The Direction of Protein Entry into the Proteasome Determines the Variety of Products and Depends on the Force Needed to Unfold Its Two Termini

Molecular Cell

Volumn 48, Issue 4, 2012, Pages 601-611

  Berko, Dikla ^a   Tabachnick Cherny, Shira ^a   Shental Bechor, Dalit ^a   Cascio, Paolo ^b   Mioletti, Silvia ^b   Levy, Yaakov ^a   Admon, Arie ^c   Ziv, Tamar ^c   Tirosh, Boaz ^d   Goldberg, Alfred L ^e   Navon, Ami ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF TURIN   (Italy)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA 26S; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEASOME;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; IMMUNE SYSTEM; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN UNFOLDING;

ANIMALS; CALMODULIN; CASEINS; CELL LINE, TUMOR; MALTOSE-BINDING PROTEINS; MICE; OVALBUMIN; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; PROTEIN UNFOLDING; PROTEINS;

ARCHAEA; MAMMALIA;

EID: 84870393391     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.08.029     Document Type: Article

References (35)

1. Beskow A., Grimberg K.B., Bott L.C., Salomons F.A., Dantuma N.P., Young P. A conserved unfoldase activity for the p97 AAA-ATPase in proteasomal degradation. J. Mol. Biol. 2009, 394:732-746.
2. Cascio P., Hilton C., Kisselev A.F., Rock K.L., Goldberg A.L. 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J. 2001, 20:2357-2366.
3. Cascio P., Call M., Petre B.M., Walz T., Goldberg A.L. Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. EMBO J. 2002, 21:2636-2645.
4. Drori A., Misaghi S., Haimovich J., Messerle M., Tirosh B. Prolonged endoplasmic reticulum stress promotes mislocalization of immunoglobulins to the cytoplasm. Mol. Immunol. 2010, 47:1719-1727.
5. Chen X., Chi Y., Bloecher A., Aebersold R., Clurman B.E., Roberts J.M. N-acetylation and ubiquitin-independent proteasomal degradation of p21(Cip1). Mol. Cell 2004, 16:839-847.
6. Groll M., Ditzel L., Löwe J., Stock D., Bochtler M., Bartunik H.D., Huber R. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 1997, 386:463-471.
7. Groll M., Bajorek M., Köhler A., Moroder L., Rubin D.M., Huber R., Glickman M.H., Finley D. A gated channel into the proteasome core particle. Nat. Struct. Biol. 2000, 7:1062-1067.
8. Hagai T., Levy Y. Ubiquitin not only serves as a tag but also assists degradation by inducing protein unfolding. Proc. Natl. Acad. Sci. USA 2010, 107:2001-2006.
9. Hoppe T., Matuschewski K., Rape M., Schlenker S., Ulrich H.D., Jentsch S. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 2000, 102:577-586.
10. Howarth M., Williams A., Tolstrup A.B., Elliott T. Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc. Natl. Acad. Sci. USA 2004, 101:11737-11742.
11. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 1996, 14:33-38. 27-28.
12. Kisselev A.F., Akopian T.N., Goldberg A.L. Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes. J. Biol. Chem. 1998, 273:1982-1989.
13. Kisselev A.F., Akopian T.N., Woo K.M., Goldberg A.L. The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem. 1999, 274:3363-3371.
14. Köhler A., Cascio P., Leggett D.S., Woo K.M., Goldberg A.L., Finley D. The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Mol. Cell 2001, 7:1143-1152.
15. Kuboniwa H., Tjandra N., Grzesiek S., Ren H., Klee C.B., Bax A. Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 1995, 2:768-776.
16. Liu C.W., Corboy M.J., DeMartino G.N., Thomas P.J. Endoproteolytic activity of the proteasome. Science 2003, 299:408-411.
17. Löwe J., Stock D., Jap B., Zwickl P., Baumeister W., Huber R. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 1995, 268:533-539.
18. Löwe J., Stock D., Jap B., Zwickl P., Baumeister W., Huber R. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 1995, 268:533-539.
19. Medalia N., Beer A., Zwickl P., Mihalache O., Beck M., Medalia O., Navon A. Architecture and molecular mechanism of PAN, the archaeal proteasome regulatory ATPase. J. Biol. Chem. 2009, 284:22952-22960.
20. Navon A., Goldberg A.L. Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol. Cell 2001, 8:1339-1349.
21. Peth A., Uchiki T., Goldberg A.L. ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol. Cell 2010, 40:671-681.
22. Porgador A., Yewdell J.W., Deng Y., Bennink J.R., Germain R.N. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997, 6:715-726.
23. Prakash S., Tian L., Ratliff K.S., Lehotzky R.E., Matouschek A. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 2004, 11:830-837.
24. Rabl J., Smith D.M., Yu Y., Chang S.C., Goldberg A.L., Cheng Y. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 2008, 30:360-368.
25. Rock K.L., Goldberg A.L. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 1999, 17:739-779.
26. Rock K.L., York I.A., Saric T., Goldberg A.L. Protein degradation and the generation of MHC class I-presented peptides. Adv. Immunol. 2002, 80:1-70.
27. Rock K.L., York I.A., Goldberg A.L. Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat. Immunol. 2004, 5:670-677.
28. Ruschak A.M., Religa T.L., Breuer S., Witt S., Kay L.E. The proteasome antechamber maintains substrates in an unfolded state. Nature 2010, 467:868-871.
29. Shabek N., Herman-Bachinsky Y., Ciechanover A. Ubiquitin degradation with its substrate, or as a monomer in a ubiquitination-independent mode, provides clues to proteasome regulation. Proc. Natl. Acad. Sci. USA 2009, 106:11907-11912.
30. Shen L., Rock K.L. Cellular protein is the source of cross-priming antigen in vivo. Proc. Natl. Acad. Sci. USA 2004, 101:3035-3040.
31. Smith D.M., Kafri G., Cheng Y., Ng D., Walz T., 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 2005, 20:687-698.
32. Swaisgood H.E. Chemistry of caseins. Advanced Dairy Chemistry, Volume 1: Proteins Part A 2003, 139-202. Springer, New York. P.F. Fox, P.L.H. McSweeney (Eds.).
33. Takeuchi J., Chen H., Coffino P. Proteasome substrate degradation requires association plus extended peptide. EMBO J. 2007, 26:123-131.
34. Tani F., Shirai N., Onishi T., Venelle F., Yasumoto K., Doi E. Temperature control for kinetic refolding of heat-denatured ovalbumin. Protein Sci. 1997, 6:1491-1502.
35. Whitby F.G., Masters E.I., Kramer L., Knowlton J.R., Yao Y., Wang C.C., Hill C.P. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 2000, 408:115-120.