High-content RNAi screening identifies the type 1 inositol triphosphate receptor as a modifier of TDP-43 localization and neurotoxicity

Human Molecular Genetics

Volumn 21, Issue 22, 2012, Pages 4845-4856

  Kim, Sang Hwa ^a   Zhan, Lihong ^a   Hanson, Keith A ^a   Tibbetts, Randal S ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; INOSITOL TRISPHOSPHATE; INOSITOL TRISPHOSPHATE RECEPTOR 1; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; AUTOPHAGOSOME; DROSOPHILA; ENDOPLASMIC RETICULUM; G2 PHASE CELL CYCLE CHECKPOINT; GENE INTERACTION; GENE SILENCING; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MOTONEURON; NERVE CELL; NEUROTOXICITY; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; RNA INTERFERENCE; SCREENING;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL LINE; CELL NUCLEUS; CYTOPLASM; DNA-BINDING PROTEINS; DROSOPHILA; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MALE; MUTATION; PHAGOSOMES; PROTEIN TRANSPORT; RNA INTERFERENCE;

EID: 84868088848     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds321     Document Type: Article

References (75)

1. Nelson, L.M. (1995) Epidemiology of ALS. Clin. Neurosci., 3, 327-331.
2. Rosen, D.R. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 364, 362.
3. Cleveland, D.W. and Rothstein, J.D. (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci., 2, 806-819.
4. 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. et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314, 130-133.
5. Buratti, E. and Baralle, F.E. (2008) Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front. Biosci., 13, 867-878.
6. Buratti, E., Dork, T., Zuccato, E., Pagani, F., Romano, M. and Baralle, F.E. (2001) Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J., 20, 1774-1784.
7. Ou, S.H., Wu, F., Harrich, D., Garcia-Martinez, L.F. and Gaynor, R.B. (1995) Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol., 69, 3584-3596.
8. Volkening, K., Leystra-Lantz, C., Yang, W., Jaffee, H. and Strong, M.J. (2009) 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., 1305, 168-182.
9. Gitcho, M.A., Baloh, R.H., Chakraverty, S., Mayo, K., Norton, J.B., Levitch, D., Hatanpaa, K.J., White, C.L. 3rd, Bigio, E.H., Caselli, R. et al. (2008) TDP-43 A315T mutation in familial motor neuron disease. Ann. Neurol., 63, 535-538.
10. Kabashi, E., Valdmanis, P., Dion, P., Spiegelman, D., McConkey, B., Vande Velde, C., Bouchard, J., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet., 40, 572-574.
11. Sreedharan, J., Blair, I.P., Tripathi, V.B., Hu, X., Vance, C., Rogelj, B., Ackerley, S., Durnall, J.C., Williams, K.L., Buratti, E. et al. (2008) TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science, 319, 1668-1672.
12. Yokoseki, A., Shiga, A., Tan, C.F., Tagawa, A., Kaneko, H., Koyama, A., Eguchi, H., Tsujino, A., Ikeuchi, T., Kakita, A. et al. (2008) TDP-43 mutation in familial amyotrophic lateral sclerosis. Ann. Neurol., 63, 538-542.
13. Vance, C., Rogelj, B., Hortobagyi, T., De Vos, K.J., Nishimura, A.L., Sreedharan, J., Hu, X., Smith, B., Ruddy, D., Wright, P. et al. (2009) Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science, 323, 1208-1211.
14. Kwiatkowski, T.J. Jr, Bosco, D.A., Leclerc, A.L., Tamrazian, E., Vanderburg, C.R., Russ, C., Davis, A., Gilchrist, J., Kasarskis, E.J., Munsat, T. et al. (2009) Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science, 323, 1205-1208.
15. Udan, M. and Baloh, R.H. (2011) Implications of the prion-related Q/N domains in TDP-43 and FUS. Prion, 5, 1-5.
16. Neumann, M., Kwong, L.K., Lee, E.B., Kremmer, E., Flatley, A., Xu, Y., Forman, M.S., Troost, D., Kretzschmar, H.A., Trojanowski, J.Q. et al. (2009) Phosphorylation of S409/410 of TDP-43 is a consistent feature in all sporadic and familial forms of TDP-43 proteinopathies. Acta Neuropathol., 117, 137-149.
17. Hasegawa, M., Arai, T., Nonaka, T., Kametani, F., Yoshida, M., Hashizume, Y., Beach, T.G., Buratti, E., Baralle, F., Morita, M. et al. (2008) Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann. Neurol., 64, 60-70.
18. Igaz, L.M., Kwong, L.K., Xu, Y., Truax, A.C., Uryu, K., Neumann, M., Clark, C.M., Elman, L.B., Miller, B.L., Grossman, M. et al. (2008) Enrichment of C-terminal fragments in TAR DNA-binding protein-43 cytoplasmic inclusions in brain but not in spinal cord of frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Am. J. Pathol., 173, 182-194.
19. Dormann, D., Rodde, R., Edbauer, D., Bentmann, E., Fischer, I., Hruscha, A., Than, M.E., Mackenzie, I.R., Capell, A., Schmid, B. et al. (2010) ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. Embo J., 29, 2841-2857.
20. Hanson, K.A., Kim, S.H., Wassarman, D.A. and Tibbetts, R.S. (2010) Ubiquilin modifies TDP-43 toxicity in a Drosophila model of amyotrophic lateral sclerosis (ALS). J. Biol. Chem., 285, 11068-11072.
21. Kabashi, E., Valdmanis, P.N., Dion, P., Spiegelman, D., McConkey, B.J., Vande Velde, C., Bouchard, J.P., Lacomblez, L., Pochigaeva, K., Salachas, F. et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet., 40, 572-574.
22. Wegorzewska, I., Bell, S., Cairns, N.J., Miller, T.M. and Baloh, R.H. (2009) TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl Acad. Sci. USA, 106, 18809-18814.
23. Wils, H., Kleinberger, G., Janssens, J., Pereson, S., Joris, G., Cuijt, I., Smits, V., Ceuterick-de Groote, C., Van Broeckhoven, C. and Kumar-Singh, S. (2010) TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc. Natl Acad. Sci. USA, 107, 3858-3863.
24. Li, Y., Ray, P., Rao, E.J., Shi, C., Guo, W., Chen, X., Woodruff, E.A. III, Fushimi, K. and Wu, J.Y. (2010) A Drosophila model for TDP-43 proteinopathy. Proc. Natl Acad. Sci. USA, 107, 3169-3174.
25. Ash, P.E., Zhang, Y.J., Roberts, C.M., Saldi, T., Hutter, H., Buratti, E., Petrucelli, L. and Link, C.D. (2010) Neurotoxic effects of TDP-43 overexpression in C. elegans. Hum. Mol. Genet., 19, 3206-3218.
26. Xu, Y.F., Gendron, T.F., Zhang, Y.J., Lin, W.L., D'Alton, S., Sheng, H., Casey, M.C., Tong, J., Knight, J., Yu, X. et al. (2010) Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J. Neurosci., 30, 10851-10859.
27. Barmada, S.J., Skibinski, G., Korb, E., Rao, E.J., Wu, J.Y. and Finkbeiner, S. (2010) Cytoplasmic mislocalization of TDP-43 is toxic to neurons and enhanced by a mutation associated with familial amyotrophic lateral sclerosis. J. Neurosci., 30, 639-649.
28. 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. et al. (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci., 14, 459-468.
29. 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. et al. (2011) Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest., 121, 726-738.
30. Ayala, Y.M., De Conti, L., Avendano-Vazquez, S.E., Dhir, A., Romano, M., D'Ambrogio, A., Tollervey, J., Ule, J., Baralle, M., Buratti, E. et al. (2011) TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J., 30, 277-288.
31. Lee, E.B., Lee, V.M. and Trojanowski, J.Q. (2012) Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat. Rev. Neurosci., 13, 38-50.
32. Bosco, D.A., Lemay, N., Ko, H.K., Zhou, H., Burke, C., Kwiatkowski, T.J. Jr, Sapp, P., McKenna-Yasek, D., Brown, R.H. Jr and Hayward, L.J. (2010) Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet., 19, 4160-4175.
33. Liu-Yesucevitz, L., Bilgutay, A., Zhang, Y.J., Vanderwyde, T., Citro, A., Mehta, T., Zaarur, N., McKee, A., Bowser, R., Sherman, M. et al. (2010) Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS ONE, 5, e13250.
34. Colombrita, C., Zennaro, E., Fallini, C., Weber, M., Sommacal, A., Buratti, E., Silani, V. and Ratti, A. (2009) TDP-43 is recruited to stress granules in conditions of oxidative insult. J. Neurochem., 111, 1051-1061.
35. McDonald, K.K., Aulas, A., Destroismaisons, L., Pickles, S., Beleac, E., Camu, W., Rouleau, G.A. and Vande Velde, C. (2011) TAR DNA-binding protein 43 (TDP-43) regulates stress granule dynamics via differential regulation of G3BP and TIA-1. Hum. Mol. Genet., 20, 1400-1410.
36. Sun, Z., Diaz, Z., Fang, X., Hart, M.P., Chesi, A., Shorter, J. and Gitler, A.D. (2011) Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS Biol., 9, e1000614.
37. Kino, Y., Washizu, C., Aquilanti, E., Okuno, M., Kurosawa, M., Yamada, M., Doi, H. and Nukina, N. (2011) Intracellular localization and splicing regulation of FUS/TLS are variably affected by amyotrophic lateral sclerosis-linked mutations. Nucleic Acids Res., 39, 2781-2798.
38. Dewey, C.M., Cenik, B., Sephton, C.F., Dries, D.R., Mayer, P. 3rd, Good, S.K., Johnson, B.A., Herz, J. and Yu, G. (2011) TDP-43 is directed to stress granules by sorbitol, a novel physiological osmotic and oxidative stressor. Mol. Cell Biol., 31, 1098-1108.
39. Hanson, K.A., Kim, S.H. and Tibbetts, R.S. (2012) RNA-binding proteins in neurodegenerative disease: TDP-43 and beyond. Wiley Interdiscip. Rev. RNA, 3, 265-285.
40. Dormann, D. and Haass, C. (2011) TDP-43 and FUS: a nuclear affair. Trends Neurosci., 34, 339-348.
41. D'Angelo, M.A., Raices, M., Panowski, S.H. and Hetzer, M.W. (2009) Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell, 136, 284-295.
42. 2+ transfer to mitochondria. Cell, 142, 270-283.
43. van de Leemput, J., Chandran, J., Knight, M.A., Holtzclaw, L.A., Scholz, S., Cookson, M.R., Houlden, H., Gwinn-Hardy, K., Fung, H.C., Lin, X. et al. (2007) Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet, 3, e108.
44. Iwaki, A., Kawano, Y., Miura, S., Shibata, H., Matsuse, D., Li, W., Furuya, H., Ohyagi, Y., Taniwaki, T., Kira, J. et al. (2008) Heterozygous deletion of ITPR1, but not SUMF1, in spinocerebellar ataxia type 16. J. Med. Genet., 45, 32-35.
45. Hara, K., Shiga, A., Nozaki, H., Mitsui, J., Takahashi, Y., Ishiguro, H., Yomono, H., Kurisaki, H., Goto, J., Ikeuchi, T. et al. (2008) Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families. Neurology, 71, 547-551.
46. Nishimura, A.L., Zupunski, V., Troakes, C., Kathe, C., Fratta, P., Howell, M., Gallo, J.M., Hortobagyi, T., Shaw, C.E. and Rogelj, B. (2010) Nuclear import impairment causes cytoplasmic trans-activation response DNA-binding protein accumulation and is associated with frontotemporal lobar degeneration. Brain, 133, 1763-1771.
47. 2+ release channels. Physiol. Rev., 87, 593-658.
48. Ling, S.C., Albuquerque, C.P., Han, J.S., Lagier-Tourenne, C., Tokunaga, S., Zhou, H. and Cleveland, D.W. (2010) ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/ TLS. Proc. Natl Acad. Sci. USA, 107, 13318-13323.
49. Pan, L., Wu, X., Zhao, D., Hessari, N.M., Lee, I., Zhang, X. and Xu, J. (2011) Sulfhydryl modification induces calcium entry through IP-sensitive store-operated pathway in activation-dependent human neutrophils. PLoS ONE, 6, e25262.
50. Kim, S.H., Shi, Y., Hanson, K.A., Williams, L.M., Sakasai, R., Bowler, M.J. and Tibbetts, R.S. (2009) Potentiation of amyotrophic lateral sclerosis (ALS)-associated TDP-43 aggregation by the proteasome-targeting factor, ubiquilin 1. J. Biol. Chem., 284, 8083-8092.
51. Criollo, A., Maiuri, M.C., Tasdemir, E., Vitale, I., Fiebig, A.A., Andrews, D., Molgo, J., Diaz, J., Lavandero, S., Harper, F. et al. (2007) Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ., 14, 1029-1039.
52. Vicencio, J.M., Ortiz, C., Criollo, A., Jones, A.W., Kepp, O., Galluzzi, L., Joza, N., Vitale, I., Morselli, E., Tailler, M. et al. (2009) The inositol 1,4,5-trisphosphate receptor regulates autophagy through its interaction with Beclin 1. Cell Death Differ., 16, 1006-1017.
53. Khan, M.T. and Joseph, S.K. (2010) Role of inositol trisphosphate receptors in autophagy in DT40 cells. J. Biol. Chem., 285, 16912-16920.
54. Harr, M.W., McColl, K.S., Zhong, F., Molitoris, J.K. and Distelhorst, C.W. (2010) Glucocorticoids downregulate Fyn and inhibit IP(3)-mediated calcium signaling to promote autophagy in T lymphocytes. Autophagy, 6, 912-921.
55. Decuypere, J.P., Bultynck, G. and Parys, J.B. (2011) A dual role for Ca(2+) in autophagy regulation. Cell Calcium, 50, 242-250.
56. Estes, P.S., Boehringer, A., Zwick, R., Tang, J.E., Grigsby, B. and Zarnescu, D.C. (2011) Wild-type and A315T mutant TDP-43 exert differential neurotoxicity in a Drosophila model of ALS. Hum. Mol. Genet., 20, 2308-2321.
57. Ritson, G.P., Custer, S.K., Freibaum, B.D., Guinto, J.B., Geffel, D., Moore, J., Tang, W., Winton, M.J., Neumann, M., Trojanowski, J.Q. et al. (2010) TDP-43 mediates degeneration in a novel Drosophila model of disease caused by mutations in VCP/p97. J. Neurosci., 30, 7729-7739.
58. Godena, V.K., Romano, G., Romano, M., Appocher, C., Klima, R., Buratti, E., Baralle, F.E. and Feiguin, F. (2011) TDP-43 regulates Drosophila neuromuscular junctions growth by modulating Futsch/ MAP1B levels and synaptic microtubules organization. PLoS One, 6, e17808.
59. Miguel, L., Frebourg, T., Campion, D. and Lecourtois, M. (2011) Both cytoplasmic and nuclear accumulations of the protein are neurotoxic in Drosophila models of TDP-43 proteinopathies. Neurobiol. Dis., 41, 398-406.
60. Elden, A.C., Kim, H.J., Hart, M.P., Chen-Plotkin, A.S., Johnson, B.S., Fang, X., Armakola, M., Geser, F., Greene, R., Lu, M.M. et al. (2010) Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature, 466, 1069-1075.
61. Li, Y., Ray, P., Rao, E.J., Shi, C., Guo, W., Chen, X., Woodruff, E.A. 3rd, Fushimi, K. and Wu, J.Y. (2010) A Drosophila model for TDP-43 proteinopathy. Proc. Natl Acad. Sci. USA, 107, 3169-3174.
62. Tollervey, J.R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., Konig, J., Hortobagyi, T., Nishimura, A.L., Zupunski, V. et al. (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci., 14, 452-458.
63. Dou, D. and Joseph, R. (1996) Cloning of human neuronatin gene and its localization to chromosome-20q 11.2-12: the deduced protein is a novel 'proteolipid'. Brain Res., 723, 8-22.
64. Oyang, E.L., Davidson, B.C., Lee, W. and Poon, M.M. (2011) Functional characterization of the dendritically localized mRNA neuronatin in hippocampal neurons. PLoS ONE, 6, e24879.
65. Higo, T., Hamada, K., Hisatsune, C., Nukina, N., Hashikawa, T., Hattori, M., Nakamura, T. and Mikoshiba, K. (2010) Mechanism of ER stress-induced brain damage by IP(3) receptor. Neuron, 68, 865-878.
66. Rothenberg, C., Srinivasan, D., Mah, L., Kaushik, S., Peterhoff, C.M., Ugolino, J., Fang, S., Cuervo, A.M., Nixon, R.A. and Monteiro, M.J. (2010) Ubiquilin functions in autophagy and is degraded by chaperone-mediated autophagy. Hum. Mol. Genet., 19, 3219-3232.
67. Tang, T.S., Tu, H., Chan, E.Y., Maximov, A., Wang, Z., Wellington, C.L., Hayden, M.R. and Bezprozvanny, I. (2003) Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Neuron, 39, 227-239.
68. Tang, T.S., Guo, C., Wang, H., Chen, X. and Bezprozvanny, I. (2009) Neuroprotective effects of inositol 1,4,5-trisphosphate receptor C-terminal fragment in a Huntington's disease mouse model. J. Neurosci., 29, 1257-1266.
69. Liu, J., Tang, T.S., Tu, H., Nelson, O., Herndon, E., Huynh, D.P., Pulst, S.M. and Bezprozvanny, I. (2009) Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 2. J. Neurosci., 29, 9148-9162.
70. Kim, S.H., Shanware, N.P., Bowler, M.J. and Tibbetts, R.S. (2010) Amyotrophic lateral sclerosis-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to co-regulate HDAC6 mRNA. J. Biol. Chem., 285, 34097-34105.
71. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
72. Deshpande, M., Venkatesh, K., Rodrigues, V. and Hasan, G. (2000) The inositol 1,4,5-trisphosphate receptor is required for maintenance of olfactory adaptation in Drosophila antennae. J. Neurobiol., 43, 282-288.
73. Joshi, R., Venkatesh, K., Srinivas, R., Nair, S. and Hasan, G. (2004) Genetic dissection of itpr gene function reveals a vital requirement in aminergic cells of Drosophila larvae. Genetics, 166, 225-236.
74. Feany, M.B. and Bender, W.W. (2000) A Drosophila model of Parkinson's disease. Nature, 404, 394-398.
75. Wu, J.S. and Luo, L. (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat. Protoc., 1, 2110-2115.