Ubiquitin-independent proteasomal degradation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 1, 2014, Pages 216-221

  Erales, Jenny ^a   Coffino, Philip ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Degradation; Degron; Intrinsically disordered proteins; Ornithine decarboxylase; Proteasome; Protein disorder; Rpn4; Thymidylate synthase; Ubiquitin

Indexed keywords

ORNITHINE DECARBOXYLASE; POLYAMINE; PROTEASOME; THYMIDYLATE SYNTHASE; UBIQUITIN;

ACETYLATION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; RETICULOCYTE LYSATE; REVIEW;

EID: 84890174353     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.05.008     Document Type: Review

References (72)

1. Hoyt M., Coffino P. Ubiquitin independent mechanisms of substrate recognition and degradation by the proteasome. Protein Degradation: The Ubiquitin-Proteasome System and Disease 2008, vol. 4:107-122. Wiley-VCH, Weinheim.
2. Jariel-Encontre I., Bossis G., Piechaczyk M. Ubiquitin-independent degradation of proteins by the proteasome. Biochim. Biophys. Acta 2008, 1786:153-177.
3. Hoyt M.A., Coffino P. Ubiquitin-free routes into the proteasome. Cell. Mol. Life Sci. 2004, 61:1596-1600.
4. Verma R., Deshaies R.J. A proteasome howdunit: the case of the missing signal. Cell 2000, 101:341-344.
5. Mannhaupt G., Schnall R., Karpov V., Vetter I., Feldmann H. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett. 1999, 450:27-34.
6. Xie Y., Varshavsky A. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3056-3061.
7. Ju D., Xie Y. Identification of the preferential ubiquitination site and ubiquitin-dependent degradation signal of Rpn4. J. Biol. Chem. 2006, 281:10657-10662.
8. Ju D., Xie Y. Proteasomal degradation of RPN4 via two distinct mechanisms, ubiquitin-dependent and -independent. J. Biol. Chem. 2004, 279:23851-23854.
9. Ha S.W., Ju D., Xie Y. The N-terminal domain of Rpn4 serves as a portable ubiquitin-independent degron and is recognized by specific 19S RP subunits. Biochem. Biophys. Res. Commun. 2012.
10. Kitchens M.E., Forsthoefel A.M., Rafique Z., Spencer H.T., Berger F.G. Ligand-mediated induction of thymidylate synthase occurs by enzyme stabilization. Implications for autoregulation of translation. J. Biol. Chem. 1999, 274:12544-12547.
11. Forsthoefel A.M., Pena M.M., Xing Y.Y., Rafique Z., Berger F.G. Structural determinants for the intracellular degradation of human thymidylate synthase. Biochemistry 2004, 43:1972-1979.
12. Melo S.P., Yoshida A., Berger F.G. Functional dissection of the N-terminal degron of human thymidylate synthase. Biochem. J. 2010, 432:217-226.
13. Almog R., Waddling C.A., Maley F., Maley G.F., Van Roey P. Crystal structure of a deletion mutant of human thymidylate synthase Delta (7-29) and its ternary complex with Tomudex and dUMP. Protein Sci. 2001, 10:988-996.
14. Pena M.M., Xing Y.Y., Koli S., Berger F.G. Role of N-terminal residues in the ubiquitin-independent degradation of human thymidylate synthase. Biochem. J. 2006, 394:355-363.
15. Pena M.M., Melo S.P., Xing Y.Y., White K., Barbour K.W., Berger F.G. The intrinsically disordered N-terminal domain of thymidylate synthase targets the enzyme to the ubiquitin-independent proteasomal degradation pathway. J. Biol. Chem. 2009, 284:31597-31607.
16. Melo S.P., Barbour K.W., Berger F.G. Cooperation between an intrinsically disordered region and a helical segment is required for ubiquitin-independent degradation by the proteasome. J. Biol. Chem. 2011, 286:36559-36567.
17. van Daalen Wetters T., Brabant M., Coffino P. Regulation of mouse ornithine decarboxylase activity by cell growth, serum and tetradecanoyl phorbol acetate is governed primarily by sequences within the coding region of the gene. Nucleic Acids Res. 1989, 17:9843-9860.
18. van Daalen Wetters T., Macrae M., Brabant M., Sittler A., Coffino P. Polyamine-mediated regulation of mouse ornithine decarboxylase is posttranslational. Mol. Cell. Biol. 1989, 9:5484-5490.
19. Russell D.H., Snyder S.H. Amine synthesis in regenerating rat liver: extremely rapid turnover of ornithine decarboxylase. Mol. Pharmacol. 1969, 5:253-262.
20. Macrae M., Coffino P. Complementation of a polyamine-deficient Escherichia coli mutant by expression of mouse ornithine decarboxylase. Mol. Cell. Biol. 1987, 7:564-567.
21. Ghoda L., van Daalen Wetters T., Macrae M., Ascherman D., Coffino P. Prevention of rapid intracellular degradation of ODC by a carboxyl-terminal truncation. Science 1989, 243:1493-1495.
22. Ghoda L., Phillips M.A., Bass K.E., Wang C.C., Coffino P. Trypanosome ornithine decarboxylase is stable because it lacks sequences found in the carboxyl terminus of the mouse enzyme which target the latter for intracellular degradation. J. Biol. Chem. 1990, 265:11823-11826.
23. Li X., Zhao X., Fang Y., Jiang X., Duong T., Fan C., Huang C.C., Kain S.R. Generation of destabilized green fluorescent protein as a transcription reporter. J. Biol. Chem. 1998, 273:34970-34975.
24. Li X., Coffino P. Regulated degradation of ornithine decarboxylase requires interaction with the polyamine-inducible protein antizyme. Mol. Cell. Biol. 1992, 12:3556-3562.
25. Li X., Coffino P. Degradation of ornithine decarboxylase: exposure of the C-terminal target by a polyamine-inducible inhibitory protein. Mol. Cell. Biol. 1993, 13:2377-2383.
26. Zhu C., Lang D.W., Coffino P. Antizyme2 is a negative regulator of ornithine decarboxylase and polyamine transport. J. Biol. Chem. 1999, 274:26425-26430.
27. Li X., Coffino P. Distinct domains of antizyme required for binding and proteolysis of ornithine decarboxylase. Mol. Cell. Biol. 1994, 14:87-92.
28. Palanimurugan R., Scheel H., Hofmann K., Dohmen R.J. Polyamines regulate their synthesis by inducing expression and blocking degradation of ODC antizyme. EMBO J. 2004, 23:4857-4867.
29. Godderz D., Schafer E., Palanimurugan R., Dohmen R.J. The N-terminal unstructured domain of yeast ODC functions as a transplantable and replaceable ubiquitin-independent degron. J. Mol. Biol. 2011, 407:354-367.
30. McConlogue L., Coffino P. A mouse lymphoma cell mutant whose major protein product is ornithine decarboxylase. J. Biol. Chem. 1983, 258:12083-12086.
31. McConlogue L., Gupta M., Wu L., Coffino P. Molecular cloning and expression of the mouse ornithine decarboxylase gene. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:540-544.
32. Kahana C., Nathans D. Isolation of cloned cDNA encoding mammalian ornithine decarboxylase. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:3645-3649.
33. Bercovich Z., Rosenberg-Hasson Y., Ciechanover A., Kahana C. Degradation of ornithine decarboxylase in reticulocyte lysate is ATP-dependent but ubiquitin-independent. J. Biol. Chem. 1989, 264:15949-15952.
34. Rosenberg-Hasson Y., Bercovich Z., Ciechanover A., Kahana C. Degradation of ornithine decarboxylase in mammalian cells is ATP dependent but ubiquitin independent. Eur. J. Biochem. 1989, 185:469-474.
35. Murakami Y., Matsufuji S., Kameji T., Hayashi S., Igarashi K., Tamura T., Tanaka K., Ichihara A. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 1992, 360:597-599.
36. Zhang M., Pickart C.M., Coffino P. Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. EMBO J. 2003, 22:1488-1496.
37. Takeuchi J., Chen H., Hoyt M.A., Coffino P. Structural elements of the ubiquitin-independent proteasome degron of ornithine decarboxylase. Biochem. J. 2008, 410:401-407.
38. 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.
39. Takeuchi J., Chen H., Coffino P. Proteasome substrate degradation requires association plus extended peptide. EMBO J. 2007, 26:123-131.
40. Janse D.M., Crosas B., Finley D., Church G.M. Localization to the proteasome is sufficient for degradation. J. Biol. Chem. 2004, 279:21415-21420.
41. Almrud J.J., Oliveira M.A., Kern A.D., Grishin N.V., Phillips M.A., Hackert M.L. Crystal structure of human ornithine decarboxylase at 2.1 A resolution: structural insights to antizyme binding. J. Mol. Biol. 2000, 295:7-16.
42. Henderson C.A., Erales J., Hoyt M.A., Coffino P. Dependence of proteasome processing rate on substrate unfolding. J. Biol. Chem. 2011, 286:17495-17502.
43. Erales J., Hoyt M.A., Troll F., Coffino P. Functional asymmetries of proteasome translocase pore. J. Biol. Chem. 2012, 287:18535-18543.
44. Hinnerwisch J., Fenton W.A., Furtak K.J., Farr G.W., Horwich A.L. Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 2005, 121:1029-1041.
45. Martin A., Baker T.A., Sauer R.T. Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 2008, 15:1147-1151.
46. Zhang F., Wu Z., Zhang P., Tian G., Finley D., Shi Y. Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 2009, 34:485-496.
47. Rubin D.M., Glickman M.H., Larsen C.N., Dhruvakumar S., Finley D. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 1998, 17:4909-4919.
48. Schwanhausser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
49. Schimke R.T. Control of enzyme levels in mammalian tissues. Adv. Enzymol. 1973, 37:135-187.
50. Wheatley D.N., Giddings M.R., Inglis M.S. Kinetics of degradation of 'short-' and 'long-lived' proteins in cultured mammalian cells. Cell Biol. Int. Rep. 1980, 4:1081-1090.
51. Schubert U., Anton L.C., Gibbs J., Norbury C.C., Yewdell J.W., Bennink J.R. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes [see comments]. Nature 2000, 404:770-774.
52. Yewdell J.W. Serendipity strikes twice: the discovery and rediscovery of defective ribosomal products (DRiPS). Cell. Mol. Biol. (Noisy-le-Grand) 2005, 51:635-641.
53. Turner G.C., Varshavsky A. Detecting and measuring cotranslational protein degradation in vivo. Science 2000, 289:2117-2120.
54. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., Harper J.W., Gygi S.P. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011.
55. Wright P.E., Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 1999, 293:321-331.
56. Tompa P., Szasz C., Buday L. Structural disorder throws new light on moonlighting. Trends Biochem. Sci. 2005, 30:484-489.
57. Dunker A.K., Lawson J.D., Brown C.J., Williams R.M., Romero P., Oh J.S., Oldfield C.J., Campen A.M., Ratliff C.M., Hipps K.W., Ausio J., Nissen M.S., Reeves R., Kang C., Kissinger C.R., Bailey R.W., Griswold M.D., Chiu W., Garner E.C., Obradovic Z. Intrinsically disordered protein. J. Mol. Graph. Model. 2001, 19:26-59.
58. Iakoucheva L.M., Brown C.J., Lawson J.D., Obradovic Z., Dunker A.K. Intrinsic disorder in cell-signaling and cancer-associated proteins. J. Mol. Biol. 2002, 323:573-584.
59. Baugh J.M., Viktorova E.G., Pilipenko E.V. Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J. Mol. Biol. 2009, 386:814-827.
60. Suskiewicz M.J., Sussman J.L., Silman I., Shaul Y. Context-dependent resistance to proteolysis of intrinsically disordered proteins. Protein Sci. 2011.
61. Tofaris G.K., Layfield R., Spillantini M.G. Alpha-synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett. 2001, 509:22-26.
62. Chen X., Barton L.F., Chi Y., Clurman B.E., Roberts J.M. Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome. Mol. Cell 2007, 26:843-852.
63. Asher G., Tsvetkov P., Kahana C., Shaul Y. A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev. 2005, 19:316-321.
64. Tsvetkov P., Myers N., Moscovitz O., Sharon M., Prilusky J., Shaul Y. Thermo-resistant intrinsically disordered proteins are efficient 20S proteasome substrates. Mol. Biosyst. 2011, 8:368-373.
65. Kravtsova-Ivantsiv Y., Ciechanover A. Non-canonical ubiquitin-based signals for proteasomal degradation. J. Cell Sci. 2012, 125:539-548.
66. Asher G., Bercovich Z., Tsvetkov P., Shaul Y., Kahana C. 20S proteasomal degradation of ornithine decarboxylase is regulated by NQO1. Mol. Cell 2005, 17:645-655.
67. Valas R.E., Bourne P.E. Rethinking proteasome evolution: two novel bacterial proteasomes. J. Mol. Evol. 2008, 66:494-504.
68. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 2009, 78:477-513.
69. Sharp P.M., Li W.H. Molecular evolution of ubiquitin genes. Trends Ecol. Evol. 1987, 2:328-332.
70. Pegg A.E. Mammalian polyamine metabolism and function. IUBMB Life 2009, 61:880-894.
71. Coffino P. Regulation of cellular polyamines by antizyme. Nat. Rev. Mol. Cell Biol. 2001, 2:188-194.
72. Hanna J., Meides A., Zhang D.P., Finley D. A ubiquitin stress response induces altered proteasome composition. Cell 2007, 129:747-759.