Ataxin-3 interactions with Rad23 and valosin-containing protein and its associations with ubiquitin chains and the proteasome are consistent with a role in ubiquitin-mediated proteolysis

Molecular and Cellular Biology

Volumn 23, Issue 18, 2003, Pages 6469-6483

  Doss Pepe, Ellen W ^a   Stenroos, Edward S ^b   Johnson, William G ^b   Madura, Kiran ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 3; PROTEASOME; PROTEIN; RAD23 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MACHADO JOSEPH DISEASE; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; TRINUCLEOTIDE REPEAT;

ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEINS; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; GLUTAMINE; HUMANS; MACHADO-JOSEPH DISEASE; MACROMOLECULAR SUBSTANCES; MULTIENZYME COMPLEXES; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; PROTEINS; REPRESSOR PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION; UBIQUITIN; YEASTS;

EID: 0042691818     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.18.6469-6483.2003     Document Type: Article

References (52)

1. Bachmair, A., D. Finley, and A. Varshavsky. 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234:179-186.
2. Baniahmad, C., A. Baniahmad, and B. W. O'Malley. 1994. A rapid method combining a functional test of fusion proteins in vivo and their purification. BioTechniques 16:194-196.
3. Bence, N. F., R. M. Sampat, and R. R. Kopito. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-1555.
4. Bertolaet, B. L., D. J. Clarke, M. Wolff, M. H. Watson, M. Henze, G. Divita, and S. I. Reed. 2001. UBA domains of DNA damage-inducible proteins interact with ubiquitin. Nat. Struct. Biol. 8:417-422.
5. Chan, V., J. W. Tobias, A. Bachmair, D. Marriott, D. J. Ecker, D. K. Gonda, and A. Varshavsky. 1989. A multi-ubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243:1576-1583.
6. Chen, L., and K. Madura. 2002. Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol. Cell. Biol. 22:4902-4913.
7. Chen, L., U. Shinde, T. G. Ortolan, and K. Madura. 2001. Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Rep. 2:933-938.
8. Cummings, C. J., M. A. Mancini, B. Antalffy, D. B. DeFranco, H. T. Orr, and H. Y. Zoghbi. 1998. Chaperone suppression of aggregation and altered sub-cellular proteasome localization imply protein misfolding in SCA1. Nat. Genet. 19:148-154.
9. Dai, R.-M., E. Chen, D. Longo, C. Gorbea, and C-C Li. 1998. Involvement of valosin-containing protein, an ATPase co-purified with IκBα and 26S proteasome, in ubiquitin-proteasome-mediated degradation of IκBα. J. Biol. Chem. 273:3562-3573.
10. Dai, R.-M., and C-C Li. 2001. Valosin-containing protein is a multi-ubiquitin chain targeting factor required in ubiquitin-proteasome degradation. Nat. Cell Biol. 3:740-744.
11. De Mot, R., I. Nagy, J. Walz, and W. Baumeister. 1999. Proteasomes and other self-compartmentalizing proteases in prokaryotes. Trends Microbiol. 7:88-92.
12. Deveraux, Q., V. Ustrell, C. Pickart, and M. Rechsteiner. 1994. A 26S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269:7059-7061.
13. Evidente, V. G., K. A. Gwinn-Hardy, J. N. Caviness, and S. Gilman. 2000. Hereditary ataxias. Mayo Clin. Proc. 75:475-490.
14. Ghislain, M., J. Dohmen, F. Levy, and A. Varshavsky. 1996. CDC48p interacts with Ufd3p, a WD repeat protein required for ubiquitin-mediated proteolysis in Saccharomyces cerevisiae. EMBO J. 15:4884-4889.
15. Gonda, D. K., A. Bachmair, I. Wunning, J. W. Tobias, W. S. Lane, and A. Varshavsky. 1989. Universality and structure of the N-end rule. J. Biol. Chem. 264:16700-16712.
16. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
17. Higashiyama, H., F. Hirose, M. Yamaguchi, Y. H. Inoue, N. Fujikake, A. Matsukage, and A. Kakizuka. 2002. Identification of ter94, Drosophila VCP, as a modulator of polyglutamine-induced neurodegeneration. Cell Death Differ. 9:264-273.
18. Hirabayashi, M., K. Inoue, K. Tanaka, K. Nakadate, Y. Ohsawa, Y. Kamei, A. H. Popiel, A. Sinohara, A. Iwamatsu, Y. Kimura, Y. Uchiyama, S. Hori, and A. Kakizuka. 2001. VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ. 8:977-984.
19. Hiyama, H., M. Yokoi, C. Masutani, K. Sugasawa, T. Maekawa, K. Tanaka, J. H. Hoeijmakers, and F. Hanaoka. 1999. Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26S proteasome. J. Biol. Chem. 274:28019-28025.
20. Hofmann, K., and L. Falquet. 2001. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26:347-350.
21. Jarosch, E., C. Taxis, C. Volkwein, J. Bordallo, D. Finley, D. H. Wolf, and T. Sommer. 2002. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 4:134-139.
22. Johnson, E. S., B. Bartel, W. Seufert, and A. Varshavsky. 1992. Ubiquitin as a degradation signal. EMBO J. 11:497-505.
23. Johnson, E. S., P. C. M. Ma, I. M. Ota, and A. Varshavsky. 1995. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem. 270:17442-17456.
24. Kawaguchi, Y., T. Okamoto, M. Taniwaki, M. Aizawa, M. Inoue, S. Katayama, H. Kawakami, S. Nakamura, M. Nishimura, I. Akiguchi, et al. 1994. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat. Genet. 8:221-228.
25. Klockgether, T., U. Wullner, A. Spauschus, and B. Evert. 2000. The molecular biology of the autosomal-dominant cerebellar ataxias. Mov. Disord. 15:604-612.
26. Kobayashi, T., K. Tanaka, K. Inoue, and A. Kakizuka. 2002. Functional ATPase activity of p97/VCP is required for the quality control of endoplasmic reticulum in neuronally differentiated mammalian PC12 cells. J. Biol. Chem. 277:47358-47365.
27. Koller, K. J., and M. J. Brownstein. 1987. Use of a cDNA clone to identify a supposed precursor protein containing valosin. Nature 325:542-545.
28. Lam, Y. A., T. G. Lawson, M. Velayutham, J. L. Zweier, and C. M. Pickart. 2002. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416:763-767.
29. Lambertson, D., L. Chen, and K. Madura. 1999. Pleiotropic defects caused by loss of the proteasome-interacting factors Rad23 and Rpn10 of Saccharomyces cerevisiae. Genetics 153:69-79.
30. Larsen, C. N., and D. Finley. 1997. Protein translocation channels in the proteasome and other proteases. Cell 91:431-434.
31. Madura, K. 2002. The ubiquitin-associated (UBA) domain: on the path from prudence to prurience. Cell Cycle 1:235-244.
32. Merrick, W. C. 1979. Assays for eukaryotic protein synthesis. Methods Enzymol. 60:108-123.
33. Meyer, H. H., Y. Wang, and G. Warren. 2002. Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Np14. EMBO J. 21:5645-5652.
34. Ortolan, T. G., P. Tongaonkar, D. Lambertson, L. Chen, C. Schauber, and K. Madura. 2000. The DNA repair protein Rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat. Cell Biol. 2:601-608.
35. Patel, S., and M. Latterich. 1998. The AAA team: related ATPases with diverse functions. Trends Cell Biol. 8:65-71.
36. Paulson, H. L. 1998. Analysis of triplet repeat disorders: spinocerebellar ataxia type 3/Machado Joseph disease. BIOS Scientific Publishers, Oxford, United Kingdom.
37. Paulson, H. L., M. K. Perez, Y. Trottier, J. Q. Trojanowski, S. H. Subramony, S. S. Das, P. Vig, J. L. Mandel, K. H. Fischbeek, and R. N. Pittman. 1997. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 19:333-344.
38. Raasi, S., and C. M. Pickart. 2003. Rad23 ubiquitin-associated domains (UBA) inhibit 26S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J. Biol. Chem. 278:8951-8959.
39. Rao, H., and A. Sastry. 2002. Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J. Biol. Chem. 277:11691-11695.
40. Rosenberg, R. 1992. Machado-Joseph disease: an autosomal dominant system degeneration. Mov. Disord. 3:193-203.
41. Schauber, C., L. Chen, P. Tongaonkar, I. Vega, D. Lambertson, W. Potts, and K. Madura. 1998. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391:715-718.
42. Schmidt, T., K. S. Lindenberg, A. Krebs, L. Schols, F. Laccone, J. Herms, M. Rechsteiner, O. Riess, and G. B. Landwehrmeyer. 2002. Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann. Neurol. 51:302-310.
43. Thrower, J. S., L. Hoffman, M. Rechsteiner, and C. M. Pickart. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19:94-102.
44. Turner, G. C., and A. Varshavsky. 2000. Detecting and measuring cotranslational protein degradation in vivo. Science 289:2117-2120.
45. van Nocker, S., S. Sadis, D. M. Rubin, M. Glickman, H. Fu, O. Coux, I. Wefes, D. Finley, and R. D. Vierstra. 1996. The multi-ubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turn-over. Mol. Cell. Biol. 16:6020-6028.
46. Verma, R., S. Chen, R. Feldman, D. Schieltz, J. Yates, J. Dohmen, and R. J. Deshaies. 2000. Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. Mol. Biol. Cell 11:3425-3439.
47. Verma, R., and R. J. DeShaies. 2000. A proteasome howdunit: the case of the missing signal. Cell 101:341-344.
48. Voges, D., P. Zwicki, and W. Baumeister. 1999. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68:1015-1068.
49. Wang, G.-H., N. Sawai, S. Kotliarova, I. Kanazawa, and N. Nukina. 2000. Ataxin-3, the MJD1 gene product, interacts with the two human homologs of yeast DNA repair protein RAD23, HHR23A and HHR23B. Hum. Mol. Genet. 9:1795-1803.
50. Wilkinson, C. R., M. Seeger, R. Hartmann-Petersen, M. Stone, M. Wallace, C. Semple, and C. Gordon. 2001. Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat. Cell Biol. 3:939-943.
51. Yoshizawa, T., Y. Yamagishi, N. Koseki, J. Goto, H. Yoshida, F. Shibasaki, S. Shoji, and I. Kanazawa. 2000. Cell cycle arrest enhances the in vitro cellular toxicity of the truncated Machado-Joseph disease gene product with an expanded polyglutamine stretch. Hum. Mol. Genet. 9:69-78.
52. Young, P., Q. Deveraux, R. Beal, C. Pickart, and M. Rechsteiner. 1998. Characterization of the two polyubiquitin binding sites in the 26S protease subunit 5a. J. Biol. Chem. 273:5461-5467.