Parkin-mediated monoubiquitination of the PDZ protein PICK1 regulates the activity of acid-sensing ion channels

Molecular Biology of the Cell

Volumn 18, Issue 8, 2007, Pages 3105-3118

  Joch, Monica ^a   Ase, Ariel R ^a   Chen, Carol X Q ^a   MacDonald, Penny A ^a   Kontogiannea, Maria ^a   Corera, Amadou T ^a   Brice, Alexis ^b   Séguéla, Philippe ^a   Fon, Edward A ^a  

^a MCGILL UNIVERSITY   (Canada)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; PARKIN; PDZ PROTEIN; PROTEASOME; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN KINASE C; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EXCITOTOXICITY; GENE MUTATION; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MOUSE; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

AMINO ACIDS; ANIMALS; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; HELA CELLS; HUMANS; ION CHANNEL GATING; MEMBRANE PROTEINS; MICE; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RATS; SODIUM CHANNELS; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

MUS;

EID: 34547780601     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-11-1027     Document Type: Article

References (68)

1. Askwith, C. C., Wemmie, J. A., Price, M. P., Rokhlina, T., and Welsh, M. J. (2004). Acid-sensing ion channel 2 (ASIC2) modulates ASIC1 H+-activated currents in hippocampal neurons. J. Biol. Chem. 279, 18296-18305.
2. Avantaggiati, M. L., Carbone, M., Graessmann, A., Nakatani, Y., Howard, B., and Levine, A. S. (1996). The SV40 large T antigen and adenovirus E1a oncoproteins interact with distinct isoforms of the transcriptional co-activator, p300. EMBO J. 15, 2236-2248.
3. Baron, A., Deval, E., Saunas, M., Lingueglia, E., Voilley, N., and Lazdunski, M. (2002a). Protein kinase C stimulates the acid-sensing ion channel ASIC2a via the PDZ domain-containing protein PICK1. J. Biol. Chem. 277, 50463-50468.
4. Baron, A., Waldmann, R., and Lazdunski, M. (2002b). ASIC-like, proton-activated currents in rat hippocampal neurons. J. Physiol. 539, 485-494.
5. Chung, K. K., Zhang, Y., Lim, K. L., Tanaka, Y., Huang, H., Gao, J., Ross, C. A., Dawson, V. L., and Dawson, T. M. (2001). Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1, implications for Lewy-body formation in Parkinson disease. Nat. Med. 7, 1144-1150.
6. Cookson, M. R. (2005). The biochemistry of Parkinson's disease. Annu. Rev. Biochem. 74, 29-52.
7. Corti, O. et al. (2003). The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration. Hum. Mol. Genet. 12, 1427-1437.
8. Dev, K. K., Nishimune, A., Henley, J. M., and Nakanishi, S. (1999). The protein kinase C alpha binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits. Neuropharmacology 38, 635-644.
9. Doss-Pepe, E. W., Chen, L., and Madura, K. (2005). Alpha-synuclein and parkin contribute to the assembly of ubiquitin lysine 63-linked multiubiquitin chains. J. Biol. Chem. 280, 16619-16624.
10. Doyle, D. A., Lee, A., Lewis, J., Kim, E., Sheng, M., and MacKinnon, R. (1996). Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85, 1067-1076.
11. Duggan, A., Garcia-Anoveros, J., and Corey, D. P. (2002). The PDZ domain protein PICK1 and the sodium channel BNaC1 interact and localize at mechanosensory terminals of dorsal root ganglion neurons and dendrites of central neurons. J. Biol. Chem. 277, 5203-5208.
12. Fallon, L. et al. (2006). A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat. Cell Biol. 8, 834-842.
13. Fallon, L., Moreau, F., Croft, B. G., Labib, N., Gu, W. J., and Fon, E. A. (2002). Parkin and CASK/LIN-2 associate via a PDZ-mediated interaction and are co-localized in lipid rafts and postsynaptic densities in brain. J. Biol. Chem. 277, 486-491.
14. Feany, M. B., and Pallanck, L. J. (2003). Parkin: a multipurpose neuroprotective agent? Neuron 38, 13-16.
15. Giasson, B. I., and Lee, V. M. (2001). Parkin and the molecular pathways of Parkinson's disease. Neuron 31, 885-888.
16. Giasson, B. I., and Lee, V. M. (2003). Are ubiquitination pathways central to Parkinson's disease? Cell 114, 1-8.
17. Goldberg, M. S. et al. (2003). Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J. Biol. Chem. 278, 43628-43635.
18. Hampe, C., Ardila-Osorio, H., Fournier, M., Brice, A., and Corti, O. (2006). Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum. Mol. Genet. 15, 2059-2075.
19. Hanley, J. G. (2006). Molecular mechanisms for regulation of AMPAR trafficking by PICK1. Biochem. Soc. Trans. 34, 931-935.
20. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
21. Hicke, L., and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
22. Hruska-Hageman, A. M., Wemmie, J. A., Price, M. P., and Welsh, M. J. (2002). Interaction of the synaptic protein PICK1 (protein interacting with C kinase 1) with the non-voltage gated sodium channels BNC1 (brain Na+ channel 1) and ASIC (acid-sensing ion channel). Biochem. J. 361, 443-450.
23. Husnjak, K., and Dikic, I. (2006). EGFR trafficking: parkin' in a jam. Nat. Cell Biol. 8, 787-788.
24. Huttner, W. B., Schiebler, W., Greengard, P., and De Camilli, P. (1983). Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374-1388.
25. Imai, Y., Soda, M., Hatakeyama, S., Akagi, T., Hashikawa, T., Nakayama, K. I., and Takahashi, R. (2002). CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol. Cell 10, 55-67.
26. Imai, Y., Soda, M., Inoue, H., Hattori, N., Mizuno, Y., and Takahashi, R. (2001). An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105, 891-902.
27. Itier, J. M. et al. (2003). Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum. Mol. Genet. 12, 2277-2291.
28. Jiang, H., Jiang, Q., and Feng, J. (2004). Parkin increases dopamine uptake by enhancing the cell surface expression of dopamine transporter. J. Biol. Chem. 279, 54380-54386.
29. Jin, W., Ge, W. P., Xu, J., Cao, M., Peng, L., Yung, W., Liao, D., Duan, S., Zhang, M., and Xia, J. (2006). Lipid binding regulates synaptic targeting of PICK1, AMPA receptor trafficking, and synaptic plasticity. J. Neurosci. 26, 2380-2390.
30. Joazeiro, C. A., and Weissman, A. M. (2000). RING finger proteins: mediators of ubiquitin ligase activity. Cell 102, 549-552.
31. Kahle, P. J., Leimer, U., and Haass, C. (2000). Does failure of parkin-mediated ubiquitination cause juvenile parkinsonism? Trends Biochem. Sci. 25, 524-527.
32. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. (1998). Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism [see comments]. Nature 392, 605-608.
33. Ko, H. S. et al. (2005). Accumulation of the authentic parkin substrate aminoacyl-tRNA synthetase cofactor, p38/JTV-1, leads to catecholaminergic cell death. J. Neurosci. 25, 7968-7978.
34. Lim, K. L. et al. (2005). Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1, implications for Lewy body formation. J. Neurosci. 25, 2002-2009.
35. Lorick, K. L., Jensen, J. P., Fang, S., Ong, A. M., Hatakeyama, S., and Weissman, A. M. (1999). RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96, 11364-11369.
36. Lu, W., and Ziff, E. B. (2005). PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron 47, 407-421.
37. Lucking, C. B. et al. (2000). Association between early-onset Parkinson's disease and mutations in the parkin gene. French Parkinson's Disease Genetics Study Group. N. Engl. J. Med. 342, 1560-1567.
38. Madsen, K. L., Beuming, T., Niv, M. Y., Chang, C. W., Dev, K. K., Weinstein, H., and Gether, U. (2005). Molecular determinants for the complex binding specificity of the PDZ domain in PICK1. J. Biol. Chem. 280, 20539-20548.
39. Matsuda, N., Kitami, T., Suzuki, T., Mizuno, Y., Hattori, N., and Tanaka, K. (2006). Diverse effects of pathogenic mutations of Parkin that catalyze multiple monoubiquitylation in vitro. J. Biol. Chem. 281, 3204-3209.
40. Miranda, M., Dionne, K. R., Sorkina, T., and Sorkin, A. (2007). Three ubiquitin conjugation sites in the amino terminus of the dopamine transporter mediate protein kinase C-dependent endocytosis of the transporter. Mol. Biol. Cell 18, 313-323.
41. Miranda, M., Wu, C. C., Sorkina, T., Korstjens, D., and Sorkin, A. (2005). Enhanced ubiquitylation and accelerated degradation of the dopamine transporter mediated by protein kinase C. J. Biol. Chem. 280, 35617-35624.
42. Moore, D. J., West, A. B., Dawson, V. L., and Dawson, T. M. (2005). Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 28, 57-87.
43. Mukhopadhyay, D., and Riezman, H. (2007). Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205.
44. Nakagawa, S., and Huibregtse, J. M. (2000). Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin- protein ligase. Mol. Cell. Biol. 20, 8244-8253.
45. Nie, J., Li, S. S., and McGlade, C. J. (2004). A novel PTB-PDZ domain interaction mediates isoform-specific ubiquitylation of mammalian Numb. J. Biol. Chem. 279, 20807-20815.
46. Perez, F. A., and Palmiter, R. D. (2005). Parkin-deficient mice are not a robust model of parkinsonism. Proc. Natl. Acad. Sci. USA 102, 2174-2179.
47. Periquet, M., Corti, O., Jacquier, S., and Brice, A. (2005). Proteomic analysis of parkin knockout mice: alterations in energy metabolism, protein handling and synaptic function. J. Neurochem. 95, 1259-1276.
48. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R., and McMahon, H. T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499.
49. Pidoplichko, V. I., and Dani, J. A. (2006). Acid-sensitive ionic channels in midbrain dopamine neurons are sensitive to ammonium, which may contribute to hyperammonemia damage. Proc. Natl. Acad. Sci. USA 103, 11376-11380.
50. Sato, A. et al. (2006). Parkin potentiates ATP-induced currents due to activation of P2X receptors in PC12 cells. J. Cell. Physiol. 209, 172-182.
51. Shimura, H. et al. (2000). Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 25, 302-305.
52. Songyang, Z., Fanning, A. S., Fu, C., Xu, J., Marfatia, S. M., Chishti, A. H., Crompton, A., Chan, A. C., Anderson, J. M., and Cantley, L. C. (1997). Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73-77.
53. Sorkina, T., Miranda, M., Dionne, K. R., Hoover, B. R., Zahniser, N. R., and Sorkin, A. (2006). RNA interference screen reveals an essential role of Nedd4-2 in dopamine transporter ubiquitination and endocytosis. J. Neurosci. 26, 8195-8205.
54. Srivastava, S. et al. (1998). Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor-binding protein ABP. Neuron 21, 581-591.
55. Staropoli, J. F., McDermott, C., Martinat, C., Schulman, B., Demireva, E., and Abeliovich, A. (2003). Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 37, 735-749.
56. Staub, O., Gautschi, I., Ishikawa, T., Breitschopf, K., Ciechanover, A., Schild, L., and Rotin, D. (1997). Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J. 16, 6325-6336.
57. Staudinger, J., Lu, J., and Olson, E. N. (1997). Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J. Biol. Chem. 272, 32019-32024.
58. Staudinger, J., Zhou, J., Burgess, R., Elledge, S. J., and Olson, E. N. (1995). PICK1, a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J. Cell Biol. 128, 263-271.
59. Torres, G. E., Yao, W. D., Mohn, A. R., Quan, H., Kim, K. M., Levey, A. I., Staudinger, J., and Caron, M. G. (2001). Functional interaction between monoamine plasma membrane transporters and the synaptic PDZ domain-containing protein PICK1. Neuron 30, 121-134.
60. Voges, D., Zwickl, P., and Baumeister, W. (1999). The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015-1068.
61. Von Coelln, R., Thomas, B., Savitt, J. M., Lim, K. L., Sasaki, M., Hess, E. J., Dawson, V. L., and Dawson, T. M. (2004). Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proc. Natl. Acad. Sci. USA 101, 10744-10749.
62. Wemmie, J. A., Askwith, C. C., Lamani, E., Cassell, M. D., Freeman, J. H., Jr., and Welsh, M. J. (2003). Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J. Neurosci. 23, 5496-5502.
63. Wemmie, J. A. et al. (2002). The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 34, 463-477.
64. Williams, M. E., Wu, S. C., McKenna, W. L., and Hinck, L. (2003). Surface expression of the netrin receptor UNC5H1 is regulated through a protein kinase C-interacting protein/protein kinase-dependent mechanism. J. Neurosci. 23, 11279-11288.
65. Winklhofer, K. F., Henn, I. H., Kay-Jackson, P. C., Heller, U., and Tatzeit, J. (2003). Inactivation of parkin by oxidative stress and C-terminal truncations: a protective role of molecular chaperones. J. Biol. Chem. 278, 47199-47208.
66. Xia, J., Zhang, X., Staudinger, J., and Huganir, R. L. (1999). Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22, 179-187.
67. Xiong, Z. G. et al. (2004). Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118, 687-698.
68. Zhang, Y., Gao, J., Chung, K. K., Huang, H., Dawson, V. L., and Dawson, T. M. (2000). Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl. Acad. Sci. USA 97, 13354-13359.