Regulation of apoptosis by the ubiquitin and proteasome pathway

Journal of Cellular and Molecular Medicine

Volumn 6, Issue 1, 2002, Pages 25-48

  Wójcik, Cezary ^a,b  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Caspases; Proteasome; Proteolysis; Ubiquitin

Indexed keywords

CASPASE; CYSTEINE PROTEINASE; ENZYME INHIBITOR; HEAT SHOCK PROTEIN; MULTIENZYME COMPLEX; PROTEASOME; UBIQUITIN;

ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CHEMICAL STRUCTURE; DRUG ANTAGONISM; HUMAN; METABOLISM; NEOPLASM; PHYSIOLOGY; PROTEIN FOLDING; REVIEW;

ANIMALS; APOPTOSIS; CASPASES; CELL DIFFERENTIATION; CYSTEINE ENDOPEPTIDASES; ENZYME INHIBITORS; HEAT-SHOCK PROTEINS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; UBIQUITIN;

EID: 0036355705     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2002.tb00309.x     Document Type: Review

References (191)

1. Mayer R. J., The meteoric rise of regulated intracellular proteolysis, Nat. Rev. Mol. Cell Biol., 1: 145-148, 2000
2. Rubin D. M., Finley D., Proteolysis. The proteasome: a protein-degrading organelle?, Curr. Biol., 5: 854-858, 1995
3. Rock K. L., Gramm C., Rothstein L., Clark K., 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 I molecules, Cell, 78: 761-71, 1994
4. Hochstrasser M., Johnson P. R., Arendt C. S., Amerik A. Y., Swaminathan S., Swanson R., Li S. J., Laney J., Pals-Rylaarsdam R., Nowak J., Connerly P. L., The Saccharomyces cerevisiae ubiquitin-proteasome system, Philos. Trans. R. Soc. Lond B Biol. Sci., 354: 1513-1522, 1999
5. Drexler H. C. A., Programmed cell death and the proteasome, Apoptosis, 3: 1-7, 1998
6. Orlowski R. Z., The role of the ubiquitin-proteasome pathway in apoptosis., Cell Death Differ, 6: 303_313-1999
7. Grimm L. M., Osborne B. A., Apoptosis and the proteasome, Results Probl Cell Differ, 23: 209-28, 1999
8. Wojcik C., Proteasomes in apoptosis: villains or guardians?, Cell Mol. Life Sci., 56: 908-917, 1999
9. Jesenberger V., Jentsch S., Deadly encounter: ubiquitin meets apoptosis, Nat. Rev. Mol. Cell Biol., 3: 112-121, 2002
10. Etlinger J. D.; Goldberg A. L., A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes, Proc. Natl. Acad. Sci. U. S. A, 74: 54-58, 1977
11. Hershko A., Ciechanover A., Varshavsky A., Basic Medical Research Award. The ubiquitin system, Nat. Med., 6: 1073-1081, 2000
12. Wu R. S., Kohn K. W., Bonner W. M., Metabolism of ubiquitinated histones, J. Biol. Chem., 256: 5916-20, 1981
13. Strous G. J., Covers R., The ubiquitin-proteasome system and endocytosis, J. Cell Sci., 112: 1417-23, 1999
14. Finley D., Bartel B., Varshavsky A., The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis, Nature, 338: 394-401, 1989
15. Ciechanover A., Hod Y., Hershko A., A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes, Biochem. Biophys. Res. Commun., 81: 1100-5, 1978
16. Hershko A., Ciechanover A., The ubiquitin system, Annu. Rev. Biochem., 67: 425-79, 1998
17. Ciechanover A., Breitschopf K., Hatoum O. A., Bengal E., Degradation of MyoD by the ubiquitin pathway: regulation by specific DNA-binding and identification of a novel site for ubiquitination, Mol. Biol. Rep., 26: 59-64, 1999
18. Pickart C. M., Mechanisms underlying ubiquitination, Annu. Rev. Biochem., 70: 503-533, 2001
19. Pickart C. M., Ubiquitin in chains, Trends Biochem. Sci., 25: 544-548, 2000
20. Coffino P., Antizyme, a mediator of ubiquitin-independent proteasomal degradation, Biochimie, 83: 319-323, 2001
21. Kamitani T., Kito K., Fukuda-Kamitani T., Yeh E. T., Targeting of NEDD8 and its conjugates for proteasomal degradation by NUB1, J. Biol. Chem., 276: 46655-46660, 2001
22. Andrea A. D., Pellman D., Deubiquitinating enzymes: a new class of biological regulators, Crit. Rev. Biochem. Mol. Biol., 33: 337-52, 1998
23. Wilkinson K. D., Regulation of ubiquitin-dependent processes by deubiquitinating enzymes, FASEB J., 11: 1245-56, 1997
24. Hendil K. B., The 19 S multicatalytic "prosome" proteinase is a constitutive enzyme in HeLa cells, Biochem. Intl., 17: 471-7, 1988
25. Arrigo A. P., Tanaka K., Goldberg A. L., Welch W. J., Identity of the 19S 'prosome' particle with the large multifunctional protease complex of mammalian cells (the proteasome), Nature, 331: 192-4, 1988
26. Bochtler M., Ditzel L., Groll M., Hartmann C., Huber R., The proteasome, Annu. Rev. Biophys. Biomol. Struct., 28: 295-317, 1999
27. Demartino G. N., Slaughter C. A., The proteasome, a novel protease regulated by multiple mechanisms, J. Biol. Chem., 274: 22123-6, 1999
28. Groll M., Ditzel L., Lowe J., Stock D., Bochtler M., Bartunik H. D., Huber R., Structure of 20S proteasome from yeast at 2.4 A resolution [see comments], Nature, 386: 463-71, 1997
29. Wilk S., Orlowski M., Cation-sensitive neutral endopeptidase: isolation and specificity of the bovine pituitary enzyme., J. Neurochem., 35: 1172-82, 1980
30. Wilk S., Orlowski M., Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex, J. Neurochem., 40: 842-9, 1983
31. Orlowski M., Wilk S., Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex, Arch. Biochem. Biophys., 383: 1-16, 2000
32. Lowe 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 [see comments], Science, 268: 533-9, 1995
33. Fenteany G., Standaert R. F., Lane W. S., Choi S., Corey E. J., Schreiber S. L., Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin, Science, 268: 726-31, 1995
34. Arendt C. S., Hochstrasser M., Identification of the yeast 20S proteasome catalytic centers and subunit interactions required for active-site formation, Proc. Natl. Acad. Sci. U S A, 94: 7156-61, 1997
35. Fruh K., Gossen M., Wang K., Bujard H., Peterson P. A., Yang Y., Displacement of housekeeping proteasome subunits by MHC-encoded LMPs: a newly discovered mechanism for modulating the multicatalytic proteinase complex, EMBO J., 13: 3236-44, 1994
36. Fruh K., Yang Y., Antigen presentation by MHC class I and its regulation by interferon gamma, Curr. Opin. Immunol., 11: 76-81, 1999
37. Kloetzel P. M., Soza A., Stohwasser R., The role of the proteasome system and the proteasome activator PA28 complex in the cellular immune response, Biol. Chem., 380: 293-7, 1999
38. Demartino G. N., Proske R. J., Moomaw C. R., Strong A. A., Song X., Hisamatsu H., Tanaka K., Slaughter C. A., Identification, purification, and characterization of a PA700-dependent activator of the proteasome, J. Biol. Chem., 271: 3112-8, 1996
39. Glickman M. H., Rubin D. M., Coux O., Wefes L, Pfeifer G., Cjeka Z., Baumeister W, Fried V. A., Finley D., A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3, Cell, 94: 615-23, 1998
40. Glickman M. H., Rubin D. M., Fried V. A., Finley D., The regulatory particle of the Saccharomyces cerevisiae proteasome, Mol. Cell. Biol., 18: 3149-62, 1998
41. Dubiel W., Pratt G., Ferrell K., Rechsteiner M., Purification of an 11 S regulator of the multicatalytic proteinase., J. Biol. Chem., 267: 22369-22377, 1992
42. Ma C. P., Slaughter C. A., Demartino G. N., Identification, purification, and characterization of a protein activator (PA28) of the 20 S proteasome (macropain), J. Biol. Chem., 267: 10515-10523, 1992
43. Rechsteiner M., Realini C., Ustrell V., The proteasome activator 11 S REG (PA28) and class I antigen presentation, Biochem. J., 345 Pt 1: 1-15, 2000
44. Tanahashi N., Yokota K., Ahn J. Y., Chung C. H., Fujiwara T., Takahashi E., Demartino G. N., Slaughter C. A., Toyonaga T., Yamamura K., Shimbara N., Tanaka K., Molecular properties of the proteasome activator PA28 family proteins and gamma-interferon regulation, Genes Cells, 2: 195-211, 1997
45. Chu-Ping M., Slaughter C. A., Demartino G. N., Purification and characterization of a protein inhibitor of the 20S proteasome (macropain), Biochim. Biophys. Acta, 1119: 303-11, 1992
46. Scherrer K., Prosomes, subcomplexes of untranslated mRNP, Molec. Biol. Rep., 14: 1-9, 1990
47. Pamnani V., Haas B., Puhler G., Sanger H. L., Baumeister W., Proteasome-associated RNAs are non-specific, Eur. J. Biochem., 225: 511-9, 1994
48. Seemuller E., Lupas A., Stock D., Lowe J., Huber R., Baumeister W., Proteasome from Thermoplasma acidophilum: a threonine protease, Science, 268: 579-582, 1995
49. Lee D. H., Goldberg A. L., Proteasome inhibitors: valuable new tools for cell biologists., Trends Cell Biol, 8: 397-403, 1998
50. Wojcik C., Inhibition of the proteasome as a therapeutic approach, Drug Discov. Today, 4: 188-192, 1999
51. Kisselev A. F., Goldberg A. L., Proteasome inhibitors: from research tools to drug candidates, Chem. Biol., 8: 739-758, 2001
52. Orlowski M., The multicatalytic proteinase complex, a major extralysosomal proteolytic system, Biochemistry, 29: 10289-97, 1990
53. Figueiredo-Pereira M. E., Berg K. A, Wilk S., A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell, J. Neurochem., 63: 1578-81, 1994
54. Spaltenstein A., Leban J. J., Huang J. J., Reinhardt K. R., Viveros O. H., Sigafoos J., Crouch R., Design and synthesis of novel protease inhibitors. Tripeptide a',b'-epoxyketones as nanomolar inactivators of the proteasome., Tetrahedron Lett., 37: 1343-6, 1996
55. Iqbal M., Chatterjee S., Kauer J. C., Das M., Messina P., Freed B., Biazzo W., Siman R., Potent inhibitors of proteasome, J. Med. Chem., 38: 2276-7, 1995
56. Lum R. T., Kerwar S. S., Meyer S. M., Nelson M. G., Schow S. R., Schiffman D., Wick M. M., Joly A., A new class of proteasome inhibitors that prevent NFkB activation., Biochem. Pharmacol., 55: 1391-1397, 1998
57. Adams J., Proteasome inhibition in cancer: development of PS-341, Semin. Oncol., 28: 613-619, 2001
58. Meng L., Mohan R., Kwok B. H., Elofsson M., Sin N., Crews C. M., Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity, Proc. Natl. Acad. Sci. USA, 96: 10403-10408, 1999
59. Meng L., Kwok B. H., Sin N., Crews C. M., Eponemycin exerts its antitumor effect through the inhibition of proteasome function, Cancer Res, 59: 2798-801, 1999
60. Kroll M., Arenzana-Seisdedos F., Bachelerie F., Thomas D., Friguet B., Conconi M., The secondary fungal metabolite gliotoxin targets proteolytic activities of the proteasome, Chem. Biol., 6: 689-98, 1999
61. Nam S., Smith D. M., Dou Q. P., Tannic Acid Potently Inhibits Tumor Cell Proteasome Activity, Increases p27 and Bax Expression, and Induces G(1) Arrest and Apoptosis, Cancer Epidemiol Biomarkers Prev., 10: 1083-1088, 2001
62. Andre P., Groettrup M., Klenerman P., de Giuli R., Booth B. L., Jr., Cerundolo V., Bonneville M., Jotereau F., Zinkernagel R. M., Lotteau V., An inhibitor of HIV-1 protease modulates proteasome activity, antigen presentation, and T cell responses, Proc. Natl. Acad. Sci. USA, 95: 13120-4, 1998
63. Rao S., Porter D. C., Chen X., Herliczek T., Lowe M., Keyomarsi K., Lovastatin-mediated G1 arrest is through inhibition of the proteasome, independent of hydroxymethyl glutaryl-CoA reductase, Proc. Natl. Acad. Sci. USA, 96: 7797-802, 1999
64. Wojcik C., Bury M., Stoklosa T., Giermasz A., Feleszko W., Mlynarczuk I., Pleban E., Basak G., Omura S., Jakobisiak M., Lovastatin and simvastatin are modulators of the proteasome, Int. J. Biochem. Cell Biol., 32: 957-965, 2000
65. Isoe T., Naito M., Hirai R., Tsuruo T., Inhibition of ubiquitin-ATP-dependent proteolysis and ubiquitination by cisplatin, Anticancer Res., 11: 1905-9, 1991
66. Isoe T., Naito M., Shirai A., Hirai R., Tsuruo T., Inhibition of different steps of the ubiquitin system by cisplatin and aclarubicin, Biochim. Btophys. Acta, 1117: 131-5, 1992
67. Figueiredo-Pereira M. E., Chen W. E., Li J., Johdo O., The antitumor drug aclacinomycin A, which inhibits the degradation of ubiquitinated proteins, shows selectivity for the chymotrypsin-like activity of the bovine pituitary 20 S proteasome, J. Biol. Chem., 271: 16455-9, 1996
68. Kiyomiya K., Matsuo S., Kurebe M., Proteasome is a carrier to translocate doxorubicin from cytoplasm into nucleus, Life Sci., 62: 1853-60, 1998
69. Piccinini M., Tazartes O., Mezzatesta C., Ricotti E., Bedino S., Grosso F., Dianzani U., Tovo P. A., Mostert M., Musso A., Rinaudo M. T., Proteasomes are a target of the anti-tumour drug vinblastine, Biochem. J., 356: 835-841, 2001
70. Schwartz L. M., Myer A., Kosz L., Engelstein M., Maier C., Activation of polyubiquitin gene expression during developmentally programmed cell death, Neuron, 5: 411-9, 1990
71. Imajoh-Ohmi S., Kawaguchi T., Sugiyama S., Tanaka K., Omura S., Kikuchi H., Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells, Biochem Biophys Res Comm, 217: 1070-7, 1995
72. Almond J. B., Snowden R. T., Hunter A., Dinsdale D., Cain K., Cohen G. M., Proteasome inhibitor-induced apoptosis of B-chronic lymphocytic leukaemia cells involves cytochrome c release and caspase activation, accompanied by formation of an approximately 700 kDa Apaf-1 containing apoptosome complex, Leukemia, 15: 1388-1397, 2001
73. Soligo D., Servida F., Delia D., Fontanella E., Lamorte G., Caneva L. Fumiatti R., Lambertenghi D. G., The apoptogenic response of human myeloid leukaemia cell lines and of normal and malignant haematopoietic progenitor cells to the proteasome inhibitor PSI, Br. J. Haematol., 113: 126-135, 2001
74. Bold R. J., Virudachalam S., McConkey D. J., Chemosensitization of pancreatic cancer by inhibition of the 26S proteasome, J. Surg. Res., 100: 11-17, 2001
75. Lee M., Hyun D. H., Marshall K. A., Ellerby L. M., Bredesen D. E., Jenner P., Halliwell B., Effect of overexpression of Bcl-2 on cellular oxidative damage, nitric oxide production, antioxidant defenses, and the proteasome, Free Radic. Biol. Med., 31: 1550-1559, 2001
76. Traenckner E. B., Wilk S. Baeuerle P. A., A proteasome inhibitor prevents activation of NF-kappa B and stabilizes a newly phosphorylated form of I kappa B-alpha that is still bound to NF-kappa B, EMBO J., 13: 5433-41, 1994
77. Wang C. Y., Mayo M. W., Baldwin A. S. Jr., TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NFkB., Science. 274: 787-789, 1996
78. Delic J., Masdehors P., Omura S., Cosset J. M., Dumont J., Binet J. L., Magdelenat H., The proteasome inhibitor lactacystin induces apoptosis and sensitizes chemo- and radioresistant human chronic lymphocytic leukaemia lymphocytes to TNF-alpha-initiated apoptosis, Br. J. Canc., 77: 1103-7, 1998
79. Fujita E., Mukasa T., Tsukahara T., Arahata K., Omura S., Momoi T., Enhancement of CPP32-like activity in the TNF-treated U937 cells by the proteasome inhibitors, Biochem Biophys. Res. Comm., 224: 74-9, 1996
80. Fujihara S., Ward C., Dransfield I., Hay R., Uings I., Hayes B., Farrow S., Haslett C., Rossi A., Inhibition of nuclear factor-κB activation un-masks the ability of TNF-α to induce human eosinophil apoptosis, Eur. J. Immunol., 32: 457-466, 2002
81. Franco A. V., Zhang X. D., Van Berkel E., Sanders J. E., Zhang X. Y., Thomas W. D., Nguyen T., Hersey P., The role of NF-kappa B in TNF-related apoptosis-inducing ligand (TRAIL)- induced apoptosis of melanoma cells, J. Immunol., 166: 5337-5345, 2001
82. Yabe T., Wilson D., Schwartz J. P., NF{kappa}B activation is required for the neuroprotective effects of pigment epithelium-derived factor (PEDF) on cerebellar granule neurons, J. Biol. Chem., 2001
83. Elliott P. J., Pien C. S., McCormack T. A., Chapman I. D., Adams J., Proteasome inhibition: A novel mechanism to combat asthma, J. Allergy Clin. Immunol., 104: 294-300, 1999
84. Wojcik C., Schroeter D., Stoehr M., Wilk S., Paweletz N., An inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces arrest in G2-phase and metaphase in HeLa cells, Europ. J. Cell. Biol., 70: 172-8, 1996
85. Machiels B. M., Henfling M. E., Gerards W. L., Broers J. L., Bloemendal H., Ramaekers F. C., Schutte B., Detailed analysis of cell cycle kinetics upon proteasome inhibition, Cytometry, 28: 243-252, 1997
86. Hershko A., Roles of ubiquitin-mediated proteolysis in cell cycle control, Curr. Opin. Cell Biol., 9: 788-99, 1997
87. Shah S. A., Potter M. W., McDade T. P., Ricciardi R., Perugini R. A., Elliott P. J., Adams J., Callery M. P., 26S proteasome inhibition induces apoptosis and limits growth of human pancreatic cancer, J. Cell Biochem., 82: 110-122, 2001
88. Shen Y., White E., p53-dependent apoptosis pathways, Adv. Cancer Res., 82: 55-84, 2001
89. Wang X. W., Role of p53 and apoptosis in carcinogenesis, Anticancer Res., 19: 4759-4771, 1999
90. Burns T. F., El Deiry W. S., The p53 pathway and apoptosis, J. Cell Physiol., 181: 231-239, 1999
91. Fang S., Jensen J. P., Ludwig R. L., Vousden K. H., Weissman A. M., Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53, J. Biol. Chem., 275: 8945-8951, 2000
92. Cho J. W., Park J. C., Lee J. C., Kwon T. K., Park J. W., Baek W. K., Suh S. I., Suh M. H., The levels of MDM2 protein are decreased by a proteasome-mediated proteolysis prior to caspase-3-dependent pRb and PARP cleavages, J. Korean Med. Sci., 16: 135-139, 2001
93. MacLaren A. P., Chapman R. S., Wyllie A. H., Watson C. J., p53-dependent apoptosis induced by proteasome inhibition in mammary epithelial cells, Cell Death. Differ., 8: 210-218, 2001
94. Herrmann J. L., Briones F. Jr., Brisbay S., Logothetis C. J., McDonnell T. J., Prostate carcinoma cell death resulting from inhibition of proteasome activity is independent of functional Bcl-2 and p53, Oncogene, 17: 2889-99, 1998
95. An B., Goldfarb R. H., Siman R., Dou Q. P., Novel dipeptidyl proteasome inhibitors overcome Bcl-2 protective function and selectively accumulate the cyclin-dependent kinase inhibitor p27 and induce apoptosis in transformed, but not normal, human fibroblasts, Cell Death Differ, 5: 1062-75, 1998
96. Wagenknecht B., Hermisson M., Eitel K. Weller M., Proteasome inhibitors induce p53/p21-independent apoptosis in human glioma cells, Cell Physiol. Biochem., 9: 117-125, 1999
97. Seluanov A., Gorbunova V., Falcovitz A., Sigal A., Milyavsky M., Zurer I., Shohat G., Goldfinger N., Rotter V., Change of the death pathway in senescent human fibroblasts in response to DNA damage is caused by an inability to stabilize p53, Mol. Cell Biol., 21: 1552-1564, 2001
98. Fukazawa T., Fujiwara T., Uno F., Teraishi F., Kadowaki Y., Itoshima T., Takata Y., Kagawa S., Roth J. A., Tschopp J., Tanaka N., Accelerated degradation of cellular FLIP protein through the ubiquitin- proteasome pathway in p53-mediated apoptosis of human cancer cells, Oncogene, 20: 5225-5231, 2001
99. Gregory M. A., Hann S. R., c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells, Mol. Cell Biol., 20: 2423-2435, 2000
100. Tani E., Kitagawa H., Ikemoto H., Matsumoto T., Proteasome inhibitors induce Fas-mediated apoptosis by c-Myc accumulation and subsequent induction of FasL message in human glioma cells, FEBS Lett., 504: 53-58, 2001
101. Kim K., Proteasome inhibitors sensitize human vascular smooth muscle cells to Fas (CD95)-mediated death, Biochem. Biophys. Res. Commun., 281: 305-310, 2001
102. Suzuki Y., Nakabayashi Y., Takahashi R., Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death, Proc. Natl. Acad. Sci. USA, 98: 8662-8667, 2001
103. Tenev T., Marani M., McNeish I., Lemoine N. R., Pro-caspase-3 overexpression sensitises ovarian cancer cells to proteasome inhibitors, Cell Death. Differ., 8: 256-264, 2001
104. Martin M. C., Dransfield I., Haslett C., Rossi A. G., Cyclic AMP regulation of neutrophil apoptosis occurs via a novel PKA-independent signaling pathway, J. Bioi. Chem., 2001
105. Lee M. H., Hyun D. H., Jenner P., Halliwell B., Effect of proteasome inhibition on cellular oxidative damage, antioxidant defences and nitric oxide production, J. Neurochem., 78: 32-41, 2001
106. Pleban E., Bury M., Mlynarczuk I., Wojcik C., Effects of proteasome inhibitor PSI on neoplastic and non-transformed cell lines, Folia Histochem. Cytobiol., 39: 133-134, 2001
107. Sadoul R., Fernandez P. A., Quiquerez A. L., Martinou I., Maki M., Schroter M., Becherer J. D., Irmler M., Tschopp J., Martinou J. C., Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons, EMBO J., 15: 3845-52, 1996
108. Grimm L. M., Goldberg A. L., Poirier G. G., Schwartz L. M., Osborne B. A., Proteasomes play an essential role in thymocyte apoptosis, EMBO J., 15: 3835-44, 1996
109. Tabata M., Tabata R., Grabowski D. R., Bukowski R. M., Ganapathi M. K., Ganapathi R., Roles of NF-kappaB and 26 S proteasome in apoptotic cell death induced by topoisomerase I and II poisons in human nonsmall cell lung carcinoma, J. Biol. Chem., 276: 8029-8036, 2001
110. 11O. Tanimoto Y., Kizaki H., Proteasome inhibitors block ras/ERK signaling pathway resulting in the downregulation of Fas ligand expression during activation-induced cell death in T cells, J. Biochem., 131: 319-326, 2002
111. Dallaporta B., Pablo M., Maisse C., Daugas E., Loeffler M., Zamzami N., Kroemer G., Proteasome activation as a critical event of thymocyte apoptosis, Cell Death. Differ., 7: 368-373, 2000
112. Distelhorst C. W., Recent insights into the mechanism of glucocorticosteroid-induced apoptosis, Cell Death. Differ., 9: 6-19, 2002
113. Wallace A. D., Cidlowski J. A., Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids, J. Biol. Chem., 276: 42714-42721, 2001
114. Hirsch T., Dallaporta B., Zamzami N., Susin S. A., Ravagnan L., Marzo I., Brenner C., Kroemer G., Proteasome activation occurs at an early, premitochondrial step of thymocyte apoptosis, J. Immunol., 161: 35-40, 1998
115. Beyette J., Mason G. G., Murray R. Z., Cohen G. M., Rivett A. J., Proteasome activities decrease during dexamethasone-induced apoptosis of thymocytes, Biochem J, 332: 315-20, 1998
116. He H., Qi X. M., Grossmann J., Distelhorst C. W., c-Fos degradation by the proteasome. An early, Bcl-2-regulated step in apoptosis, J. Biol. Chem., 273: 25015-9, 1998
117. Ivanov V. N., Nikolic-Zugic J., Biochemical and kinetic characterization of the glucocorticoid-induced apoptosis of immature CD4+CD8+ thymocytes, Int. Immunol., 10: 1807-17, 1998
118. Grassilli E., Benatti F., Dansi P., Giammarioli A. M., Malorni W., Franceschi C., Desiderio M. A., Inhibition of proteasome function prevents thymocyte apoptosis: involvement of ornithine decarboxylase, Biochem. Biophys. Res. Comm., 250: 293-7, 1998
119. Gil-Gomez G., Berns A., Brady H. J., A link between cell cycle and cell death: Bax and Bcl-2 modulate Cdk2 activation during thymocyte apoptosis, EMBO J., 17: 7209-7218, 1998
120. Yang Y., Fang S., Jensen J. P., Weissman A. M., Ashwell J. D., Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli, Science, 288: 874-877, 2000
121. Bannerman D. D., Tupper J. C., Ricketts W. A., Bennett C. F., Winn R. K., Harlan J. M., A constitutive cytoprotective pathway protects endothelial cells from lipopolysaccharide-induced apoptosis, J. Biol. Chem., 276: 14924-14932, 2001
122. Richter B. W., Duckett C. S., The IAP proteins: caspase inhibitors and beyond, Sci. STKE., 2000: E1-2000
123. Yang Y. L., Li X. M., The IAP family: endogenous caspase inhibitors with multiple biological activities, Cell Res., 10: 169-177, 2000
124. Mahoney J. A., Odin J. A., White S. M., Shaffer D., Koff A., Casciola-Rosen L., Rosen A., The human homologue of the yeast polyubiquitination factor Ufd2p is cleaved by caspase 6 and granzyme B during apoptosis, Biochem. J., 361: 587-595, 2002
125. Koegl M., Hoppe T., Schlenker S., Ulrich H. D., Mayer T. U., Jentsch S., A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly, Cell, 96: 635-644, 1999
126. Pizzuti A., Novelli G., Ratti A., Amati F., Mari A., Calabrese G., Nicolis S., Silani V., Marino B., Scarlato G., Ottolenghi S., Dallapiccola B., UFD1L, a developmentally expressed ubiquitination gene, is deleted in CATCH 22 syndrome, Hum. Mol. Genet., 6: 259-265, 1997
127. Dai R. M., Li C. C., Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation, Nat. Cell Biol., 3: 740-744, 2001
128. Ye Y., Meyer H. H., Rapoport T. A., The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol, Nature, 414: 652-656, 2001
129. Araya R., Takahashi R., Nomura Y., Yeast two-hybrid screening using constitutive-active caspase-7 as bait in the identification of PA28gamma as an effector caspase substrate, Cell Death. Differ., 9: 322-328, 2002
130. Li J., Gao X., Ortega J., Nazif T., Joss L., Bogyo M., Steven A. C., Rechsteiner M., Lysine 188 substitutions convert the pattern of proteasome activation by REGgamma to that of REGs alpha and beta, EMBO J., 20: 3359-3369, 2001
131. Murata S., Kawahara H., Tohma S., Yamamoto K., Kasahara M., Nabeshima Y., Tanaka K., Chiba T., Growth retardation in mice lacking the proteasome activator PA28gamma, J. Biol. Chem., 274: 38211-38215, 1999
132. Mullally J. E., Moos P. J., Edes K., Fitzpatrick F. A., Cyclopentenone prostaglandins of the J series inhibit the ubiquitin isopeptidase activity of the proteasome pathway, J. Biol. Chem., 276: 30366-30373, 2001
133. Migone T. S., Humbert M., Rascle A., Sanden D., D'Andrea A., Johnston J. A., The deubiquitinating enzyme DUB-2 prolongs cytokine-induced signal transducers and activators of transcription activation and suppresses apoptosis following cytokine withdrawal, Blood, 98: 1935-1941, 2001
134. Mimnaugh E. G., Kayastha G., McGovern N. B., Hwang S. G., Marcu M. G., Trepel J., Cai S. Y., Marchesi V. T., Neckers L., Caspase-dependent deubiquitination of monoubiquitinated nucleosomal histone H2A induced by diverse apoptogenic stimuli, Cell Death. Differ., 8: 1182-1196, 2001
135. Neves D. D., Rehen S. K., Linden R., Differentiation-dependent sensitivity to cell death induced in the developing retina by inhibitors of the ubiquitin-proteasome proteolytic pathway, Eur. J. Neurosci., 13: 1938-1944, 2001
136. Guzman M. L., Neering S. J., Upchurch D., Grimes B., Howard D. S., Rizzieri D. A., Luger S. M., Jordan C. T., Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells, Blood, 98: 2301-2307, 2001
137. Perletti L., Kopf E., Carre L., Davidson I., Coordinate regulation of RARgamma2, TBP, and TAFI135 by targeted proteolysis during retinoic acid-induced differentiation of F9 embryonal carcinoma cells, BMC. Mol. Biol., 2: 4-2001
138. Wójcik C., Schroeter D., Wilk S., Lamprecht J., Paweletz N., Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome, Eur. J. Cell Biol., 71: 311-8, 1996
139. Johnston J. A., Ward C. L., Kopito R. R., Aggresomes: a cellular response to misfolded proteins, J. Cell Biol., 143: 1883-98, 1998
140. Wojcik C., An inhibitor of the chymotrypsin-like activity of the proteasome (PSI) induces similar morphological changes in various cell lines, Folia Histochem. Cytobiol., 35: 211-214, 1997
141. Wojcik C., On the spatial organization of ubiquitin-dependent proteolysis in HeLa cells, Folia Histochem. Cytobiol., 35: 117-118, 1997
142. Rideout H. J., Larsen K. E., Sulzer D., Stefanis L., Proteasomal inhibition leads to formation of ubiquitin/alpha-synuclein-immunoreactive inclusions in PC12 cells, J. Neurochem., 78: 899-908, 2001
143. Bence N. F., Sampat R. M., Kopito R. R., Impairment of the ubiquitin-proteasome system by protein aggregation, Science, 292: 1552-1555, 2001
144. Volbracht C., Leist M., Kolb S. A., Nicotera P., Apoptosis in caspase-inhibited neurons, Mol. Med., 7: 36-48, 2001
145. Kuusisto E., Suuronen T., Salminen A., Ubiquitin-binding protein p62 expression is induced during apoptosis and proteasomal inhibition in neuronal cells, Biochem. Biophys. Res. Commun., 280: 223-228, 2001
146. Hauser H. P., Bardroff M., Pyrowolakis G., Jentsch S., A giant ubiquitin-conjugating enzyme related to IAP apoptosis inhibitors, J. Cell Biol., 141: 1415-22, 1998
147. De Vrij F. M., Sluijs J. A., Gregori L., Fischer D. F., Hermens W. T., Goldgaber D., Verhaagen J., Van Leeuwen F. W., Hol E. M., Mutant ubiquitin expressed in Alzheimer's disease causes neuronal death, FASEB J., 15: 2680-2688, 2001
148. Tanaka Y., Engelender S., Igarashi S., Rao R. K., Wanner T., Tanzi R. E., Sawa A., Dawson L., Dawson T. M., Ross C. A., Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis, Hum. Mol. Genet., 10: 919-926, 2001
149. Anton L. C., Schubert U., Bacik I., Princiotta M. F., Wearsch P. A. Gibbs J., Day P. M., Realini C., Rechsteiner M. C., Bennink J. R., Yewdell J. W., Intracellular localization of proteasomal degradation of a viral antigen, J. Cell Biol., 146: 113-124, 1999
150. Jana N. R., Zemskov E. A., Wang G., Nukina N., Altered proteasomal function due to the expression of polyglutamine- expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release, Hum. Mol. Genet., 10: 1049-1059, 2001
151. Sherman M. Y., Goldberg A. L., Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases, Neuron, 29: 15-32, 2001
152. Kopito R. R., Aggresomes, inclusion bodies and protein aggregation, Trends Cell Biol., 10: 524-530, 2000
153. Matsuzawa S., Takayama S., Froesch B. A., Zapata J. M., Reed J. C., p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by Bag-1, EMBO J., 17: 2736-47, 1998
154. Sondermann H., Scheufler C., Schneider C., Hohfeld J., Hartl F. U., Moarefi I., Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors, Science, 291: 1553-1557, 2001
155. Luders J., Demand J., Hohfeld J., The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome, J. Biol. Chem., 275: 4613-4617, 2000
156. Murata S., Minami Y., Minami M., Chiba T., Tanaka K., CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein, EMBO Rep., 2: 1133-1138, 2001
157. Demand J., Alberti S., Patterson C., Hohfeld J., Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling, Curr. Biol., 11: 1569-1577, 2001
158. Fabunmi R. P., Wigley W. C., Thomas P. J., Demartino G N., Activity and regulation of the centrosome-associated proteasome, J. Biol. Chem., 275: 409-413, 2000
159. Wigley W. C., Fabunmi R. P., Lee M. G., Marino C. R., Muallem S., Demartino G. N., Thomas P. J., Dynamic association of proteasomal machinery with the centrosome, J. Cell Biol., 145: 481-490, 1999
160. Ashok B. T., Kim E., Mittelman A., Tiwari R. K., Proteasome inhibitors differentially affect heat shock protein response in cancer cells, Int. J. Mol. Med., 8: 385-390, 2001
161. Kobayashi Y., Sobue G., Protective effect of chaperones on polyglutamine diseases, Brain Res. Bull., 56: 165-168, 2001
162. Nimmanapalli R., O'Bryan E., Bhalla K., Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr- Abl-positive human leukemic blasts, Cancer Res., 61: 1799-1804, 2001
163. Pajonk F., McBride W. H., The Proteasome in Cancer Biology and Treatment, Radiat. Res., 156: 447-459, 2001
164. Shah S. A., Potter M. W., Gallery M. P., Ubiquitin proteasome pathway: implications and advances in cancer therapy, Surg. Oncol., 10: 43-52, 2001
165. Orlowski R. Z., Eswara J. R., Lafond-Walker A., Grever M. R., Orlowski M., Dang C. V., Tumor growth inhibition induced in a murine model of human Burkitt's lymphoma by a proteasome inhibitor, Cancer Res, 58: 4342-8, 1998
166. Stoklosa T., Golab J., Wojcik C., Jalili A., Marczak M., Giermasz A., Januszko P., Balkowiec E., Jakóbisiak M., Wilk S., Antitumor effect of proteasome inhibitor dependent on p53 induction and angiogenesis inhibition., Third Workshop on Proteasomes, Clermont-Ferrand, France, March 1999
167. Sunwoo J. B., Chen Z., Dong G., Yeh N., Crowl B. C., Sausville E., Adams J., Elliott P., Van Waes C., Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor- kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma, Clin. Cancer Res., 7: 1419-1428, 2001
168. Sun J., Nam S., Lee C. S., Li B., Coppola D., Hamilton A. D., Dou Q. P., Sebti S. M., CEP1612, a dipeptidyl proteasome inhibitor, induces p21WAF1 and p27KIP1 expression and apoptosis and inhibits the growth of the human lung adenocarcinoma A-549 in nude mice, Cancer Res., 61: 1280-1284, 2001
169. Hideshima T., Richardson P., Chauhan D., Palombella V. J., Elliott P. J., Adams J., Anderson K. C., The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells, Cancer Res., 61: 3071-3076, 2001
170. Meiners S., Laule M., Rother W., Guenther C., Prauka I., Muschick P., Baumann G., Kloetzel P. M., Stangl K., Ubiquitin-proteasome pathway as a new target for the prevention of restenosis, Circulation, 105: 483-489, 2002
171. Pervan M., Pajonk F., Sun J. R., Withers H. R., McBride W. H., Molecular pathways that modify tumor radiation response, Am. J. Clin. Oncol., 24: 481-485, 2001
172. Russo S. M., Tepper J. E., Baldwin A. S. Jr., Liu R., Adams J., Elliott P., Cusack J. C. Jr., Enhancement of radiosensitivity by proteasome inhibition: implications for a role of NF-kappaB, Int. J. Radiat. Oncol. Biol. Phys., 50: 183-193, 2001
173. Oyaizu H., Adachi Y., Okumura T., Okigaki M., Oyaizu N., Taketani S., Ikebukuro K., Fukuhara S., Ikehara S., Proteasome inhibitor 1 enhances paclitaxel-induced apoptosis in human lung adenocarcinoma cell line, Oncol. Rep., 8: 825-829, 2001
174. Cusack J. C. Jr., Liu R., Houston M., Abendroth K., Elliott P. J., Adams J., Baldwin A. S. Jr., Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition, Cancer Res., 61: 3535-3540, 2001
175. Milligan S. A., Nopajaroonsri C., Inhibition of NF-kappa B with proteasome inhibitors enhances apoptosis in human lung adenocarcinoma cells in vitro, Anticancer Res., 21: 39-44, 2001
176. Golab J., Stoklosa T., Czajka A., Dabrowska A., Jakobisiak M., Zagozdzon R., Wojcik C., Marczak M., Wilk S., Synergistic antitumor effects of a selective proteasome inhibitor and TNF in mice, Anticancer Res., 20: 1717-1721, 2000
177. Wojcik C., Mlynarczuk I., Hoser G., Kawiak J., Stoklosa T., Golab J., Wilk S., A combination of retinoic acid and proteasome inhibitors for the treatment of leukemias is potentially dangerous., Blood, 94: 1827-1828, 1999
178. Brophy V. A., Tavare J. M., Rivett A. J., Treatment of COS-7 cells with proteasome inhibitors or gamma-interferon reduces the increase in caspase 3 activity associated with staurosporine-induced apoptosis, Arch. Biochem. Biophys., 397: 199-205, 2002
179. Stoklosa T., Wójcik C., Golab J., Giermasz A., Wilk S., Inhibition of proteasome, apoptosis and sensitization to tumour necrosis factor alpha: do they always go together?, Br. J. Cancer, 79: 375-376, 1999
180. Glas R., Bogyo M., McMaster J. S., Gaczynska M., Ploegh H. L., A proteolytic system that compensates for loss of proteasome function, Nature, 392: 618-622, 1998
181. Wang E. W., Kessler B. M., Borodovsky A., Cravatt B. F., Bogyo M., Ploegh H. L., Glas R., Integration of the ubiquitin-proteasome pathway with a cytosolic oligopeptidase activity, Proc. Natl. Acad. Sci. USA, 97: 9990-9995, 2000
182. Geier E., Pfeifer G., Wilm M., Lucchiari-Hartz M., Baumeister W., Eichmann K., Niedermann G., A giant protease with potential to substitute for some functions sof the proteasome, Science, 283: 978-81, 1999
183. Bury M., Mlynarczuk I., Pleban E., Hoser G., Kawiak J., Wojcik C., Effects of an inhibitor of tripeptidyl peptidase II (Ala-Ala- Phechloromethylketone) and its combination with an inhibitor of the chymotrypsin-like activity of the proteasome (PSI) on apoptosis, cell cycle and proteasome activity in U937 cells, Folia Histochem. Cytobiol., 39: 131-132, 2001
184. Princiotta M. F., Schubert U., Chen W., Bennink J. R., Myung J., Crews C. M., Yewdell J. W., Cells adapted to the proteasome inhibitor 4-hydroxy- 5-iodo-3- nitrophenylacetyl-Leu-Leu-leucinal-vinyl sulfone require enzymatically active proteasomes for continued survival, Proc. Natl. Acad. Sci. USA, 98: 513-518, 2001
185. Gavioli R., Frisan T., Vertuani S., Bornkamm G W., Masucci M. G., c-myc overexpression activates alternative pathways for intracellular proteolysis in lymphoma cells, Nat. Cell Biol., 3: 283-288, 2001
186. Wojcik C., Demartino G. N., Analysis of Drosophila 26 S proteasome using RNA interference, J. Biol. Chem., 277: 6188-6197, 2002
187. Tomkinson B., Tripeptidyl peptidases: enzymes that count, Trends Biochem. Sci., 24: 355-359, 1999
188. Huang Y., Shin N. H., Sun Y., Wang K. K., Molecular cloning and characterization of a novel caspase-3 variant that attenuates apoptosis induced by proteasome inhibition, Biochem. Biophys. Res. Commun., 283: 762-769, 2001
189. Adams J., Palombella V. J., Sausville E. A., Johnson J., Destree A., Lazarus D. D., Maas J., Pien C. S., Prakash S., Elliott P. J., Proteasome inhibitors: a novel class of potent and effective antitumor agents, Cancer Res, 59: 2615-22, 1999
190. Wójcik C., Ubiquitin- and proteasome-dependent proteolytic pathway as an emerging therapeutic target, Emerging Therapeutic Targets, 4: 1-23, 2000
191. Luo H., Wu Y., Qi S., Wan X., Chen H., Wu J., A proteasome inhibitor effectively prevents mouse heart allograft rejection, Transplantation, 72: 196-202, 2001