Buratti E., Pagani F., Baralle F.E. Functional analysis of cis-acting elements regulating the alternative splicing of human CFTR exon 9. Hum. Mol. Genet. 1999, 8:2339-2349.
65. Norris A.D., Calarco J.A. Emerging roles of alternative pre-mRNA splicing regulation in neuronal development and function. Front. Neurosci. 2012, 6:122.
66. Palmieri N., Nolte V., Suvorov A., Kosiol C., Schlotterer C. Evaluation of different reference based annotation strategies using RNA-seq-a case study in Drososphila pseudoobscura. PLoS One 2012, 7:e46415.
67. Passoni M., De Conti L., Baralle M., Buratti E. UG repeats/TDP-43 interactions near 5' splice sites exert unpredictable effects on splicing modulation. J. Mol. Biol. 2012, 415:46-60.
68. Polymenidou M., Lagier-Tourenne C., Hutt K.R., Huelga S.C., Moran J., Liang T.Y., Ling S.C., Sun E., Wancewicz E., Mazur C., Kordasiewicz H., Sedaghat Y., Donohue J.P., Shiue L., Bennett C.F., Yeo G.W., Cleveland D.W. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci. 2011, 14:459-468.
69. Polymenidou M., Lagier-Tourenne C., Hutt K.R., Bennett C.F., Cleveland D.W., Yeo G.W. Misregulated RNA processing in amyotrophic lateral sclerosis. Brain Res. 2012, 1462:3-15.
70. Potthast T. Paradigm shifts versus fashion shifts? Systems and synthetic biology as new epistemic entities in understanding and making 'life'. EMBO Rep. 2009, 10(Suppl. 1):S42-S45.
71. Prudencio M., Jansen-West K.R., Lee W.C., Gendron T.F., Zhang Y.-J., Xu Y.-F., Gass J., Stuani C., Stetler C., Rademakers R., Dickson D.W., Buratti E., Petrucelli L. Misregulation of human sortilin splicing leads to the generation of a non-functional progranulin receptor. PNAS 2012, 109:21510-21515.
72. Rabin S.J., Kim J.M., Baughn M., Libby R.T., Kim Y.J., Fan Y., Libby R.T., La Spada A., Stone B., Ravits J. Sporadic ALS has compartment-specific aberrant exon splicing and altered cell-matrix adhesion biology. Hum. Mol. Genet. 2010, 19:313-328.
73. Rademakers R., Neumann M., Mackenzie I.R. Advances in understanding the molecular basis of frontotemporal dementia. Nat. Rev. Neurol. 2012, 8:423-434.
74. Renoux A.J., Todd P.K. Neurodegeneration the RNA way. Prog. Neurobiol. 2012, 97:173-189.
75. Sanchez-Pla A., Reverter F., Ruiz de Villa M.C., Comabella M. Transcriptomics: mRNA and alternative splicing. J. Neuroimmunol. 2012, 248:23-31.
76. Sanford J.R., Coutinho P., Hackett J.A., Wang X., Ranahan W., Caceres J.F. Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLoS One 2008, 3:e3369.
77. Schena M., Shalon D., Davis R.W., Brown P.O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 1995, 270:467-470.
78. Schlitt T., Kemmeren P. From microarray data to results. Workshop on genomic approaches to microarray data analysis. EMBO Rep. 2004, 5:459-463.
79. Sephton C.F., Good S.K., Atkin S., Dewey C.M., Mayer P., Herz J., Yu G. TDP-43 is a developmentally regulated protein essential for early embryonic development. J. Biol. Chem. 2010, 285:6826-6834.
80. Sephton C.F., Cenik C., Kucukural A., Dammer E.B., Cenik B., Han Y., Dewey C.M., Roth F.P., Herz J., Peng J., Moore M.J., Yu G. Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J. Biol. Chem. 2011, 286:1204-1215.
81. Sephton C.F., Cenik B., Cenik B.K., Herz J., Yu G. TDP-43 in central nervous system development and function: clues to TDP-43-associated neurodegeneration. Biol. Chem. 2012, 393:589-594.
82. Sieben A., Van Langenhove T., Engelborghs S., Martin J.J., Boon P., Cras P., De Deyn P.P., Santens P., Van Broeckhoven C., Cruts M. The genetics and neuropathology of frontotemporal lobar degeneration. Acta Neuropathol. 2012, 124:353-372.
83. Tarazona S., Garcia-Alcalde F., Dopazo J., Ferrer A., Conesa A. Differential expression in RNA-seq: a matter of depth. Genome Res. 2011, 21:2213-2223.
84. Tollervey J.R., Curk T., Rogelj B., Briese M., Cereda M., Kayikci M., Konig J., Hortobagyi T., Nishimura A.L., Zupunski V., Patani R., Chandran S., Rot G., Zupan B., Shaw C.E., Ule J. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 2011, 14:452-458.
85. Tollervey J.R., Wang Z., Hortobagyi T., Witten J.T., Zarnack K., Kayikci M., Clark T.A., Schweitzer A.C., Rot G., Curk T., Zupan B., Rogelj B., Shaw C.E., Ule J. Analysis of alternative splicing associated with aging and neurodegeneration in the human brain. Genome Res. 2011, 21:1572-1582.
86. Ugras S.E., Shorter J. RNA-binding proteins in amyotrophic lateral sclerosis and neurodegeneration. Neurol. Res. Int. 2012, 2012:432780.
87. Ule J., Jensen K.B., Ruggiu M., Mele A., Ule A., Darnell R.B. CLIP identifies Nova-regulated RNA networks in the brain. Science 2003, 302:1212-1215.
88. Ule J., Ule A., Spencer J., Williams A., Hu J.S., Cline M., Wang H., Clark T., Fraser C., Ruggiu M., Zeeberg B.R., Kane D., Weinstein J.N., Blume J., Darnell R.B. Nova regulates brain-specific splicing to shape the synapse. Nat. Genet. 2005, 37:844-852.
89. van Blitterswijk M., van Es M.A., Hennekam E.A., Dooijes D., van Rheenen W., Medic J., Bourque P.R., Schelhaas H.J., van der Kooi A.J., de Visser M., de Bakker P.I., Veldink J.H., van den Berg L.H. Evidence for an oligogenic basis of amyotrophic lateral sclerosis. Hum. Mol. Genet. 2012, 21:3776-3784.
90. Volkening K., Leystra-Lantz C., Yang W., Jaffee H., Strong M.J. Tar DNA binding protein of 43kDa (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 Res. 2009, 1305:168-182.
91. Witten J.T., Ule J. Understanding splicing regulation through RNA splicing maps. Trends Genet. 2011, 27:89-97.
92. Wu L.S., Cheng W.C., Hou S.C., Yan Y.T., Jiang S.T., Shen C.K. TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Genesis 2010, 48:56-62.
93. Xiao S., Sanelli T., Dib S., Sheps D., Findlater J., Bilbao J., Keith J., Zinman L., Rogaeva E., Robertson J. RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol. Cell. Neurosci. 2011, 47:167-180.
94. Xu Z.S. Does a loss of TDP-43 function cause neurodegeneration?. Mol. Neurodegener. 2012, 7:27.
95. Youmans K.L., Wolozin B. TDP-43: a new player on the AD field?. Exp. Neurol. 2012, 237:90-95.
96. Zhang C., Darnell R.B. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat. Biotechnol. 2011, 29:607-614.