Huntingtin Bodies Sequester Vesicle-Associated Proteins by a Polyproline-Dependent Interaction

Journal of Neuroscience

Volumn 24, Issue 1, 2004, Pages 269-281

  Qin, Zheng Hong ^a   Wang, Yumei ^a   Sapp, Ellen ^a   Cuiffo, Benjamin ^a   Wanker, Erich ^c   Hayden, Michael R ^d   Kegel, Kimberly B ^a   Aronin, Neil ^b   DiFiglia, Marian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Autophagy; Dynamin; Huntingtin; Huntington's disease; Protein aggregates; Protein interactions; Vesicle trafficking

Indexed keywords

CATHEPSIN D; DYNAMIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HEAT SHOCK PROTEIN 70; HUNTINGTIN; PROLINE; PROTEASOME;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL DEATH; HUNTINGTON CHOREA; IMMUNOREACTIVITY; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SYNAPSE VESICLE; TISSUE DISTRIBUTION;

ANIMALS; CELL LINE; CEREBRAL CORTEX; DYNAMINS; ENDOPEPTIDASES; EPITOPES; HUMANS; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MICE; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PEPTIDES; PHAGOSOMES; PROTEIN STRUCTURE, TERTIARY; TRANSFERRIN; VESICULAR TRANSPORT PROTEINS;

EID: 0842322740     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1409-03.2004     Document Type: Article

References (54)

1. Andrade MA, Bork P (1995) HEAT repeats in the Huntington's disease protein. Nat Genet 11:115-116.
2. Bao J, Sharp AH, Wagster MV, Becher M, Schilling G, Dawson CA, Dawson M (1996) Expansion of polyglutamine repeat in huntingtin leads to abnormal protein interactions involving calmodulin. Proc Natl Acad Sci USA 93:5037-5042.
3. Bevivino AE, Loll PJ (2001) An expanded glutamine repeat destabilizes native ataxin-3 structure and mediates formation of parallel β-fibrils. Proc Natl Acad Sci USA 98:11955-11960.
4. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, Teplow DB (2003) Amyloid β-protein (Aβ) assembly: Aβ 40 and Aβ 42 oligomerize through distinct pathways. Proc Natl Acad Sci USA 100:330-335.
5. Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, Scherzoner E, Wanker EE, Manginarini L, Bates GP (1997) Formation of neuronal intranulear inclusions underlies neurological dysfunction in mice transgenic for the mutation. Cell 90:537-548.
6. DiFiglia M, Sapp E, Chase K, Schwarz C, Meloni A, Young C, Martin E, Vonsattel J-P, Carraway R, Reeves SA, Boyce FM, Aronin N (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14:1075-1081.
7. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neuritis in brain. Science 277:1990-1993.
8. Engqvist-Goldstein AE, Kessels MM, Chopra VS, Hayden MR, Drubin DG (1999) An actin-binding protein of the Sla2/Huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles. J Cell Biol 147:1503-1518.
9. Faber PW, Barnes GT, Srinidhi J, Guesella JF, MacDonald ME (1998) Huntingtin interacts with a family of WW domain proteins. Hum Mol Genet 7:1463-1474.
10. Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, She WC, Luchak JM, Martinez P, Turiegano E, Benito J, Capovilla M, Skinner PJ, McCall A, Canal I, Orr HT, Zoghbi HY, Botas J (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408:101-106.
11. Gafni J, Ellerby LM (2002) Calpain activation in Huntington's disease. J Neurosci 22:4842-4849.
12. Gervais FG, Singaraja RX, Anthoudakis S, Gutekunst C-A, Leavitt BR, Metzler M, Hackam AS, Tam J, Vaillancourt JP, Houtzager V, Rasper DM, Roy S, Hayden MR, Nicholson DW (2002) Recruitment and activation of caspase 8 by the huntingtin-interacting protein Hip-1 and a novel partner Hippi. Nat Cell Biol 4:95-105.
13. Gutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, Jones R, Rye D, Ferrante RJ, Hersch SM, Li XJ (1999) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J Neurosci 19:2522-2534.
14. Hattula K, Peränen J (2000) FIP-2, a coiled-coil protein, links huntingtin to Rab8 and modulates cellular morphogenesis. Curr Biol 10:1603-1606.
15. Hazeki N, Tsukamoto T, Yazawa I, Koyama M, Hattori S, Someki I, Iwatsubo T, Nakamura K, Goto J, Kanazawa I (2002) Ultrastructure of nuclear aggregates formed by expressing an expanded polyglutamine. Biochem Biophys Res Commun 294:429-440.
16. Katzmann DJ, Odorizzi G, Emr SC (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3:893-905.
17. Kegel KB, Kim M, Sapp E, McIntyre C, Castaño JG, Aronin N, DiFiglia M (2000) Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J Neurosci 20:7268-7278.
18. Khoshnan A, Ko J, Patterson PH (2002) Effects of intracellular expression of anti-huntingtin antibodies of various specificities on mutant huntingtin aggregation and toxicity. Proc Natl Acad Sci USA 99:1002-1007.
19. Kim M, Lee S-H, LaForet G, McIntyre C, Martin EL, Chang P, Kim TW, William M, Reddy PH, Tagle D, Boyce FM, Won L, Heller A, Aronin N, DiFiglia M (1999) Mutant huntingtin expression in clonal striatal cells: dissociation of inclusion formation and neuronal survival by caspase inhibition. J Neurosci 19:964-973.
20. Kim YJ, Yi Y, Sapp E, Wang Y, Cuiffo B, Kegel KB, Qin Z-H, Aronin N (2001) Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain- dependent proteolysis. Proc Natl Acad Sci USA 98:12784-12789.
21. Klionsky DJ (1999) Vacuolar import of proteins and organelles from the cytoplasm. Annu Rev Cell Biol 15:1-32.
22. Kuemmerle S, Gutekunst CA, Klein AM, Li XJ, Li SH, Beal MF, Hersch SM, Ferrante RJ (1999) Huntingtin aggregates may not predict neuronal death in Huntington's disease. Ann Neurol 46:842-849.
23. Kunz J, Schneider U, Howald I, Schmidt A, Hall MN (2000) HEAT repeats mediate plasma membrane localization of Tor2p in yeast. J Biol Chem 275:37011-37020.
24. Li H, Li S-H, Yu Z-X, Shelbourne P, Li XJ (2001) Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J Neurosci 21:8473-8481.
25. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676.
26. Liu YF, Deth RC, Devys D (1997) SH3 domain-dependent association of huntingtin with epidermal growth factor receptor signaling complex. J Biol Chem 272:8121-8124.
27. Metzler M, Legendre-Guillemin V, Gan L, Chopra V, Kwok A, McPherson PS, Hayden MR (2001) HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J Biol Chem 276:39271-39276.
28. Miake H, Mizusawa H, Iwatsubo T, Hasegawa M (2002) Biochemical characterization of the core structure of α-synuclein filaments. J Biol Chem 277:19213-19219.
29. Modregger J, DiProspero NA, Charles V, Tagle DA, Plomann M (2002) Pacsin 1 interacts with huntingtin and is absent from synaptic varicosities in presymptomatic Huntington's disease brains. Hum Mol Genet 11:2547-2558.
30. Panov AV, Gutekunst CA, Leavitt BR, Haden MR, Burke JR, Strittmatter WJ, Greenamyre JT (2002) Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat Neurosci 5:731-736.
31. Passani LA, Bedford MT, Faber PW, McGinnis KM, Sharp AH, Gusella JF, Vonsattel JP, McDonald ME (2000) Huntingtin's WW domain partners in Huntingtin's disease post-mortem brain fulfill genetic criteria for direct involvement in Huntington's disease pathogenesis. Hum Mol Genet 9:2175-2182.
32. Perutz MF, Finch JT, Lesk A (2002) Amyloid fibers are water-filled nanotubes. Proc Natl Acad Sci USA 99:5591-5595.
33. Pitts KR, Yoon Y, Krueger EW, McNiven MA (1999) The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol Biol Cell 10:4403-4417.
34. Poirier MA, Li H, Macosko J, Cai S, Amzel M (2002) Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrilization. J Biol Chem 277:41032-41037.
35. Qin Z-H, Wang Y, Kikly KK, Sapp E, Kegel KB, Aronin N, DiFiglia M (2001) Pro-caspase-8 is predominantly localized in mitochondria and released into cytoplasm upon apoptotic stimulation. J Biol Chem 276:8079-8086.
36. Qin Z-H, Wang Y, Kegel KB, Kazantsev A, Apostol BL, Thompson LM, Yoder J, Aronin H, DiFiglia M (2003) Autophagy regulates the processing of amino terminal huntingtin fragments. Hum Mol Gen 12:3231-3244.
37. Sapp E, Ge P, Aizawa H, Bird E, Penney J, Young AB, Vonsattel JP, DiFiglia M (1995) Evidence for a preferential loss of enkephalin immnoreactivity in the external globus pallidus in low grade Huntington's disease using high resolution image analysis. Neuroscience 64:397-404.
38. Sapp E, Schwarz C, Chase K, Bhide PG, Young AB, Penney J, Vonsattel JP, Aronin N, DiFiglia M (1997) Huntingtin localization in brains of normal and Huntington's disease patients. Ann Neurol 42:604-612.
39. Sapp E, Penney J, Young A, Aronin N, Vonsattel JP, DiFiglia M (1999) Axonal transport of N-terminal huntingtin suggests early pathology of corticostriatal projections in Huntington disease. J Neuropathol Exp Neurol 58:165-173.
40. Saudou F, Finkbeiner S, Devys D, Greenberg ME (1998) Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95:55-66.
41. Scherzinger E, Lutz R, Turmaine M, Mangiarini L, Hollenbach B, Hasenbank R, Bates GP, Davies SW, Lhrach H, Wanker EE (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90:549-558.
42. Sever S (2002) Dynamin and endocytosis. Curr Opin Cell Biol 14:463-467.
43. Sisodia SS (1998) Nuclear inclusions in glutamine repeat disorders: are they pernicious, coincidental, or beneficial? Cell 95:1-4.
44. Sittler A, Walter S, Wedemeyer N, Hasenbank R, Scherzinger E, Eickhoff H, Bates GP, Lehrach H, Wanker EE (1998) SH3GL3 associates with the huntingtin exon 1 protein and promotes the formation of polygln-containing protein aggregates. Mol Cell 2:427-436.
45. So CW, Sham MH, Chew SL, Cheung N, So CKC, Chung SK, Caldas C, Wiedemann LM, Chan LC (2000) Expression and protein-binding studies of the EEN gene family, new interacting partners for dynamin, synaptojanin and huntingtin proteins. Biochem J 348:447-458.
46. Takano H, Gusella JF (2002) The predominantly HEAT-like motif structure of huntingtin and its association and coincident nuclear entry with dorsal, an NF-κB/Rel/dorsal family transcription factor. BMC Neurosci 3:15.
47. Velier J, Kim M, Schwarz C, Kim TW, Sapp E, Chase K, Aronin N, DiFiglia M (1998) Wild-type and mutant huntingtins function in vesicle trafficking in the secretory and endocytic pathways. Exp Neurol 152:34-40.
48. Vonsattel JP, DiFiglia M (1998) Huntington disease. J Neuropathol Exp Neurol 57:369-384.
49. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson Jr EP (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44:559-577.
50. Waelter S, Scherzinger E, Hasenbank R, Nordhoff E, Lurz R, Goehler H, Gauss C, Sathasivam K, Bates GP, Lehrach H, Wanker EE (2001) The huntingtin interacting protein 1 is a clathrin and α-adaptin-binding protein involved in receptor-mediated endocytosis. Hum Mol Genet 10:1807-1817.
51. Wainwright MS, Perry BD, Won LA, O'Malley KL, Wang WY, Ehrlich ME, Heller A (1995) Immortalized murine striatal neuronal cell lines expressing dopamine receptors and cholinergic properties. J Neurosci 15:676-688.
52. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539.
53. Wanker E, Rovira C, Scherzinger E, Hasenbank R, Wälter S, Tait D, Colicelli J, Lehrach H (1997) HIP-1: a huntingtin interacting protein isolated by the yeast two-hybrid system. Hum Mol Genet 6:487-495.
54. Wellington CL, Ellerby LM, Rogers CAD, Warby S, Graham RK, Loubser O, van Raamsdonk J, Singaraja R, Yang YZ, Gafni J, Bredesen D, Hersch SM, Leavitt BR, Roy S, Nicholson DW, Hayden MR (2002) Caspase cleavage of mutant huntingtin precedes neurodegeneration in Huntington's disease. J Neurosci 22:7862-7872.