Huntingtin interacts with the cue domain of gp78 and inhibits gp78 binding to ubiquitin and p97/VCP

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Yang, Hui ^a   Liu, Chao ^a   Zhong, Yongwang ^a   Luo, Shouqing ^b   Monteiro, Mervyn J ^a   Fang, Shengyun ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLYCOPROTEIN; GLYCOPROTEIN GP 78; HUNTINGTIN; POLYGLUTAMINE; POLYUBIQUITIN; PROTEIN P97; PROTEIN VCP; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; AUTOCRINE MOTILITY FACTOR RECEPTOR; CDC48 PROTEIN; CELL CYCLE PROTEIN; CYTOKINE RECEPTOR; HD PROTEIN, HUMAN; NERVE PROTEIN; NUCLEAR PROTEIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE MAPPING; HUMAN; HUMAN CELL; MUTANT; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; UBIQUITINATION; BINDING SITE; CELL LINE; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; CELL CYCLE PROTEINS; CELL LINE; ENDOPLASMIC RETICULUM; HUMANS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; RECEPTORS, CYTOKINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 77749270634     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008905     Document Type: Article

References (67)

1. Vonsattel JP, DiFiglia M (1998) Huntington disease. J Neuropathol Exp Neurol 57: 369-384.
2. Cattaneo E, Zuccato C, Tartari M (2005) Normal huntingtin function: an alternative approach to Huntington's disease. Nat Rev Neurosci 6: 919-930.
3. Li S, Li XJ (2006) Multiple pathways contribute to the pathogenesis of Huntington disease. Mol Neurodegener 1: 19.
4. Imarisio S, Carmichael J, Korolchuk V, Chen CW, Saiki S, et al. (2008) Huntington's disease: from pathology and genetics to potential therapies. Biochem J 412: 191-209.
5. Finkbeiner S, Mitra S (2008) The ubiquitin-proteasome pathway in Huntington's disease. ScientificWorldJournal 8: 421-433.
6. Kegel KB, Meloni AR, Yi Y, Kim YJ, Doyle E, et al. (2002) Huntingtin is present in the nucleus, interacts with the transcriptional corepressor C-terminal binding protein, and represses transcription. J Biol Chem 277: 7466-7476.
7. Hilditch-Maguire P, Trettel F, Passani LA, Auerbach A, Persichetti F, et al. (2000) Huntingtin: an iron-regulated protein essential for normal nuclear and perinuclear organelles. Hum Mol Genet 9: 2789-2797.
8. Kegel KB, Sapp E, Yoder J, Cuiffo B, Sobin L, et al. (2005) Huntingtin associates with acidic phospholipids at the plasma membrane. J Biol Chem 280: 36464-36473.
9. Strehlow AN, Li JZ, Myers RM (2007) Wild-type huntingtin participates in protein trafficking between the Golgi and the extracellular space. Hum Mol Genet 16: 391-409.
10. Rockabrand E, Slepko N, Pantalone A, Nukala VN, Kazantsev A, et al. (2007) The first 17 amino acids of Huntingtin modulate its sub-cellular localization, aggregation and effects on calcium homeostasis. Hum Mol Genet 16: 61-77.
11. Atwal RS, Xia J, Pinchev D, Taylor J, Epand RM, et al. (2007) Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity. Hum Mol Genet 16: 2600-2615.
12. Orr AL, Li S, Wang CE, Li H, Wang J, et al. (2008) N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J Neurosci 28: 2783-2792.
13. Wang H, Lim PJ, Karbowski M, Monteiro MJ (2009) Effects of overexpression of huntingtin proteins on mitochondrial integrity. Hum Mol Genet 18: 737-752.
14. Ravikumar B, Imarisio S, Sarkar S, O'Kane CJ, Rubinsztein DC (2008) Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J Cell Sci 121: 1649-1660.
15. Li X, Standley C, Sapp E, Valencia A, Qin ZH, et al. (2009) Mutant huntingtin impairs vesicle formation from recycling endosomes by interfering with Rab11 activity. Mol Cell Biol 29: 6106-6116.
16. Li XJ, Orr AL, Li S (2010) Impaired mitochondrial trafficking in Huntington's disease. Biochim Biophys Acta 1802: 62-65.
17. Caviston JP, Holzbaur EL (2009) Huntingtin as an essential integrator of intracellular vesicular trafficking. Trends Cell Biol 19: 147-155.
18. Kazantsev AG, Hersch SM (2007) Drug targeting of dysregulated transcription in Huntington's disease. Prog Neurobiol 83: 249-259.
19. Wang CE, Tydlacka S, Orr AL, Yang SH, Graham RK, et al. (2008) Accumulation of N-terminal mutant huntingtin in mouse and monkey models implicated as a pathogenic mechanism in Huntington's disease. Hum Mol Genet 17: 2738-2751.
20. Gafni J, Hermel E, Young JE, Wellington CL, Hayden MR, et al. (2004) Inhibition of calpain cleavage of huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J Biol Chem 279: 20211-20220.
21. Graham RK, Deng Y, Slow EJ, Haigh B, Bissada N, et al. (2006) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125: 1179-1191.
22. Roze E, Saudou F, Caboche J (2008) Pathophysiology of Huntington's disease: from huntingtin functions to potential treatments. Curr Opin Neurol 21: 497-503.
23. Tydlacka S, Wang CE, Wang X, Li S, Li XJ (2008) Differential activities of the ubiquitin-proteasome system in neurons versus glia may account for the preferential accumulation of misfolded proteins in neurons. J Neurosci 28: 13285-13295.
24. Ahner A, Brodsky JL (2004) Checkpoints in ER-associated degradation: excuse me, which way to the proteasome? Trends Cell Biol 14: 474-478.
25. Rutkowski DT, Arnold SM, Miller CN, Wu J, Li J, et al. (2006) Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol 4: e374.
26. Duennwald ML, Lindquist S (2008) Impaired ERAD and ER stress are early and specific events in polyglutamine toxicity. Genes Dev 22: 3308-3319.
27. Reijonen S, Putkonen N, Norremolle A, Lindholm D, Korhonen L (2008) Inhibition of endoplasmic reticulum stress counteracts neuronal cell death and protein aggregation caused by N-terminal mutant huntingtin proteins. Exp Cell Res 314: 950-960.
28. Noh JY, Lee H, Song S, Kim NS, Im W, et al. (2009) SCAMP5 links endoplasmic reticulum stress to the accumulation of expanded polyglutamine protein aggregates via endocytosis inhibition. J Biol Chem 284: 11318-11325.
29. Carnemolla A, Fossale E, Agostoni E, Michelazzi S, Calligaris R, et al. (2009) Rrs1 is involved in endoplasmic reticulum stress response in Huntington disease. J Biol Chem 284: 18167-18173.
30. Kostova Z, Tsai YC, Weissman AM (2007) Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation. Semin Cell Dev Biol 18: 770-779.
31. Fang S, Ferrone M, Yang C, Jensen JP, Tiwari S, et al. (2001) The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc Natl Acad Sci U S A 98: 14422-14427.
32. Zhong X, Shen Y, Ballar P, Apostolou A, Agami R, et al. (2004) AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J Biol Chem 279: 45676-45684.
33. Ye Y, Shibata Y, Kikkert M, van Voorden S, Wiertz E, et al. (2005) Inaugural Article: Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 102: 14132-14138.
34. Lilley BN, Ploegh HL (2005) Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 102: 14296-14301.
35. Song BL, Sever N, DeBose-Boyd RA (2005) Gp78, a membrane-anchored ubiquitin ligase, associates with Insig-1 and couples sterol-regulated ubiquitination to degradation of HMG CoA reductase. Mol Cell 19: 829-840.
36. Li W, Tu D, Brunger AT, Ye Y (2007) A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446: 333-337.
37. Christianson JC, Shaler TA, Tyler RE, Kopito RR (2008) OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat Cell Biol 10: 272-282.
38. Mueller B, Klemm EJ, Spooner E, Claessen JH, Ploegh HL (2008) SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc Natl Acad Sci U S A 105: 12325-12330.
39. Kikkert M, Doolman R, Dai M, Avner R, Hassink G, et al. (2004) Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J Biol Chem 279: 3525-3534.
40. Ye Y, Meyer HH, Rapoport TA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414: 652-656.
41. Ye Y, Meyer HH, Rapoport TA (2003) Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J Cell Biol 162: 71-84.
42. Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429: 841-847.
43. Lilley BN, Ploegh HL (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429: 834-840.
44. Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, et al. (2008) ALSlinked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22: 1451-1464.
45. Lindholm D, Wootz H, Korhonen L (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13: 385-392.
46. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
47. Chen L, Gao X (2002) Neuronal apoptosis induced by endoplasmic reticulum stress. Neurochem Res 27: 891-898.
48. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389.
49. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
50. Homma K, Katagiri K, Nishitoh H, Ichijo H (2009) Targeting ASK1 in ER stress-related neurodegenerative diseases. Expert Opin Ther Targets 13: 653-664.
51. Yang H, Zhong X, Ballar P, Luo S, Shen Y, et al. (2007) Ubiquitin ligase Hrd1 enhances the degradation and suppresses the toxicity of polyglutamine-expanded huntingtin. Exp Cell Res 313: 538-550.
52. Ballar P, Shen Y, Yang H, Fang S (2006) The role of a novel p97/valosincontaining protein-interacting motif of gp78 in endoplasmic reticulumassociated degradation. J Biol Chem 281: 35359-35368.
53. Bays NW, Hampton RY (2002) Cdc48-Ufd1-Npl4: stuck in the middle with Ub. Curr Biol 12: R366-71.
54. Tsai B, Ye Y, Rapoport TA (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat Rev Mol Cell Biol 3: 246-255.
55. Ye Y (2006) Diverse functions with a common regulator: ubiquitin takes command of an AAA ATPase. J Struct Biol 156: 29-40.
56. Chen B, Mariano J, Tsai YC, Chan AH, Cohen M, et al. (2006) The activity of a human endoplasmic reticulum-associated degradation E3, gp78, requires its Cue domain, RING finger, and an E2-binding site. Proc Natl Acad Sci U S A 103: 341-346.
57. Morito D, Hirao K, Oda Y, Hosokawa N, Tokunaga F, et al. (2008) Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508. Mol Biol Cell 19: 1328-1336.
58. Ponting CP (2000) Proteins of the endoplasmic-reticulum-associated degradation pathway: domain detection and function prediction. Biochem J 351 Pt 2: 527-535.
59. Prag G, Misra S, Jones EA, Ghirlando R, Davies BA, et al. (2003) Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113: 609-620.
60. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
61. Zhang K, Kaufman RJ (2008) From endoplasmic-reticulum stress to the inflammatory response. Nature 454: 455-462.
62. Vembar SS, Brodsky JL (2008) One step at a time: endoplasmic reticulumassociated degradation. Nat Rev Mol Cell Biol 9: 944-957.
63. Younger JM, Chen L, Ren HY, Rosser MF, Turnbull EL, et al. (2006) Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126: 571-582.
64. Ying Z, Wang H, Fan H, Zhu X, Zhou J, et al. (2009) Gp78, an ER associated E3, promotes SOD1 and ataxin-3 degradation. Hum Mol Genet 18: 4268-4281.
65. Li W, Tu D, Li L, Wollert T, Ghirlando R, et al. (2009) Mechanistic insights into active site-associated polyubiquitination by the ubiquitin-conjugating enzyme Ube2g2. Proc Natl Acad Sci U S A 106: 3722-3727.
66. Ballar P, Ors AU, Yang H, Fang S (2010) Differential regulation of CFTRDeltaF508 degradation by ubiquitin ligases gp78 and Hrd1. Int J Biochem Cell Biol 42: 167-173.
67. Luo S, Mizuta H, Rubinsztein DC (2008) p21-activated kinase 1 promotes soluble mutant huntingtin self-interaction and enhances toxicity. Hum Mol Genet 17: 895-905.