Intersectin enhances huntingtin aggregation and neurodegeneration through activation of c-Jun-NH2-terminal kinase

Human Molecular Genetics

Volumn 16, Issue 15, 2007, Pages 1862-1871

  Scappini, Erica ^a   Koh, Tong Wey ^b   Martin, Negin P ^a   O'Bryan, John P ^a,c  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; HUNTINGTIN; INTERSECTIN; POLYGLUTAMINE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DROSOPHILA; ENZYME ACTIVATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MUTANT; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

EID: 34547843693     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm134     Document Type: Article

References (55)

1. Wexler, N.S., Rose, E.A. and Housman, D.E. (1991) Molecular approaches to hereditary diseases of the nervous system: Huntington's disease as a paradigm. Annu. Rev. Neurosci., 14, 503-529.
2. Group, H.s.D.C.R (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell, 72, 971-983.
3. Petersen, A., Mani, K. and Brundin, P. (1999) Recent advances on the pathogenesis of Huntington's disease. Exp. Neurol., 157, 1-18.
4. La Spada, A.R., Wilson, E.M., Lubahn, D.B., Harding, A.E. and Fischbeck, K.H. (1991) Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature (London), 352, 77-79.
5. Kawaguchi, Y., Okamoto, T., Taniwaki, M., Aizawa, M., Inoue, M., Katayama, S., Kawakami, H., Nakamura, S., Nishimura, M., Akiguchi, I. et al. (1994) CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat. Genet., 8, 221-228.
6. Koide, R., Ikeuchi, T., Onodera, O., Tanaka, H., Igarashi, S., Endo, K., Takahashi, H., Kondo, R., Ishikawa, A., Hayashi, T. et al. (1994) Unstable expansion of CAG repeat in hereditary dentatorubral-pallidoluysian atrophy (DRPLA). Nat. Genet., 6 9-13.
7. Bates, G. (2003) Huntingtin aggregation and toxicity in Huntington's disease. Lancet, 361, 1642-1644.
8. Rubinsztein, D.C., Leggo, J., Chiano,M., Dodge, A., Norbury, G., Rosser, E. and Craufurd, D. (1997) Genotypes at the GluR6 kainate receptor locus are associated with variation in the age of onset of Huntington disease. Proc. Natl Acad. Sci. USA., 94, 3872-3876.
9. Becher, M.W., Kotzuk, J.A., Sharp, A.H., Davies, S.W., Bates, G.P., Price, D.L. and Ross, C.A. (1998) Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length. Neurobiol. Dis., 4, 387-397.
10. Saudou, F., Finkbeiner, S., Devys, D. and Greenberg, M.E. (1998) Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell, 95, 55-66.
11. Kim, S., Nollen, E.A., Kitagawa, K., Bindokas, V.P. and Morimoto, R.I. (2002) Polyglutamine protein aggregates are dynamic. Nat. Cell. Biol. 4, 826-831.
12. Yang, W., Dunlap, J.R., Andrews, R.B. and Wetzel, R. (2002) Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum. Mol. Genet., 11, 2905-2917.
13. Kazantsev, A., Walker, H.A., Slepko, N., Bear, J.E., Preisinger, E., Steffan, J.S., Zhu, Y.Z., Gertler, F.B., Housman, D.E., Marsh, J.L. et al. (2002) A bivalent Huntingtin binding peptide suppresses polyglutamine aggregation and pathogenesis in Drosophila. Nat. Genet. 30, 367-376.
14. Pollitt, S.K., Pallos, J., Shao, J., Desai, U.A., Ma, A.A., Thompson, L.M., Marsh, J.L. and Diamond, M.I. (2003) A rapid cellular FRET assay of polyglutamine aggregation identifies a novel inhibitor. Neuron, 40, 685-694.
15. Sanchez, I., Mahlke, C. and Yuan, J. (2003) Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature (London), 421, 373-379.
16. Tanaka, M., Machida, Y., Niu, S., Ikeda, T., Jana, N.R., Doi, H., Kurosawa, M., Nekooki, M. and Nukina, N. (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat. Med., 10, 148-154.
17. Arrasate, M., Mitra, S., Schweitzer, E.S., Segal, M.R. and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature (London), 431, 805-810.
18. Bodner, R.A., Outeiro, T.F., Altmann, S., Maxwell, M.M., Cho, S.H., Hyman, B.T., McLean, P.J., Young, A.B., Housman, D.E. and Kazantsev, A.G. (2006) Pharmacological promotion of inclusion formation: A therapeutic approach for Huntington's and Parkinson's diseases. Proc. Natl Acad. Sci. USA., 103, 4246-4251.
19. O'Bryan, J.P., Mohney, R.P. and Oldham, C.E. (2001) Mitogenesis and endocytosis: What's at the INTERSECTIoN? Oncogene, 20, 6300-6308.
20. Sengar, A.S., Wang, W., Bishay, J., Cohen, S. and Egan, S.E. (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J., 18, 1159-1171.
21. McPherson, P.S. (2002) The endocytic machinery at an interface with the actin cytoskeleton: A dynamic, hip intersection. Trends Cell Biol. 12, 312-315.
22. Martin, N.P., Mohney, R.P., Dunn, S., Das, M., Scappini, E. and O'Bryan, J.P. (2006) Intersectin regulates epidermal growth factor receptor endocytosis, ubiquitylation, and signaling. Mol. Pharmacol., 70 1643-1653.
23. Johnston, J.A., Ward, C.L. and Kopito, R.R. (1998) Aggresomes: A cellular response to misfolded proteins. J. Cell. Biol., 143 1883-1898.
24. Meriin, A.B., Mabuchi, K., Gabai, V.L., Yaglom, J.A., Kazantsev, A. and Sherman, M.Y. (2001) Intracellular aggregation of polypeptides with expanded polyglutamine domain is stimulated by stress-activated kinase MEKK1. J. Cell. Biol., 153, 851-864.
25. Mohney, R.P., Das, M., Bivona, T.G., Hanes, R., Adams, A.G., Philips, M.R. and O'Bryan, J.P. (2003) Intersectin activates Ras but stimulates transcription through an independent pathway involving JNK. J. Biol. Chem., 278, 47038-47045.
26. Mattson, M.P. and Sherman, M. (2003) Perturbed signal transduction in neurodegenerative disorders involving aberrant protein aggregation. Neuromolecular Med., 4, 109-132.
27. Meriin, A.B., Zhang, X., Miliaras, N.B., Kazantsev, A., Chernoff, Y.O., McCaffery, J.M., Wendland, B. and Sherman, M.Y. (2003) Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol. Cell. Biol., 23, 7554-7565.
28. Adams, A., Thorn, J.M., Yamabhai,M., Kay, B.K. and O'Bryan, J.P. (2000) Intersectin, an adaptor protein involved in clathrin-mediated endocytosis, activates mitogenic signaling pathways. J. Biol. Chem. 275, 27414-27420.
29. Tong, X.K., Hussain, N.K., Adams, A.G., O'Bryan, J.P. and McPherson, P.S. (2000) Intersectin can regulate the Ras/MAP kinase pathway independent of its role in endocytosis. J. Biol. Chem., 275, 29894-29899.
30. Jenna, S., Hussain, N.K., Danek, E.I., Triki, I., Wasiak, S., McPherson, P.S. and Lamarche-Vane, N. (2002) The activity of the GTPase-activating protein CdGAP is regulated by the endocytic protein intersectin. J. Biol. Chem., 277, 6366-6373.
31. Marsh, J.L., Walker, H., Theisen, H., Zhu, Y.Z., Fielder, T., Purcell, J. and Thompson, L.M. (2000) Expanded polyglutamine peptides alone are intrinsically cytotoxic and cause neurodegeneration in Drosophila. Hum. Mol. Genet., 9, 13-25.
32. Kazemi-Esfarjani, P. and Benzer, S. (2000) Genetic suppression of polyglutamine toxicity in Drosophila. Science, 287, 1837-1840.
33. Koh, T.W., Verstreken, P. and Bellen, H.J. (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron, 43, 193-205.
34. Roos, J. and Kelly, R.B. (1998) Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem., 273, 19108-19119.
35. Giot, L., Bader, J.S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y.L., Ooi, C.E., Godwin, B., Vitols, E. et al. (2003) A protein interaction map of Drosophila melanogaster. Science, 302, 1727-1736.
36. Cowan, K.J., Diamond, M.I. and Welch, W.J. (2003) Polyglutamine protein aggregation and toxicity are linked to the cellular stress response. Hum. Mol. Genet., 12, 1377-1391.
37. Okamura-Oho, Y., Miyashita, T., Nagao, K., Shima, S., Ogata, Y., Katada, T., Nishina, H. and Yamada, M. (2003) Dentatorubral-pallidoluysian atrophy protein is phosphorylated by c-Jun NH2-terminal kinase. Hum. Mol. Genet., 12, 1535-1542.
38. Schilling, B., Gafni, J., Torcassi, C., Cong, X., Row, R.H., LaFevre-Bernt, M.A., Cusack, M.P., Ratovitski, T., Hirschhorn, R., Ross, C.A. et al. (2006) Huntingtin phosphorylation sites mapped by mass spectrometry. Modulation of cleavage and toxicity. J. Biol. Chem., 281, 23686-23697.
39. Garcia, M., Charvin, D. and Caboche, J. (2004) Expanded Huntingtin activates the c-Jun terminal kinase/c-Jun pathway prior to aggregate formation in striatal neurons in culture. Neuroscience, 127, 859-870.
40. Liu, Y.F., Dorow, D. and Marshall, J. (2000) Activation of MLK2-mediated signaling cascades by polyglutamine-expanded Huntingtin. J. Biol. Chem., 275, 19035-19040.
41. Liu, Y.F. (1998) Expression of polyglutamine-expanded Huntingtin activates the SEK1-JNK pathway and induces apoptosis in a hippocampal neuronal cell line. J. Biol. Chem., 273, 28873-28877.
42. Apostol, B.L., Illes, K., Pallos, J., Bodai, L., Wu, J., Strand, A., Schweitzer, E.S., Olson, J.M., Kazantsev, A., Marsh, J.L. et al. (2006) Mutant Huntingtin alters MAPK signaling pathways in PC12 and striatal cells: ERK1/2 protects against mutant Huntingtin-associated toxicity. Hum. Mol. Genet., 15, 273-285.
43. Morfini, G., Pigino, G., Szebenyi, G., You, Y., Pollema, S. and Brady, S.T. (2006) JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat. Neurosci., 9 907-916.
44. Song, C., Perides, G. and Liu, Y.F. (2002) Expression of full-length polyglutamine-expanded Huntingtin disrupts growth factor receptor signaling in rat pheochromocytoma (PC12) cells. J. Biol. Chem., 277, 6703-6707.
45. Lievens, J.C., Rival, T., Iche, M., Chneiweiss, H. and Birman, S. (2005) Expanded polyglutamine peptides disrupt EGF receptor signaling and glutamate transporter expression in Drosophila. Hum. Mol. Genet., 14, 713-724.
46. Keating, D.J., Chen, C. and Pritchard, M.A. (2006) Alzheimer's disease and endocytic dysfunction: Clues from the Down syndrome-related proteins, DSCR1 and ITSN1. Ageing Res. Rev., 5, 388-401.
47. Gardiner, K. (2003) Predicting pathway perturbations in Down syndrome. J. Neural. Transm. Suppl., (67) 21-37.
48. Pucharcos, C., Fuentes, J.J., Casas, C., de la Luna, S., Alcantara, S., Arbones, M.L., Soriano, E., Estivill, X. and Pritchard, M. (1999) Alu-splice cloning of human Intersectin (ITSN), a putative multivalent binding protein expressed in proliferating and differentiating neurons and overexpressed in Down syndrome. Eur. J. Hum. Genet., 7, 704-712.
49. Kola, I. and Hertzog, P.J. (1998) Down syndrome and mouse models. Curr. Opin. Genet. Dev., 8, 316-321.
50. Gardiner, K., Davisson, M.T. and Crnic, L.S. (2004) Building protein interaction maps for Down's syndrome. Brief. Funct. Genomic Proteomic 3, 142-156.
51. von Schwedler, U.K., Stuchell, M., Muller, B., Ward, D.M., Chung, H.Y., Morita, E., Wang, H.E., Davis, T., He, G.P., Cimbora, D.M. et al. (2003) The protein network of HIV budding. Cell., 114, 701-713.
52. Freeman, M. (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell. 87, 651-660.
53. Apostol, B.L., Kazantsev, A., Raffioni, S., Illes, K., Pallos, J., Bodai, L., Slepko, N., Bear, J.E., Gertler, F.B., Hersch, S. et al. (2003) A cell-based assay for aggregation inhibitors as therapeutics of polyglutamine-repeat disease and validation in Drosophila. Proc. Natl Acad. Sci. USA., 100, 5950-5955.
54. Verstreken, P., Koh, T.W., Schulze, K.L., Zhai, R.G., Hiesinger, P.R., Zhou, Y., Mehta, S.Q., Cao, Y., Roos, J. and Bellen, H.J. (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron, 40, 733-748.
55. Lee, T. and Luo, L. (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.