An Arsenite-Inducible 19S Regulatory Particle-Associated Protein Adapts Proteasomes to Proteotoxicity

Molecular Cell

Volumn 23, Issue 6, 2006, Pages 875-885

  Stanhill, Ariel ^a   Haynes, Cole M ^a   Zhang, Yuhong ^a   Min, Guangwei ^a   Steele, Matthew C ^b   Kalinina, Juliya ^a   Martinez, Enid ^a   Pickart, Cecile M ^b   Kong, Xiang Peng ^a   Ron, David ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

PROTEINS

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARSENIC TRIOXIDE; GENE PRODUCT; GLUTATHIONE TRANSFERASE; POLYUBIQUITIN; PROTEASOME; PROTEIN AIRAP; TRYPSIN; UNCLASSIFIED DRUG;

AIRAP GENE; ANIMAL CELL; ARTICLE; AUTORADIOGRAPHY; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENZYME SUBSTRATE; GENE; KNOCKOUT MOUSE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN FOLDING; RNA INTERFERENCE; STRESS; UBIQUITINATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ARSENITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE; HEAT-SHOCK RESPONSE; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN SUBUNITS; RNA-BINDING PROTEINS; UBIQUITIN;

CAENORHABDITIS ELEGANS;

EID: 33748439489     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.07.023     Document Type: Article

References (48)

1. Abernathy C.O., Liu Y.P., Longfellow D., Aposhian H.V., Beck B., Fowler B., Goyer R., Menzer R., Rossman T., Thompson C., and Waalkes M. Arsenic: health effects, mechanisms of actions, and research issues. Environ. Health Perspect. 107 (1999) 593-597
2. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M., and Cook J.L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274 (1999) 26071-26078
3. An J.H., and Blackwell T.K. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17 (2003) 1882-1893
4. Aposhian H.V. Biochemical toxicology of arsenic. Rev J. Biochem. Toxicol. 10 (1989) 265-299
5. Bence N.F., Sampat R.M., and Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292 (2001) 1552-1555
6. Berleth E.S., Kasperek E.M., Grill S.P., Braunscheidel J.A., Graziani L.A., and Pickart C.M. Inhibition of ubiquitin-protein ligase (E3) by mono- and bifunctional phenylarsenoxides. Evidence for essential vicinal thiols and a proximal nucleophile. J. Biol. Chem. 267 (1992) 16403-16411
7. Bhattacharjee H., and Rosen B.P. Spatial proximity of Cys113, Cys172, and Cys422 in the metalloactivation domain of the ArsA ATPase. J. Biol. Chem. 271 (1996) 24465-24470
8. Bhattacharjee H., Li J., Ksenzenko M., and Rosen B. Role of cysteinyl residues in metalloactivation of the oxyanion-translocating ArsA ATPase. J. Biol. Chem. 270 (1995) 11245-11250
9. Bond U., Agell N., Haas A.L., Redman K., and Schlesinger M.J. Ubiquitin in stressed chicken embryo fibroblasts. J. Biol. Chem. 263 (1988) 2384-2388
10. Braun B.C., Glickman M., Kraft R., Dahlmann B., Kloetzel P.M., Finley D., and Schmidt M. The base of the proteasome regulatory particle exhibits chaperone-like activity. Nat. Cell Biol. 1 (1999) 221-226
11. Casagrande R., Stern P., Diehn M., Shamu C., Osario M., Zuniga M., Brown P.O., and Ploegh H. Degradation of proteins from the ER of S. cerevisiae requires an intact unfolded protein response pathway. Mol. Cell 5 (2000) 729-735
12. Cascio P., Call M., Petre B.M., Walz T., and Goldberg A.L. Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. EMBO J. 21 (2002) 2636-2645
13. Elsasser S., and Finley D. Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol. 7 (2005) 742-749
14. Elsasser S., Gali R.R., Schwickart M., Larsen C.N., Leggett D.S., Muller B., Feng M.T., Tubing F., Dittmar G.A., and Finley D. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4 (2002) 725-730
15. Eytan E., Ganoth D., Armon T., and Hershko A. ATP-dependent incorporation of 20S protease into the 26S complex that degrades proteins conjugated to ubiquitin. Proc. Natl. Acad. Sci. USA 86 (1989) 7751-7755
16. Gamer J., Bujard H., and Bukau B. Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32. Cell 69 (1992) 833-842
17. Glickman M., and Coux O. Purification and characterization of proteasomes from Saccharomyces cerevisiae. In: Coligan J.E., Dunn B.M., Speicher D.W., and Wingfield P.T. (Eds). Current Protocols in Protein Science (2001), John Wiley & Sons, New York 21.5.5-22.5.12
18. Goellner G.M., and Rechsteiner M. Are Huntington's and polyglutamine-based ataxias proteasome storage diseases?. Int. J. Biochem. Cell Biol. 35 (2003) 562-571
19. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 426 (2003) 895-899
20. Gong P., Stewart D., Hu B., Vinson C., and Alam J. Multiple basic-leucine zipper proteins regulate induction of the mouse heme oxygenase-1 gene by arsenite. Arch. Biochem. Biophys. 405 (2002) 265-274
21. Hershko A., and Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67 (1998) 425-479
22. Holmberg C.I., Staniszewski K.E., Mensah K.N., Matouschek A., and Morimoto R.I. Inefficient degradation of truncated polyglutamine proteins by the proteasome. EMBO J. 23 (2004) 4307-4318
23. Inoue H., Hisamoto N., An J.H., Oliveira R.P., Nishida E., Blackwell T.K., and Matsumoto K. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev. 19 (2005) 2278-2283
24. Johnston D., Oppermann H., Jackson J., and Levinson W. Induction of four proteins in chick embryo cells by sodium arsenite. J. Biol. Chem. 255 (1980) 6975-6980
25. Kirkpatrick D.S., Dale K.V., Catania J.M., and Gandolfi A.J. Low-level arsenite causes accumulation of ubiquitinated proteins in rabbit renal cortical slices and HEK293 cells. Toxicol. Appl. Pharmacol. 186 (2003) 101-109
26. Klemperer N.S., Berleth E.S., and Pickart C.M. A novel, arsenite-sensitive E2 of the ubiquitin pathway: purification and properties. Biochemistry 28 (1989) 6035-6041
27. Levinson W., Oppermann H., and Jackson J. Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim. Biophys. Acta 606 (1980) 170-180
28. Ludtke S.J., Baldwin P.R., and Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128 (1999) 82-97
29. Marciniak S.J., Yun C.Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., Nagata K., Harding H.P., and Ron D. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18 (2004) 3066-3077
30. Morimoto R.I. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12 (1998) 3788-3796
31. Navon A., and Goldberg A.L. Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol. Cell 8 (2001) 1339-1349
32. Orino E., Tanaka K., Tamura T., Sone S., Ogura T., and Ichihara A. ATP-dependent reversible association of proteasomes with multiple protein components to form 26S complexes that degrade ubiquitinated proteins in human HL-60 cells. FEBS Lett. 284 (1991) 206-210
33. Pickart C.M., and Cohen R.E. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell Biol. 5 (2004) 177-187
34. Rao H., and Sastry A. Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. J. Biol. Chem. 277 (2002) 11691-11695
35. Rechsteiner M., and Hill C.P. Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol. 15 (2005) 27-33
36. Skarnes W.C., von Melchner H., Wurst W., Hicks G., Nord A.S., Cox T., Young S.G., Ruiz P., Soriano P., Tessier-Lavigne M., et al. A public gene trap resource for mouse functional genomics. Nat. Genet. 36 (2004) 543-544
37. Smith D.M., Kafri G., Cheng Y., Ng D., Walz T., and Goldberg A.L. ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol. Cell 20 (2005) 687-698
38. Sok J., Calfon M., Lu J., Lichtlen P., Clark S., and Ron D. Arsenite-inducible RNA-associated protein (AIRAP) protects cells from arsenite toxicity. Cell Stress Chaperones 6 (2001) 6-15
39. Tanaka K., and Tsurumi C. The 26S proteasome: subunits and functions. Mol. Biol. Rep. 24 (1997) 3-11
40. Tchounwou P.B., Patlolla A.K., and Centeno J.A. Carcinogenic and systemic health effects associated with arsenic exposure-a critical review. Toxicol. Pathol. 31 (2003) 575-588
41. Thrower J.S., Hoffman L., Rechsteiner M., and Pickart C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19 (2000) 94-102
42. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., and Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101 (2000) 249-258
43. Verma R., Oania R., Graumann J., and Deshaies R.J. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118 (2004) 99-110
44. Whitby F.G., Masters E.I., Kramer L., Knowlton J.R., Yao Y., Wang C.C., and Hill C.P. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408 (2000) 115-120
45. Yang Y., Fruh K., Ahn K., and Peterson P.A. In vivo assembly of the proteasomal complexes, implications for antigen processing. J. Biol. Chem. 270 (1995) 27687-27694
46. Ye Y., Shibata Y., Yun C., Ron D., and Rapoport T.A. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429 (2004) 841-847
47. Zhang M., Pickart C.M., and Coffino P. Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. EMBO J. 22 (2003) 1488-1496
48. Zheng P.Z., Wang K.K., Zhang Q.Y., Huang Q.H., Du Y.Z., Zhang Q.H., Xiao D.K., Shen S.H., Imbeaud S., Eveno E., et al. Systems analysis of transcriptome and proteome in retinoic acid/arsenic trioxide-induced cell differentiation/apoptosis of promyelocytic leukemia. Proc. Natl. Acad. Sci. USA 102 (2005) 7653-7658