Nano-liquid chromatography-orbitrap ms-based quantitative proteomics reveals differences between the mechanisms of action of carnosic acid and carnosol in colon cancer cells

Molecular and Cellular Proteomics

Volumn 16, Issue 1, 2017, Pages 8-22

  Valdés, Alberto ^a   García Canãs, Virginia ^a   Artemenko, Konstantin A ^b   Simó, Carolina ^a   Bergquist, Jonas ^b   Cifuentes, Alejandro ^a  

^a INSTITUTE OF FOOD SCIENCE RESEARCH CIAL   (Spain)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

20S PROTEASOME; 26S PROTEASOME; AKR1B10 PROTEIN; AKR1C1 PROTEIN; AKR1C3 PROTEIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CARNOSIC ACID; CARNOSOL; CHYMOTRYPSIN; DNAJB1 PROTEIN; EFHD2 PROTEIN; GLUCOSE TRANSPORTER 1; HEME OXYGENASE 1; HSPA1A PROTEIN; HSPH1 PROTEIN; MESSENGER RNA; MISP PROTEIN; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PEPTIDES AND PROTEINS; POF1B PROTEIN; PROTEASOME; PROTEOME; PSMC4 PROTEIN; RPS24 PROTEIN; RPS26 PROTEIN; SDHA PROTEIN; SLC25A3 PROTEIN; SLC3A2 PROTEIN; SQSTM1 PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ABIETANE DERIVATIVE;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME INHIBITION; HT 29 CELL LINE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MOLECULAR BIOLOGY; NANO LIQUID CHROMATOGRAPHY; NANOANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; UNFOLDED PROTEIN RESPONSE; COLON TUMOR; COMPARATIVE STUDY; DRUG EFFECTS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HT-29 CELL LINE; METABOLISM; PROCEDURES; SIGNAL TRANSDUCTION;

CHROMATOGRAPHY, LIQUID; COLONIC NEOPLASMS; DITERPENES, ABIETANE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEOSTASIS; HT29 CELLS; HUMANS; ISOTOPE LABELING; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UNFOLDED PROTEIN RESPONSE;

EID: 85008430104     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M116.061481     Document Type: Article

References (100)

1. González, M. A. (2015) Aromatic abietane diterpenoids: their biological activity and synthesis. Nat. Prod. Rep. 32, 684-704
2. Aruoma, O. I., Halliwell, B., Aeschbach, R., and Löligers, J. (1992) Antioxidant and pro-oxidant properties of active rosemary constituents: carnosol and carnosic acid. Xenobiotica 22, 257-268
3. Satoh, T., Kosaka, K., Itoh, K., Kobayashi, A., Yamamoto, M., Shimojo, Y., Kitajima, C., Cui, J., Kamins, J., Okamoto, S., Izumi, M., Shirasawa, T., and Lipton, S. A. (2008) Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cyteines on Keap1. J. Neurochem. 104, 1116-1131
4. Tsai, C. W., Lin, C. Y., Lin, H. H., and Chen, J. H. (2011) Carnosic acid, a rosemary phenolic compound, induces apoptosis through reactive oxygen species-mediated p38 activation in human neuroblastoma IMR-32 cells. Neurochem. Res. 36, 2442-2451
5. Satoh, T., McKercher, S. R., and Lipton, S. A. (2013) Nrf2/ARE-mediated antioxidant actions of pro-electrophilic drugs. Free Radic. Biol. Med. 65, 645-657
6. González-Vallinas, M., Reglero, G., and Ramírez de Molina, A. (2015) Rosemary (Rosmarinus officinalis L.) extract as a potential complementary agent in anticancer therapy. Nutr. Cancer 67, 1221-1229
7. Takahashi, T., Tabuchi, T., Tamaki, Y., Kosaka, K., Takikawa, Y., and Satoh, T. (2009) Carnosic acid and carnosol inhibit adipocyte differentiation in mouse 3T3-L1 cells through induction of phase2 enzymes and activation of glutathione metabolism. Biochem. Biophys. Res. Commun. 382, 549-554
8. Tamaki, Y., Tabuchi, T., Takahashi, T., Kosaka, K., and Satoh, T. (2010) Activated glutathione metabolism participates in protective effects of carnosic acid against oxidative stress in neuronal HT22 cells. Planta Med. 76, 683-688
9. Visanji, J. M., Thompson, D. G., and Padfield, P. J. (2006) Induction of G2/M phase cell cycle arrest by carnosol and carnosic acid is associated with alteration of cyclin A and cyclin B1 levels. Cancer Lett. 237, 130-136
10. Valdés, A., García-Canãs, V., Simó, C., Ibánẽz, C., Micol, V., Ferragut, J. A., and Cifuentes, A. (2014) Comprehensive Foodomics study on the mechanisms operating at various molecular levels in cancer cells in response to individual rosemary polyphenols. Anal. Chem. 86, 9807-9815
11. Valdés, A., García-Canãs, V., Koçak, E., Simó, C., and Cifuentes, A. (2016) Foodomics study on the effects of extracellular production of hydrogen peroxide by rosemary polyphenols on the anti-proliferative activity of rosemary polyphenols against HT-29 cells. Electrophoresis 37, 1-10
12. Petiwala, S. M., and Johnson, J. J. (2015) Diterpenes from rosemary (Rosmarinus officinalis): Defining their potential for anti-cancer activity. Cancer Lett. 367, 93-102
13. Dörrie, J., Sapala, K., and Zunino, S. J. (2001) Carnosol-induced apoptosis and downregulation of Bcl-2 in B-lineage leukemia cells. Cancer Lett. 170, 33-39
14. Subbaramaiah, K., Cole, P. A., and Dannenberg, A. J. (2002) Retinoids and carnosol suppress cyclooxygenase-2 transcription by CREB-binding protein/p300-dependent and-independent mechanisms. Cancer Res. 62, 2522-2530
15. Huang, S. C., Ho, C. T., Lin-Shiau, S. Y., and Lin, J. K. (2005) Carnosol inhibits the invasion of B16/F10 mouse melanoma cells by suppressing metalloproteinase-9 through down-regulating nuclear factor-kappa B and c-Jun. Biochem. Pharmacol. 69, 221-232
16. Moran, A. E., Carothers, A. M., Weyant, M. J., Redston, M., and Bertagnolli, M. M. (2005) Carnosol inhibits beta-catenin tyrosine phosphorylation and prevents adenoma formation in the C57BL/6J/Min/ (Min/ ) mouse. Cancer Res. 65, 1097-1104
17. Al Dhaheri, Y., Attoub, S., Ramadan, G., Arafat, K., Bajbouj, K., Karuvantevida, N., AbuQamar, S., Eid, A., and Iratni, R. (2014) Carnosol induces ROS-mediated beclin1-independent autophagy and apoptosis in triple negative breast cancer. PLoS ONE 9:e109630
18. Park, K. W., Kundu, J., Chae, I. G., Kim, D. H., Yu, M. H., Kundu, J. K., and Chun, K. S. (2014) Carnosol induces apoptosis through generation of ROS and inactivation of STAT3 signaling in human colon cancer HCT116 cells. Int. J. Oncol. 44, 1309-1315
19. Johnson, J. J., Syed, D. N., Heren, C. R., Suh, Y., Adhami, V. M., and Mukhtar, H. (2008) Carnosol, a dietary diterpene, displays growth inhibitory effects in human prostate cancer PC3 cells leading to G2-phase cell cycle arrest and targets the 5AMP-activated protein kinase (AMPK) pathway. Pharm. Res. 25, 2125-2134
20. Johnson, J. J., Syed, D. N., Suh, Y., Heren, C. R., Saleem, M., Siddiqui, I. A., and Mukhtar, H. D. (2010) Disruption of androgen and estrogen receptor activity in prostate cancer by a novel dietary diterpene carnosol: implications for chemoprevention. Cancer Prev. Res. 3, 1112-1123
21. Petiwala, S. M., Berhe, S., Li, G., Puthenveetil, A. G., Rahman, O., Nonn, L., and Johnson, J. J. (2014) Rosemary (Rosmarinus officinalis) extract modulates CHOP/GADD153 to promote androgen receptor degradation and decreases xenograft tumor growth. PLoS ONE 9, e89772
22. Barni, M. V., Carlini, M. J., Cafferata, E. G., Puricelli, L., and Moreno, S. (2012) Carnosic acid inhibits the proliferation and migration capacity of human colorectal cancer cells. Oncol. Rep. 27, 1041-1048
23. Kar, S., Palit, S., Ball, W. B., and Das, P. K. (2012) Carnosic acid modulates Akt/IKK/NF--B signaling by PP2A and induces intrinsic and extrinsic pathway mediated apoptosis in human prostate carcinoma PC-3 cells. Apoptosis 17, 735-747
24. Min, K. J., Jung, K. J., and Kwon, T. K. (2014) Carnosic acid induces apoptosis through reactive oxygen species-mediated endoplasmic reticulum stress induction in human renal carcinoma Caki cells. J. Cancer Prev. 19, 170-178
25. Gao, Q., Liu, H., Yao, Y., Geng, L., Zhang, X., Jiang, L., Shi, B., and Yang, F. (2015) Carnosic acid induces autophagic cell death through inhibition of the Akt/mTOR pathway in human hepatoma cells. J. Appl. Toxicol. 35, 485-492
26. Wang, R., Cong, W. H., Guo, G., Li, X. X., Chen, X. L., Yu, X. N., and Li, H. (2012) Synergism between carnosic acid and arsenic trioxide on induction of acute myeloid leukemia cell apoptosis is associated with modulation of PTEN/Akt signaling pathway. Chin. J. Integr. Med. 18, 934-941
27. Valdés, A., Simó, C., Ibánẽz, C., Rocamora-Reverte, L., Ferragut, J. A., García-Canãs, V., and Cifuentes, A. (2012) Effect of dietary polyphenols on K562 leukemia cells: A Foodomics approach. Electrophoresis 33, 2314-2327
28. Ibánẽz, C., Valdés, A., García-Canãs, V., Simó, C., Celebier, M., Rocamora-Reverte, L., Gómez-Martínez, A., Herrero, M., Castro-Puyana, M., Segura-Carretero, A., Ibánẽz, E., Ferragut, J. A., and Cifuentes, A. (2012) Global Foodomics strategy to investigate the health benefits of dietary constituents. J. Chromatogr. A 1248, 139-153
29. Valdés, A., Sullini, G., Ibánẽz, E., Cifuentes, A., and García-Canãs, V. (2015) Rosemary polyphenols induce unfolded protein response and changes in cholesterol metabolism in colon cancer cells. J. Funct. Foods 15, 429-439
30. Valdés, A., Artemenko, K. A., Bergquist, J., García-Canãs, V., and Cifuentes, A. (2016) Comprehensive proteomic study of the antiproliferative activity of a polyphenol-enriched rosemary extract on colon cancer cells using nanoliquid chromatography-orbitrap MS/MS. J. Proteome Res. DOI: 10.1021/acs.jproteome.6b00154
31. Kisselev, A. F., and Goldberg, A. L. (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 398, 364-378
32. Radhakrishnan, S. K., Lee, C. S., Young, P., Beskow, A., Chan, J. Y., and Deshaies, R. J. (2010) Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell. 38, 17-28
33. Yeung, Y. G., and Stanley, E. R. (2010) Rapid detergent removal from peptide samples with ethyl acetate for mass spectrometry analysis. Curr. Protoc. Protein Sci. 16, 16.12
34. Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck, A. J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494
35. Vizcaíno, J. A., Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Ríos, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., Gatto, L., Campos, A., Chalkley, R. J., Kraus, H. J., Albar, J. P., Martinez-Bartolome, S., Apweiler, R., Omenn, G. S., Martens, L., Jones, A. R., and Hermjakob, H. (2014) Proteome-Xchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223-226
36. Baker, P. R., and Chalkley, R. J. (2014) MS-viewer: a web-based spectral viewer for proteomics results. Mol. Cell. Proteomics 13, 1392-1396
37. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteomewide protein quantification. Nat. Biotechnol. 26, 1367-1372
38. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
39. Waters, K. M., Pounds, J. G., and Thrall, B. D. (2006) Data merging for integrated microarray and proteomic analysis. Brief. Funct. Genomic Proteomic. 5, 261-272
40. Suzuki, T., and Yamamoto, M. (2015) Molecular basis of the Keap1-Nrf2 system. Free Radic. Biol. Med. 88, 93-100
41. Eletto, D., Chevet, E., Argon, Y., and Appenzeller-Herzog, C. (2014) Redox controls UPR to control redox. J. Cell Sci. 127, 3649-3658
42. Levonen, A. L., Hill, B. G., Kansanen, E., Zhang, J., and Darley-Usmar, V. M. (2014) Redox regulation of antioxidants, autophagy, and the response to stress: implications for electrophile therapeutics. Free Radic. Biol. Med. 71, 196-207
43. Dodson, M., Redmann, M., Rajasekaran, N. S., Darley-Usmar, V., and Zhang, J. (2015) KEAP1-NRF2 signalling and autophagy in protection against oxidative and reductive proteotoxicity. Biochem. J. 469, 347-355
44. Lee, A. S. (2005) The ER chaperone and signling regulator GRP78/Bip as a monitor of endosplasmic reticulum stress. Methods 35, 373-381
45. Wek, R. C., Jiang, H. Y., and Anthony, T. G. (2006) Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11
46. Yu, L., Andruska, N., Zheng, X., and Shapiro, D. J. (2016) Anticipatory activation of the unfolded protein response by epidermal growth factor is required for immediate early gene expression and cell proliferation. Mol. Cell Endocr. 422, 31-41
47. Andruska, N., Zheng, X., Yang, X., Helferich, W. G., and Shapiro, D. J. (2015) Anticipatory estrogen activation of the unfolded protein response is linked to cell proliferation and poor survival in estrogen receptor alpha-positive breast cancer. Oncogene 34, 3760-3769
48. Shapiro, D. J., Livezey, M., Yu, L., Zheng, X., and Andruska, N. (2016) Anticipatory UPR Activation: A Protective Pathway and Target in Cancer. Trends Endocrinol. Metab. 27, 731-741
49. Yan, M., Li, G., Petiwala, S. M., Householter, E., and Johnson, J. J. (2015) Standardized rosemary (Rosmarinus officinalis) extract in-duces Nrf2/sestrin-2 pathway in colon cancer cells. J. Func. Foods 13, 137-147
50. Wang, M., and Kaufman, R. J. (2014) The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat. Rev. Cancer 14, 581-597
51. Nevins, J. R. (2001) The Rb/E2F pathway and cancer. Hum. Mol. Genet. 10, 699-703
52. Kim, M., Ju, H., Lim, B., and Kang, C. (2012) Maspin genetically and functionally associates with gastric cancer by regulating cell cycle progression. Carcinogenesis 33, 2344-2350
53. Malhotra, S., Lapointe, J., Salari, K., Higgins, J. P., Ferrari, M., Montgomeryet, K., van de Rijn, M., Brooks, J. D., and Pollack, J. R. (2011) A tri-marker proliferation index predicts biochemical recurrence after surgery for prostate cancer. PLoS ONE 6, e20293
54. Liu, M., Huang, F., Zhang, D., Ju, J., Wu, X. B., Wang, Y., Wang, Y., Wu, Y., Nie, M., Li, Z., Ma, C., Chen, X., Zhou, J. Y., Tan, R., Yang, B. L., Zen, K., Zhang, C. Y., Chen, Y. G., and Zhao, Q. (2015) Heterochromatin protein HP1 promotes colorectal cancer progression and is regulated by miR-30a. Cancer Res. 75, 4593-4604
55. Huang, M. C., Chen, H. Y., Huang, H. C., Huang, J., Liang, J. T., Shen, T. L., Lin, N. Y., Ho, C. C., Cho, I. M., and Hsu, S. M. (2006) C2GnT-M is downregulated in colorectal cancer and its re-expression causes growth inhibition of colon cancer cells. Oncogene 25, 3267-3276
56. González-Vallinas, M., Molina, S., Vicente, G., Zarza, V., Martín-Hernández, R., García-Risco, M. R., Fornari, T., Reglero, G., and Ramírez de Molina, A. (2014) Expression of microRNA-15b and the glycosyltransferase GCNT3 correlates with antitumor efficacy of Rosemary diterpenes in colon and pancreatic cancer. PLoS ONE 9, e98556
57. Xu, H., Tian, Y., Yuan, X., Wu, H., Liu, Q., Pestell, R. G., and Wu, K. (2015) The role of CD44 in epithelial-mesenchymal transition and cancer development. Onco Targets Ther. 8, 3783-3792
58. Ishimoto, T., Nagano, O., Yae, T., Tamada, M., Motohara, T., Oshima, H., Oshima, M., Ikeda, T., Asaba, R., Yagi, H., Masuko, T., Shimizu, T., Ishikawa, T., Kai, K., Takahashi, E., Imamura, Y., Baba, Y., Ohmura, M., Suematsu, M., Baba, H., and Saya, H. (2011) CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19, 387-400
59. Bara, J., Chastre, E., Mahiou, J., Singh, R. L., Forgue-Lafitte, M. E., Hollande, E., and Godeau, F. (1998) Gastric M1 mucin, an early oncofetal marker of colon carcinogenesis, is encoded by the MUC5AC gene. Int. J. Cancer 75, 767-773
60. Truant, S., Bruyneel, E., Gouyer, V., De Wever, O., Pruvot, F. R., Mareel, M., and Huet, G. (2003) Requirement of both mucins and proteoglycans in cell-cell dissociation and invasiveness of colon carcinoma HT-29 cells. Int. J. Cancer 104, 683-694
61. Hayashi, Y., Molina, J. R., Hamilton, S. R., and Georgescu, M. M. (2010) NHERF1/EBP50 is a new marker in colorectal cancer. Neoplasia 12, 1013-1022
62. Kruger, W. A., Monteith, G. R., and Poronnik, P. (2013) NHERF-1 regulation of EGF and neurotensin signalling in HT-29 epithelial cells. Biochem. Biophys. Res. Commun. 432, 568-573
63. Glickman, M. H., and Ciechanover, A. (2002) The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82, 373-428
64. Schmidt, M., and Finley, D. (2014) Regulation of proteasome activity in health and disease. Biochim. Biophys. Acta 1843, 13-25
65. Sengupta, S., and Henry, R. W. (2015) Regulation of the retinoblastoma-E2F pathway by the ubiquitin-proteasome system. Biochim. Biophys. Acta 1849, 1289-1297
66. Demasi, M., Netto, L. E., Silva, G. M., Hand, A., de Oliveira, C. L., Bicev, R. N., Gozzo, F., Barros, M. H., Leme, J. M., and Ohara, E. (2013) Redox regulation of the proteasome via S-glutathionylation. Redox Biol. 2, 44-51
67. Peters, J. M. (1994) Proteasomes: protein degradation machines of the cell. Trends Biochem. Sci. 19, 377-382
68. Peters, J. M., Franke, W. W., and Kleinschmidt, J. A. (1994) Distinct 19 S and 20 S subcomplexes of the 26 S proteasome and their distribution in the nucleus and the cytoplasm. J. Biol. Chem. 269, 7709-7718
69. McDougall, G. J., Ross, H. A., Ikeji, M., and Stewart, D. (2008) Berry extracts exert different antiproliferative effects against cervical and colon cancer cells grown in vitro. J. Agric. Food Chem. 56, 3016-3023
70. Shen, M., Schmitt, S., Buac, D., and Dou, Q. P. (2013) Targeting the ubiquitin-proteasome system for cancer therapy. Expert Opin. Ther. Targets 17, 1091-1108
71. Coux, O., Tanaka, K., and Goldberg, A. L. (1996) Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65, 801-847
72. Adams, J. (2002) Proteasome inhibition: a novel approach to cancer therapy. Trends Mol. Med. 8, S49-S54
73. An, B., Goldfarb, R. H., Siman, R., and Dou, Q. P. (1998) 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, 1062-1075
74. Lopes, U. G., Erhardt, P., Yao, R., and Cooper, G. M. (1997) p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem. 272, 12893-12896
75. Nam, S., Smith, D. M., and Dou, Q. P. (2001) Tannic acid potently inhibits tumor cell proteasome activity, increases p27 and Bax expression, and induces G1 arrest and apoptosis. Cancer Epidemiol. Biomarkers Prev. 10, 1083-1088
76. Wada, M., Kosaka, M., Saito, S., Sano, T., Tanaka, K., and Ichihara, A. (1993) Serum concentration and localization in tumor cells of proteasomes in patients with hematologic malignancy and their pathophysiologic significance. J. Lab. Clin. Med. 12, 215-231
77. Kumatori, A., Tanaka, K., Inamura, N., Sone, S., Ogura, T., Matsumoto, T., Tachikawa, T., Shin, S., and Ichihara, A. (1990) Abnormally high expression of proteasomes in human leukemic cells. Proc. Natl. Acad. Sci. U.S.A. 87, 7071-7075
78. Kisselev, A. F., and Goldberg, A. L. (2001) Proteasome inhibitors: from research tools to drug candidates, Chem. Biol. 8, 739-758
79. Afjehi-Sadat, L., Gruber-Olipitz, M., Felizardo, M., Slavc, I., and Lubec, G. (2004) Expression of proteasomal proteins in ten different tumor cell lines. Amino Acids 27, 129-140
80. Ishibashi, Y., Hanyu, N., Suzuki, Y., Yanai, S., Tashiro, K., Usuba, T., Iwabuchi, S., Takahashi, T., Takada, K., Ohkawa, K., Urashima, M., and Yanaga, K. (2004) Quantitative analysis of free ubiquitin and multiubiquitin chain in colorectal cancer. Cancer Lett. 211, 111-117
81. Marfella, R., D'Amico, M., Esposito, K., Baldi, A., Di Filippo, C., Siniscalchi, M., Sasso, F. C., Portoghese, M., Cirillo, F., Cacciapuoti, F., Carbonara, O., Crescenzi, B., Baldi, F., Ceriello, A., Nicoletti, G. F., D'Andrea, F., Verza, M., Coppola, L., Rossi, F., and Giugliano, D. (2006) The ubiquitinproteasome system and inflammatory activity in diabetic atherosclerotic plaques: effects of rosiglitazone treatment. Diabetes 55, 622-632
82. Deng, J., Carlson, N., Takeyama, K., Dal Cin, P., Shipp, M., and Letai, A. (2007) BH3 Profiling Identifies Three Distinct Classes of Apoptotic Blocks to Predict Response to ABT-737 and Conventional Chemotherapeutic Agents. Cancer Cell 12, 171-185
83. Bugno, M., Daniel, M., Chepelev, N. L., and Willmore, W. G. (2015) Changing gears in Nrf1 research, from mechanisms of regulation to its role in disease and prevention. Biochim. Biophys. Acta 1849, 1260-1276
84. Sha, Z., and Goldberg, A. L. (2014) Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr. Biol. 24, 1573-1583
85. Kwak, M. K., Cho, J. M., Huang, B., Shin, S., and Kensler, T. W. (2007) Role of increased expression of the proteasome in the protective effects of sulforaphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells. Free Radic. Biol. Med. 43, 809-817
86. Steffen, J., Seeger, M., Koch, A., and Krüger, E. (2010) Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell. 40, 147-158
87. Radhakrishnan, S. K., den Besten, W., and Deshaies, R. J. (2014) p97-dependent retrotranslocation and proteolytic processing govern formation of active Nrf1 upon proteasome inhibition. Elife 3, e01856
88. Dou, Q. P., and Li, B. (1999) Proteasome inhibitors as potential novel anticancer agents. Drug Resist. Updat. 2, 215-223
89. Gottesman, S., Wickner, S., and Maurizi, M. R. (1997) Protein quality control: triage by chaperones and proteases. Genes Dev. 11, 815-823
90. Bence, N. F., Sampat, R. M., and Kopito, R. R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555
91. Kazi, A., Daniel, K. G., Smith, D. M., Kumar, N. B., and Dou, Q. P. (2003) Inhibition of the proteasome activity, a novel mechanism associated with the tumor cell apoptosis-inducing ability of genistein. Biochem. Pharmacol. 66, 965-976
92. Landis-Piwowar, K. R., Milacic, V., Chen, D., Yang, H., Zhao, Y., Chan, T. H., Yan, B., and Dou, Q. P. (2006) The proteasome as a potential target for novel anticancer drugs and chemosensitizers. Drug Resist. Updat. 9, 263-273
93. Shen, M., Chan, T. H., and Dou, Q. P. (2012) Targeting tumor ubiquitinproteasome pathway with polyphenols for chemosensitization. Anticancer Agents Med. Chem. 12, 891-901
94. Chen, D., Daniel, K. G., Chen, M. S., Kuhn, D. J., Landis-Piwowar, K. R., and Dou, Q. P. (2005) Dietary flavonoids as proteasome inhibitors and apoptosis inducers in human leukemia cells. Biochem. Pharmacol. 69, 1421-1432
95. Shim, S. H. (2011) 20S proteasome inhibitory activity of flavonoids isolated from Spatholobus suberectus. Phytother. Res. 25, 615-618
96. Dick, L. R., Cruikshank, A. A., Destree, A. T., Grenier, L., McCormack, T. A., Melandri, F. D., Nunes, S. L., Palombella, V. J., Parent, L. A., Plamondon, L., and Stein, R. L. (1997) Mechanistic studies on the inactivation of the proteasome by lactacystin in cultured cells. J. Biol. Chem. 272, 182-188
97. Nam, S., Smith, D. M., and Dou, Q. P. (2001) Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo. J. Biol. Chem. 276, 13322-13330
98. Akerfelt, M., Trouillet, D., Mezger, V., and Sistonen, L. (2007) Heat shock factors at a crossroad between stress and development. Ann. N.Y. Acad. Sci. 1113, 15-27
99. Qi, W., White, M. C., Choi, W., Guo, C., Dinney, C., McConkey, D. J., and Siefker-Radtke, A. (2013) Inhibition of inducible heat shock protein-70 (hsp72) enhances bortezomib-induced cell death in human bladder cancer cells. PLoS ONE 8, e69509
100. Shah, S. P., Lonial, S., and Boise, L. H. (2015) When Cancer Fights Back: Multiple Myeloma, Proteasome Inhibition, and the Heat-Shock Response. Mol. Cancer Res. 13, 1163-1173