Proteasome and proteolysis;Régulation de la protéolyse: L'action des protéasomes

Journal de la Societe de Biologie

Volumn 198, Issue 3, 2004, Pages 263-278

  Papapostolou, David ^a   Rebound Ravaus, Michéle ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; PROTEIN; PROTEIN SUBUNIT; PROTEINASE INHIBITOR; UBIQUITIN;

AGING; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; HYDROLYSIS; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; PROTEIN PROCESSING; REVIEW; STRUCTURE ACTIVITY RELATION;

AGING; ANIMALS; HUMANS; HYDROLYSIS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; UBIQUITIN;

EID: 14944357261     PISSN: 12950661     EISSN: None     Source Type: Journal    
DOI: 10.1051/jbio/2004198030263     Document Type: Article

References (106)

1. Adams J., Potential of proteasome inhibition in the treatment of cancer. Drug Discovery Today, 2003, 8, 307-315.
2. Adams J., Behnke M., Chen S., Cruickshank A. A., Dick L. R., Genier L., Klunder J. M, Ma Y. T., Plamodon L. & Stein R. L., Potent and selective inhibitors of the proteasome: dipeptidyl boronic acids. Bioorg. Med. Chem. Lett., 1998, 8, 333-338.
3. Akopian T. N., Kisselev A. F. & Goldberg A. L., Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum. J. Biol. Chem., 1997,272, 1791-1798.
4. Anselmi B., Conconi M., Veyrat-Durebex C, Turlin E., Biville F., Alliot J. & Friguet B., Dietary self-selection can compensate an age-related decrease of rat liver 20S proteasome activity observed with standard diet. J. Gerontol. Biol. Sci., 1998, 53A, B173-B179.
5. Arendt C. S. & Hochstrasse M., Eukaryotic 20S proteasome catalytic subunit propeptides prevent active site inactivation by N-terminal acetylation and promote particle assembly, EMB OJ., 1999, 18, 3575-3585.
6. Bachmair A., Finley D. & Varshavsky A., In vivo half-life of a protein is a function of its amino-terminal residue. Science, 234, 179-186.
7. Baumeister W., Walz J., Zuhl F. & Seemuler E., The proteasome: a paradigm of a self-compartmentalizing protease. Cell, 1998, 92, 367-380.
8. Berthelot A., Piguel S., Le Dour G. & Vidal J., Synthesis of macrocyclic peptide analogues of proteasome inhibitor TMC-95A. J. Org. Chem., 2003, 68, 9835-9838.
9. Bertlett B. S. & Stadtman E. R., Protein oxidation in aging, disease and oxidative stress. J. Biol. Chem., 1997, 272, 20313-20316.
10. Bogyo M., McMaster J. S., Gaczynska M., Tortorella D., Goldberg A. L. & Ploegh H., Covalent modification of the active Thr of proteasome β-subunits and the E. coli homologue of HslV by a new class of inhibitors. Proc. Natl. Acad. Sci. USA, 1997, 94, 6629-6634.
11. Bogyo M, Shin S, McMaster J. S. & Ploegh H. L., Substrate binding and sequence preference of the proteasome revealed by active-site-directed affinity probes. Chem. Biol., 1998, 5, 307-320.
12. Bossis G., Frerrar P., Acquaviva C, Jariel-Encontre I. & Piechaczyl M., c-Fos proto-oncoprotein is degraded by the proteasome independently of its own ubiquitinylation in vivo. Mol. Cell. Biol, 2003, 23, 7425-7436.
13. Brannigan J. A., Dodson G., Duggleby H. J., Moody P. C, Smith J. L., Tomchick D. R. & Muzrin A. G., A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature, 1995, 378, 416-419.
14. Braun B. C, Glickman M., Kraft R., Dahlmann B., Kloetzel P. M., Finley D. & Schmidt M., The base of the proteasome regulatory particle exhibits chaperone-like activity. Nat. Cell. Biol., 1999, 1, 221-226.
15. Carrard G., Bulteau A. L., Petropoulos I. & Friguet B., Impairment of proteasome structure and function in aging. Int. J. Biochem. Cell Biol, 2002, 34, 1461-1474.
16. Ciechanover A., The ubiquitin-proteasome proteolytic pathway, Cell, 1994, 79, 13-21.
17. Ciechanover A., The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J., 1998, 17, 7151-7160.
18. Conconi M., Szweda L. L., Levine R. L., Stadtman E. R. & Friguet B., Age-related decline of rat liver multicatalytic proteinase activity and protection from oxidative damage by heat-shock protein. Arch. Biochem. BioPhys., 1996, 331, 232-240.
19. Coux O., An interaction map of proteasome subunits. Biochem. Soc. Trans., 2003, 31, 465-469. Coux O., The 26S proteasome. Prog. Mol Subcell. Biol, 2002, 29, 85-107.
20. Coux O., Tanaka K. & Goldberg A. L., Structure and functions of 20S and 26S proteasomes. Annu. Rev. BioChem., 1996, 65, 801-847.
21. Cuervo A. M. & Dice J. F., When lysosomes get old? Exp. Gerontol., 2000, 35, 119-131.
22. Daniel K. G., Gupta P., Harbach R. H., Guida W. C. & Dou P. Q., Organic copper complexes as a new class of proteasome inhibitors and apoptosis inducers in human cancer cells. Biochem. Pharm., 2004, 67, 1139-1151.
23. Davies K. J. A., Degradation of oxidized proteins by the 20S proteasome. Biochimie, 2001, 83, 301-310.
24. DeMartino G. N. & Goldberg A. L., Identification and purification of an ATP-stimulated alkaline protease in rat liver. J. Biol. Chem., 1979, 254, 3712-3715.
25. Dick L. R., Cruikshank A. A., Genier F. D., Melandri F. D., Nunes S. L. & Stein R. L., Mechanistic studies on the inactivation of the proteasome by lactacystin in cultured cells. J. Biol. Chem., 1997, 277, 182-188.
26. Dick T. P., Nussbaum A. K., Deeg M., Heinemmeyer W., Groll M., Huber R., Rammensee H. G. & Schild H., Contribution of proteasomal β-subunits to the cleavage of peptide substrates analyzed with yeast mutants. J. Biol. Chem., 1998, 273, 25637-25646.
27. Engel M., Hoffmann T., Wagner L., Wermann M., Heiser U., Kiefersauer R., Huber R., Bode W., Demuth H. U. & Brandstetter H., The crystal structure of dipeptidyl peptidase IV (CD26) reveals its functional regulation and enzymatic mechanism. Proc. Natl. Acad. Sci. USA, 2003, 700, 5063-5068.
28. Fenteany G., Standaert R. F., Lane W. S., Choi S., Corey E. J. & Schriber S. L., Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystine. Science, 1995, 268, 726-731.
29. Förster A., Whitby F. G. & Hill C. P., The pore of activated 20S proteasomes has an ordered 7-fold symmetric conformation, EMBO J., 2003, 22, 4356-4364.
30. Friguet B., Aging of proteins and the proteasome, organism. In: Progress in Molecular and Subcellular Biology, 2002, Vol. 29, Reboud-Ravaux M., Ed, Springer-Verlag Berlin Heidelberg, pp. 17-33.
31. Glaser T., Schwarz-Benmeier N., Barnoy S., Barak Z. & Kosower
32. 2+ dependent thiol protease) in erythrocytes of young and old individuals. Proc. Natl. Acad. Sci. USA, 1994, 91, 7879-7883.
33. Glickman M. H., Rubin D. M., Fried V. A. & Finley D., The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell. Biol., 1998, 18, 3149-3162.
34. Glickman M. H. & Ciechanover A., The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev., 2002, 82, 373-428.
35. Groll M., Bajorek M., Kohler 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.
36. Groll M., Ditzel L., Löwe J., Stock D., Bochtler M. Bartunik H. D. & Huber R., Structure of 20S proteasome from yeast at a 2.4 Angstrom resolution. Nature, 1997, 386, 463-471.
37. Groll M., Heinemeyer \V., Jager S., Ullrich T., Bochtler M., Wolf D. H. & Huber R., The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc.'Natl. Acad. Sci. USA, 1999, 96, 10976-10983.
38. Groll M. & Huber R., Substrate access and processing by the 20S proteasome core particle. Int. J. Biochem. Cell Biol., 2003, 35,606-616.
39. Groll M., Kim K. B., Kairies N., Huber R. & Crews CM., Crystal structure of epoxomicin: 20S proteasome reveals a molecular basis for selectivity of alpha, "beta"-epoxyketone proteasome inhibitors. J. Amer. Chem. Soc, 2000,122, 1237-1238.
40. Groll M., Koguchi Y., Huber R.-, Khono J., Crystal structure of the 20S proteasome: TMC-95A complex: a non-covalent proteasome inhibitor. J. Mol. Biol., 2001, 311, 543-548.
41. Grune T., Merker K., Sandig G.;& Davies K. J. A., Selective degradation of oxidatively modified protein substrates by proteasome. Biochm. Biophs. Res. Comm., 2003, 305, 709-718.
42. Hayashi T. & Goto S., Age-related changes in the 20S and 26S proteasome activities in the liver of male F344 rats. Mech. Aging Dev., 1998, 102, 55-66.
43. Hershko A., Lessons from the disiscovery of the ubiquitin system. Trends Biochem. Sci., 1996, 21, 445-449.
44. Hershko A. & Ciechanover A., The ubiquitin system. Annu. Rev. BioChem., 1998, 67, 425-479.
45. Heusch M., Lin L., Geleziunas R. & Greene W. C, The generation of NFKB2 p52: mechanism and efficiency. Oncogene, 1999, 18, 6201-6208.
46. Huibregtse J. M., Scheffner M., Beaudenon S. & Howley P. M., A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA, 1995, 92, 2563-2567.
47. Hoyt M. A., Zhang M. & Coffino P., Ubiquitin-independent mechanisms of mouse ornithine decarboxylase degradation are conserved between mammalian and funaal cells. J. Biol. Chem., 2003, 278, 12135-43
48. Jager S., GrolhM., Huber R., Wolf D. H. & Heinemeyer W., Proteasome (β-type subunits: unequal roles of propeptides in core particle maturation and a hierarchy of active site function. J. Mol. Biol., 1999, 291, 997-1013.
49. Joazeiro C. & Weissman A. M., RING finger proteins: mediators of ubiquitin ligase activity. Cell, 2000, 102, 549-552.
50. Jackson P. K., Eldridge A. G., Freed E., Frustenthal L., Hsu J. Y., Kaiser B. K. & Reimann J. D. R., The lore of the RINGS: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol., 2000, 10, 429-439.
51. Kaiser M., Groll M., Renner C, Huber R. & Moroder L.,The core structure of TMC-95A is a promising lead for reversible proteasome inhibition. Angew. Chem. Int. Ed., 2002, 41, 780-783.
52. Kaiser M., Milbradt A. G., Siciliano C, Assfalg-Machleidt I., Machleidt W., Groll M, Renner C. & Moroder L., TMC-95A - analogues with endocyclic biphenyl ether group as proteasome inhibitors. Chemistry & Biodiversity, 2004, 1, 161-173.
53. Keller J. N., Hanni K. B. & Markesbery W. R., Possible involvement of proteasome inhibition in aging: implications of oxidative stress. Mech. Ageing Dev., 2000, 113, 61-70.
54. 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.
55. Kisselev A. F., Akopian T. N., Castillo V. & Goldberg A. L., Proteasome active sites allosterically regulate each other, suggesting a cyclical bite-chew mechanism for protein breakdown. Mol. Cell., 1999, 4, 395-402.
56. Kisselev A. F., Garcia-Calvo M., Overkleeft H. S., Peterson E., Pennington M. W., Ploegh H. L., Thornberry N. A., Gold berg A. L., The caspase-like sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J. Biol Chem., 278, 35869-35877.
57. Kisselev A. F., Kaganovich D. & Goldberg A. L., Binding of hydrophobic peptides to several non-catalytic sites promotes peptide hydrolysis by all active sites of 20S proteasome. J. Biol. Chem., 2002, 277, 22260-22270.
58. Kisselev A. F., Songyang Z. & Goldberg A. L., Why does threonine, and not serine, function as the active site nucleophile in proteasomes? J. Biol. Chem., 2000, 275, 14831-14837.
59. Kisselev A. F. & Goldberg A. L., Proteasome inhibitors: from reearch tools to drug candidates. Chem. Biol., 2001, 8, 739-758.
60. Koegl M., Hoppe T., Schenker S., Ulrich H. D., Mayer T. U. & Jentsch S., A novel ubiquitination dfactor, E4, is involved in multiubiquitin chain assembly. Cell, 1999, 96, 635-644.
61. Koguchi Y., Kohno J., Nishio M., Takahashi K., Okuda T., Ohnuki T. & Komatsubara S., TMC-95A, B, C, and D, novel proteasome inhibitors produced by Apiospora montagnei Sacc. TC 1093. Taxonomy, production, isolation, and biological activities. J. Antibiot., 2000, 53, 105-109.
62. Kohno J., Koguchi Y., Nishio M., Nakao K., Kuroda M., Shimizu R., Ohnuki T. & Komatsubara S., Structures of TMC- 95A-D: novel proteasome inhibitors from Apiospora montagnei sacc. TC 1093. J. Org. Chem., 2000, 65, 990-995.
63. Lam Y. A., Xu W., DeMartino G. N. & Cohen R. E., Editing of ubiquitin conjueates by an isopeptidase in the 26S proteasome. Nature, 1991, 385, 737-740.
64. Lin S., Yang Z. Q., Kwok B. H. B., Lkoldobskiy M., Crews C. M. & Danishefsky S. J., Total synthesis of TMC-95A and -B via a new reaction leading to Z-enamides. Some preliminary findings as to SAR. J. Amer. Chem. Soc., 2004, published on web.
65. Löwe J., Stock D., Jap B., Zwickl P., Baumeister W. & Huber R., Crystal structure of the 26S proteasome from the archeon T. acidophilum at 3.4 Angstrom resolution. Science, 1995, 268, 533-539.
66. Mack T. C, Dayanandan R., van Siegtenhorst M., Whone A., Hutton M., Lovestone S. & Anderton B. H., Tau levels with frontotemporal dementia-17 mutations have both altered expression levels and phosphorylation profiles in differential neuroblastoma cells. Newoscience, 2001, 108, 701-712.
67. Marastoni M., Baldisserotto A., Canella A., Gavioli R., De Risi C, Pollini G. P. & Tomatis R., Arecoline tripeptides inhibitors of proteasome. J. Med. Chem., 2004a, 47, 1587-1590.
68. Marastoni M., McDonald J., Baldisserotto A., Canella A., De Risi C, Pollini G. P. & Tomatis R., Proteasome inhibitors: synthesis and activity of arecoline oxide tipeptide derivatives. Bioorg. Med. Chem. Letters, 2004b, 14, 1965-1968.
69. Matthews W., Driscoll J., Tanaka K., Ichihara A. & Goldberg A. L., Involvement of the proteasome in various degradative processes in mammalian cells. Proc. Natl. Acad. Sci. USA, 1989, 86, 2597-2601.
70. Meng L. H., Kwok B. H. B., Sin N. & Crews C. M., Eponemycin exerts its antitumor effect through the inhibition of proteasome function. Cancer Res., 1999, 59, 2798-2801.
71. Myung J., Kim B. K., Lindsten K., Dantuma N. P. & Crews C. M., Lack of proteasome active site allostery as revealed by subunit-specific inhibitors. Mol. Cell, 2001, 7, 411-420.
72. Nam S., Smith D. M. & Dou Q. P., Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo. J. Biol. Chem., 2001, 276, 13322-13330.
73. Nussbaum A. K., Dick T. P., Keiholz W., Schirle M., Stavanovic S., Dietz K., Heinemeyer W., Groll M., Wolf D. H., Huber R. & Rammensee H. G., Cleavage motifs of the yeast 20S proteasome beta subunits deduced from digests of enolase 1. Proc. Natl. Acad. Sci. USA, 1998, 95, 12504-12509.
74. Obin M. S., Shang F., Gong X., Handelman G., Blumberg J. & Taylor A., Redox regulation of ubiquitin-conjugating enzymes: mechanistic insights using thiol-specific oxidant diamide. FASEBJ., 1998, 12, 561-569.
75. 14C]-3,4-dichloroisocoumarin with subunits of pituuitary and spleen multicatalytic proteinases complexes (proteasomes). Biochemistry, 1997, 36, 13946-13953.
76. Orlowski M. & Wilk S., Ubiquitin-independent proteolytic functions of the proteasome. Arch. Biochem. BioPhys., 2003, 415, 1-5.
77. Palombella V. J., Rando O. J., Goldberg A. L. & Maniatis T., The ubiquitin proteasome pathway is required for processing of the NF-KB1 precursor protein and activation of NF-KB. Cell, 1994, 78, 773-785.
78. Papapostolou D., Coux O. & Reboud-Ravaux M., Regulation of the 26S proteasome activities by peptides mimicking cleavage products. Biochem. Biophys. Res. Commum., 2002, 295, 1090-1095.
79. Pempler K. P. & Hammond A. L., Protein degradation in human disease. In: progress in molecular and subcellular biology, 2002, Vol. 29, Reboud-Ravaux M., Ed, Springer-Verlag Berlin Heidelberg, pp. 61-83.
80. Picot C. R., Perichon M. Cintrat J. C, Friguet B. & Petropoulos I., The peptide methionine sulfoxide reductases, MsrA and MsrB (hCBS-1), are down-regulated during replicative senescence of human WI-38 fibroblasts. FEBS Lett., 2004, 558, 74-78.
81. Reboud-Ravaux M., Proteasome inhibitors. In: Progress in mole cular and mubcellular biology, 2002, Vol. 29, Reboud-Ravaux M., Ed, Springer-Verlag Berlin Heidelberg, pp. 109-125.
82. Reinheckel T., Sitte N., Ulrich O., Kuckelkorn U., Grune T., Davies K. J. A., Comparative resistance of the the 20S and 26S proteasome resistance to oxidative stress. Biochem. J., 1998, 335, 637-642.
83. Richardson P. G., Hideshima T. & Anderson K. C, Bortezomid (PS-341): a novel, first-in-class proteasome inhibitor for the treatment of multiple myeloma and other cancers. Cancer Control, 2003, 10, 361.
84. Rivett A. J. & Gardner R. C, Proteasome inhibitors: from in vitro studies to clinical trials. J. Peptide Sci., 2000, 6, 478-488.
85. Rock K. L., Gramm C, Rothstein L., Clark R., Stein R., Dick L., Hwang D. & Goldberg A. L., Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class 1 molecules. Cell, 1994, 78, 761-771.
86. Saito K. I., Elce J. S., Hamos J. E. & Nixon R. A., Widespread activation of calcium activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degenration. Proc. Natl. Acad. Sci. USA., 1993, 90, 2628-2632.
87. Sears C, Olesen J., Rubin D. M., Finley D. & Maniatis T., NF-KB p105 proocessing via the ubiquitin-proteasome pathway. J. Biol. Chem., 1998,275, 1409-1419.
88. Seemüller E., Lupas A., Stock D., Löwe J., Huber R. & Baumeister W., Proteasome from Thermoplasma acidophilum - a threonine protease. Science, 1995, 265, 579-582.
89. Scheffner M., Nuber U & Huibregste J. M., Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature, 1995, 373, 81-83.
90. Shibatini T., Nazir M. & Ward W. F., Alteration of rat liver 20S proteasome activities by age and food restriction. J. Gerontol. Biol. Sci., 1996, 51A, B316-B322.
91. Schmidtke G., Emch S., Groettrup M. & Holzhutter H. G., Evidence for the existence of a non-catalytic modifier site of peptide hydrolysis by the 20 S proteasome. J. Biol. Chem., 2000, 275, 22056-22063.
92. Sheaff R. J., Singer J. D., Swanger J., Smitherman M., Roberts J. M. & Clurman B. E., Proteasomal turnover of p21Cipl does not require p21Cipl ubiquitination. Mol. Cell, 2000, 5, 403-410.
93. Shringarpure R., Grune T., Mehlhase J. & Davies K. J., Ubiqui-tinconjugation is not required for the degradation of oxidized proteins by the proteasome. J. Biol. Chem., 2003, 278, 311-318.
94. Smith D. M., Daniel K. G., Wang Z., Guida W. C., Chan T. H. & Dou Q. P., Docking studies and model development of tea polyphenol proteasome inhibitors: applications to rational drug design. Proteins, 2004, 54, 58-70.
95. Stadtman E. R., Protein oxidation in aging and age-related diseases. Ann. NY Acad. Sci., 2001, 928, 22-38.
96. Strickland E., Hakala K., Thomas P. J. & DeMartino G., Recognition of misfolding proteins by PA700, the regulatory subcomplex of the 26 S proteasome. J. Biol. Chem., 2000, 275, 5565-5572.
97. Teplyakov A., Obmolova G., Badet B., Badet-Denisot M. A., Channeling of ammonia in glucosamine-6-phosphate synthase. J. Mol. Biol., 2001, 313, 1093-102.
98. Voges D., Zwickl P. & Baumeister W., The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. BioChem., 1999, 68, 1015-1068.
99. Ward W. F., Protein degradation in the aging organism. In: Progress in molecular and subcellular biology, 2002, Vol. 29, Reboud-Ravaux M., Ed, Springer-Verlag Berlin Heidelberg, pp. 17-33.
100. Ward W. F., The relentless effects of aging on protein turnover. Biogerontology, 2000, 1, 195-1999.
101. Weimer J. M., Kriscenski-Perry E., Elshatory Y. & Pearce D. A., The neuronal lipofuscinoses; mutations in different proteins result in similar disease. Neurol. MEd., 2002, 1, 111-124.
102. 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 US regulators. Nature, 2000, 408, 115-120.
103. Witt E., Zantopf D., Schmidt M., Kraft R., Kloetzel P. M. & Kruger E., Characterisation of the newly identified human Umpl homologue POMP and analysis of LMP7(beta 5i) incorporation into 20S proteasomes. J. Mol. Biol., 2000, 301, 1-9.
104. Yin D., Biochemical basis of lipofuscin, ceroid, and age pigmentlike fluorophores. Free Radic. Biol. MEd., 1996, 21, 871-888.
105. Zhang M., Pickart C. M. & Coffino P., Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. EMBO J., 2003, 22, 1488-1496.
106. Zhang M., MacDonald A. I., Hoyt M. A. & Coffino P., Proteasomes begin ornithine decarboxylase digestion at the C terminus. J. Biol. Chem., 2004, 27.9, 20959-20965.