Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway

Journal of Cell Biology

Volumn 172, Issue 5, 2006, Pages 719-731

  Yamamoto, Ai ^a   Cremona, M Laura ^a   Rothman, James E ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; INSULIN; INSULIN RECEPTOR SUBSTRATE 2; INTERLEUKIN 4; MAMMALIAN TARGET OF RAPAMYCIN; MUTANT PROTEIN; S6 KINASE; SOMATOMEDIN C;

ARTICLE; AUTOPHAGY; GENE IDENTIFICATION; HUMAN; HUNTINGTON CHOREA; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TARGETING; REMISSION; SIGNAL TRANSDUCTION; STARVATION; TRANSGENE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AUTOPHAGY; CELL LINE; GENE EXPRESSION PROFILING; INSULIN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 33644540193     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200510065     Document Type: Article

References (66)

1. Andrejewski, N., E.L. Punnonen, G. Guhde, Y. Tanaka, R. Lullmann-Rauch, D. Hartmann, K. von Figura, and P. Saftig. 1999. Normal lysosomal morphology and function in LAMP-1-deficient mice. J. Biol. Chem. 274:12692-12701.
2. Arrasate, M., S. Mitra, E.S. Schweitzer, M.R. Segal, and S. Finkbeiner. 2004. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature. 431:805-810.
3. Backer, J.M. 2000. Phosphoinositide 3-kinases and the regulation of vesicular trafficking. Mol. Cell Biol. Res. Commun. 3:193-204.
4. Bence, N.F., R.M. Sampat, and R.R. Kopito. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 292:1552-1555.
5. Blommaart, E.F., U. Krause, J.P. Schellens, H. Vreeling-Sindelarova, and A.J. Meijer. 1997. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243:240-246.
6. Chaussade, C., L. Pirola, S. Bonnafous, F. Blondeau, S. Brenz-Verca, H. Tronchere, F. Portis, S. Rusconi, B. Payrastre, J. Laporte, and E. Van Obberghen. 2003. Expression of myotubularin by an adenoviral vector demonstrates its function as a phosphatidylinositol 3-phosphate [PtdIns(3)P] phosphatase in muscle cell lines: involvement of PtdIns(3)P in insulin-stimulated glucose transport. Mol. Endocrinol. 17:2448-2460.
7. Elbashir, S.M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 411:494-498.
8. Franke, T.F., D.R. Kaplan, L.C. Cantley, and A. Toker. 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4- bisphosphate. Science. 275:665-668.
9. Gossen, M., A.L. Bonin, S. Freundlieb, and H. Bujard. 1994. Inducible gene expression systems for higher eukaryotic cells. Curr. Opin. Biotechnol. 5:516-520.
10. Harper, S.Q., P.D. Staber, X. He, S.L. Eliason, I.H. Martins, Q. Mao, L. Yang, R.M. Kotin, H.L. Paulson, and B.L. Davidson. 2005. From the cover: RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc. Natl. Acad. Sci. USA. 102:5820-5825.
11. Humbert, S., E.A. Bryson, F.P. Cordelieres, N.C. Connors, S.R. Datta, S. Finkbeiner, M.E. Greenberg, and F. Saudou. 2002. The IGF-1/Akt pathway is neuroprotective in Huntington's disease and involves huntingtin phosphorylation by Akt. Dev. Cell. 2:831-837.
12. Iwata, A., J.C. Christianson, M. Bucci, L.M. Ellerby, N. Nukina, L.S. Forno, and R.R. Kopito. 2005a. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc. Natl. Acad. Sci. USA. 102:13135-13140.
13. Iwata, A., B.E. Riley, J.A. Johnston, and R.R. Kopito. 2005b. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 280:40282-40292.
14. Jacinto, E., and M.N. Hall. 2003. Tor signalling in bugs, brain and brawn. Nat. Rev. Mol. Cell Biol. 4:117-126.
15. Jagla, B., N. Aulner, P.D. Kelly, D. Song, A. Volchuk, A. Zatorski, D. Shum, T. Mayer, D.A. De Angelis, O. Ouerfelli, et al. 2005. Sequence characteristics of functional siRNAs. RNA. 11:864-872.
16. Jana, N.R., M. Tanaka, G. Wang, and N. Nukina. 2000. Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: their role in suppression of aggregation and cellular toxicity. Hum. Mol. Genet. 9:2009-2018.
17. Jana, N.R., E.A. Zemskov, G. Wang, and N. Nukina. 2001. Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum. Mol. Genet. 10:1049-1059.
18. Jiang, Z.Y., Q.L. Zhou, K.A. Coleman, M. Chouinard, Q. Boese, and M.P. Czech. 2003. Insulin signaling through Akt/protein kinase B analyzed by small interfering RNA-mediated gene silencing. Proc. Natl. Acad. Sci. USA. 100:7569-7574.
19. Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
20. Kamada, Y., T. Funakoshi, T. Shintani, K. Nagano, M. Ohsumi, and Y. Ohsumi. 2000. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150:1507-1513.
21. Kanekura, K., Y. Hashimoto, Y. Kita, J. Sasabe, S. Aiso, I. Nishimoto, and M. Matsuoka. 2005. A Rac1/phosphatidylinositol 3-kinase/Akt3 antiapoptotic pathway, triggered by AlsinLF, the product of the ALS2 gene, antagonizes Cu/Zn-superoxide dismutase (SOD1) mutant-induced motoneuronal cell death. J. Biol. Chem. 280:4532-4543.
22. Kaspar, B.K., J. Llado, N. Sherkat, J.D. Rothstein, and F.H. Gage. 2003. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science. 301:839-842.
23. Kihara, A., Y. Kabeya, Y. Ohsumi, and T. Yoshimori. 2001. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2:330-335.
24. Kim, M., H.S. Lee, G. LaForet, C. McIntyre, E.J. Martin, P. Chang, T.W. Kim, M. Williams, P.H. Reddy, D. Tagle et al. 1999. Mutant huntingtin expression in clonal striatal cells: dissociation of inclusion formation and neuronal survival by caspase inhibition. J. Neurosci. 19:964-973.
25. Klionsky, D.J., and S.D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science. 290:1717-1721.
26. Klionsky, D.J., A.J. Meijer, P. Codogno, T.P. Neufeld, and R.C. Scott. 2005. Autophagy and p70S6 Kinase. Autophagy. 1:59-61.
27. Lai, E.C., K.J. Felice, B.W. Festoff, M.J. Gawel, D.F. Gelinas, R. Kratz, M.F. Murphy, H.M. Natter, F.H. Norris, and S.A. Rudnicki. 1997. Effect of recombinant human insulin-like growth factor-I on progression of ALS. A placebo-controlled study. The North America ALS/IGF-I Study Group. Neurology. 49:1621-1630.
28. Liang, X.H., S. Jackson, M. Seaman, K. Brown, B. Kempkes, H. Hibshoosh, and B. Levine. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 402:672-676.
29. Loh, J.E., C.H. Chang, W.L. Fodor, and R.A. Flavell. 1992. Dissection of the interferon gamma-MHC class II signal transduction pathway reveals that type I and type II interferon systems share common signalling component(s). EMBO J. 11:1351-1363.
30. Maffucci, T., A. Brancaccio, E. Piccolo, R.C. Stein, and M. Falasca. 2003. Insulin induces phosphatidylinositol-3-phosphate formation through TC10 activation. EMBO J. 22:4178-4189.
31. Martin-Aparicio, E., A. Yamamoto, F. Hernandez, R. Hen, J. Avila, and J.J. Lucas. 2001. Proteasomal-dependent aggregate reversal and absence of cell death in a conditional mouse model of Huntington's disease. J. Neurosci. 21:8772-8781.
32. Meijer, A.J., and P. Codogno. 2004. Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36:2445-2462.
33. Mizushima, N. 2004. Methods for monitoring autophagy. Int. J. Biochem. Cell Biol. 36:2491-2502.
34. Mizushima, N., A. Yamamoto, M. Matsui, T. Yoshimori, and Y. Ohsumi. 2004. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell. 15:1101-1111.
35. Nakagawa, I., A. Amano, N. Mizushima, A. Yamamoto, H. Yamaguchi, T. Kamimoto, A. Nara, J. Funao, M. Nakata, K. Tsuda, et al. 2004. Autophagy defends cells against invading group A Streptococcus. Science. 306:1037-1040.
36. Nakamura, K., A. Hongo, J. Kodama, Y. Miyagi, M. Yoshinouchi, and T. Kudo. 2000. Down-regulation of the insulin-like growth factor I receptor by antisense RNA can reverse the transformed phenotype of human cervical cancer cell lines. Cancer Res. 60:760-765.
37. Pelkmans, L., E. Fava, H. Grabner, M. Hannus, B. Habermann, E. Krausz, and M. Zerial. 2005. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature. 436:78-86.
38. Petiot, A., E. Ogier-Denis, E.F. Blommaart, A.J. Meijer, and P. Codogno. 2000. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:992-998.
39. Qin, Z.H., Y. Wang, K.B. Kegel, A. Kazantsev, B.L. Apostol, L.M. Thompson, J. Yoder, N. Aronin, and M. DiFiglia. 2003. Autophagy regulates the processing of amino terminal huntingtin fragments. Hum. Mol. Genet. 12:3231-3244.
40. Rangone, H., G. Poizat, J. Troncoso, C.A. Ross, M.E. MacDonald, F. Saudou, and S. Humbert. 2004. The serum- and glucocorticoid-induced kinase SGK inhibits mutant huntingtin-induced toxicity by phosphorylating serine 421 of huntingtin. Eur. J. Neurosci. 19:273-279.
41. Rangone, H., R. Pardo, E. Colin, J.A. Girault, F. Saudou, and S. Humbert. 2005. Phosphorylation of arfaptin 2 at Ser260 by Akt Inhibits PolyQ-huntingtin-induced toxicity by rescuing proteasome impairment. J. Biol. Chem. 280:22021-22028.
42. Ravikumar, B., R. Duden, and D.C. Rubinsztein. 2002. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11:1107-1117.
43. Ravikumar, B., C. Vacher, Z. Berger, J.E. Davies, S. Luo, L.G. Oroz, F. Scaravilli, D.F. Easton, R. Duden, C.J. O'Kane, and D.C. Rubinsztein. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36:585-595.
44. Regulier, E., Y. Trottier, V. Perrin, P. Aebischer, and N. Deglon. 2003. Early and reversible neuropathology induced by tetracycline-regulated lentiviral overexpression of mutant huntingtin in rat striatum. Hum. Mol. Genet. 12:2827-2836.
45. Saltiel, A.R. 2001. New perspectives into the molecular pathogenesis and treatment of type 2 diabetes. Cell. 104:517-529.
46. Saudou, F., S. Finkbeiner, D. Devys, and M.E. Greenberg. 1998. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:55-66.
47. Scarlatti, F., C. Bauvy, A. Ventruti, G. Sala, F. Cluzeaud, A. Vandewalle, R. Ghidoni, and P. Codogno. 2004. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1. J. Biol. Chem. 279:18384-18391.
48. Schu, P.V., K. Takegawa, M.J. Fry, J.H. Stack, M.D. Waterfield, and S.D. Emr. 1993. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science. 260:88-91.
49. Schubert, M., D.P. Brazil, D.J. Burks, J.A. Kushner, J. Ye, C.L. Flint, J. Farhang-Fallah, P. Dikkes, X.M. Warot, C. Rio, et al. 2003. Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 23:7084-7092.
50. Scott, R.C., O. Schuldiner, and T.P. Neufeld. 2004. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell. 7:167-178.
51. Seglen, P.O., and P.B. Gordon. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA. 79:1889-1892.
52. Sun, X.J., M. Miralpeix, M.G. Myers Jr., E.M. Glasheen, J.M. Backer, C.R. Kahn, and M.F. White. 1992. Expression and function of IRS-1 in insulin signal transmission. J. Biol. Chem. 267:22662-22672.
53. Sun, X.J., L.M. Wang, Y. Zhang, L. Yenush, M.G. Myers Jr., E. Glasheen, W.S. Lane, J.H. Pierce, and M.F. White. 1995. Role of IRS-2 in insulin and cytokine signalling. Nature. 377:173-177.
54. Talloczy, Z., W. Jiang, H.W. Virgin, D.A. Leib, D. Scheuner, R.J. Kaufman, E.L. Eskelinen, and B. Levine. 2002. Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. USA. 99:190-195.
55. Tanaka, Y., G. Guhde, A. Suter, E.L. Eskelinen, D. Hartmann, R. Lullmann-Rauch, P.M. Janssen, J. Blanz, K. von Figura, and P. Saftig. 2000. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature. 406:902-906.
56. Tassa, A., M.P. Roux, D. Attaix, and D.M. Bechet. 2003. Class III phosphoinositide 3-kinase-Beclin1 complex mediates the amino acid-dependent regulation of autophagy in C2C12 myotubes. Biochem. J. 376:577-586.
57. Taylor, J.P., F. Tanaka, J. Robitschek, C.M. Sandoval, A. Taye, S. Markovic-Plese, and K.H. Fischbeck. 2003. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum. Mol. Genet. 12:749-757.
58. Vassen, L., W. Wegrzyn, and L. Klein-Hitpass. 1999. Human insulin receptor substrate-2 (IRS-2) is a primary progesterone response gene. Mol. Endocrinol. 13:485-494.
59. Virbasius, J.V., X. Song, D.P. Pomerleau, Y. Zhan, G.W. Zhou, and M.P. Czech. 2001. Activation of the Akt-related cytokine-independent survival kinase requires interaction of its phox domain with endosomal phosphatidylinositol 3-phosphate. Proc. Natl. Acad. Sci. USA. 98:12908-12913.
60. Waelter, S., A. Boeddrich, R. Lurz, E. Scherzinger, G. Lueder, H. Lehrach, and E.E. Wanker. 2001. Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol. Biol. Cell. 12:1393-1407.
61. Wang, G.H., K. Mitsui, S. Kotliarova, A. Yamashita, Y. Nagao, S. Tokuhiro, T. Iwatsubo, I. Kanazawa, and N. Nukina. 1999. Caspase activation during apoptotic cell death induced by expanded polyglutamine in N2a cells. Neuroreport. 10:2435-2438.
62. White, M.F. 2003. Insulin signaling in health and disease. Science. 302:1710-1711.
63. Xia, H., Q. Mao, S.L. Eliason, S.Q. Harper, I.H. Martins, H.T. Orr, H.L. Paulson, L. Yang, R.M. Kotin, and B.L. Davidson. 2004. RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat. Med. 10:816-820.
64. Yamamoto, A., J.J. Lucas, and R. Hen. 2000. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell. 101:57-66.
65. Zacharias, D.A., J.D. Violin, A.C. Newton, and R.Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296:913-916.
66. Zu, T., L.A. Duvick, M.D. Kaytor, M.S. Berlinger, H.Y. Zoghbi, H.B. Clark, and H.T. Orr. 2004. Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J. Neurosci. 24:8853-8861.