Proteasome expression and activity in cancer and cancer stem cells

Tumor Biology

Volumn 39, Issue 3, 2017, Pages 1-17

  Voutsadakis, Ioannis A ^a,b  

^a Sault Area Hospitals   (Canada)

^b NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

Author keywords

19S; 20S; cancer stem cells; carcinogenesis; pluripotency; Proteasome; sub units

Indexed keywords

PROTEASOME;

APOPTOSIS; CANCER CELL LINE; CANCER STEM CELL; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; CELL SURVIVAL; HUMAN; MALIGNANT NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; TRANSCRIPTION REGULATION; UBIQUITINATION; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; MOUSE; NEOPLASM; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NEOPLASMS; NEOPLASTIC STEM CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY;

EID: 85016923851     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1177/1010428317692248     Document Type: Review

References (124)

1. Simons BD, Clevers H., Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 2011; 145(6): 851–862.
2. Villadsen R, Fridriksdottir AJ, Rønnov-Jessen L. Evidence for a stem cell hierarchy in the adult human breast. J Cell Biol 2007; 177(1): 87–101.
3. Blanpain C, Fuchs E., Plasticity of epithelial stem cells in tissue regeneration. Science 2014; 344(6189): 1242281.
4. Vogelstein B, Papadopoulos N, Velculescu VE. Cancer genome landscape. Science 2013; 339: 1546–1558.
5. Al-Hajj M, Wicha MS, Benito-Hernandez A. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100(7): 3983–3988.
6. Ginestier C, Hur MH, Charafe-Jauffret E. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007; 15(1): 555–567.
7. Kozovska Z, Gabrisova V, Kucerova L., Colon cancer: cancer stem cells markers, drug resistance and treatment. Biomed Pharmacother 2014; 68(8): 911–916.
8. Reinisch A, Chan SM, Thomas D. Biology and clinical relevance of acute myeloid leukemia stem cells. Semin Hematol 2015; 52(3): 150–164.
9. Pine SR, Marshall B, Varticovski L., Lung cancer stem cells. Dis Markers 2008; 24(4–5): 257–266.
10. Hanahan D, Weinberg RA., Hallmarks of cancer: the next generation. Cell 2011; 144(5): 646–674.
11. Voutsadakis IA., Ubiquitin, ubiquitination and the ubiquitin-proteasome system in cancer. Atlas Genet Cytogen Oncol Haematol 2010, http://atlasgeneticsoncology.org/Deep/UbiquitininCancerID20083.html.
12. Okita Y, Nakayama KI., UPS delivers pluripotency. Cell Stem Cell 2012; 11: 728–730.
13. Teicher BA, Tomaszewski JE., Proteasome inhibitors. Biochem Pharmacol 2015; 96: 1–9.
14. Ramnath Pathare G, Nagy I, Bohn S. The proteasomal subunit Rpn6 is a molecular clamp holding the core and regulatory subcomplexes together. Proc Natl Acad Sci USA 2012; 109: 149–154.
15. Wolf DH, Hilt W., The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Biochim Biophys Acta 2004; 1695: 19–31.
16. Voutsadakis IA., The ubiquitin-proteasome system in colorectal cancer. Biochim Biophys Acta 2008; 1782: 800–808.
17. Baugh JM, Viktorova EG, Pilipenko EV., Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. J Mol Biol 2009; 386: 814–827.
18. Ebstein F, Kloetzel P-M, Krüger E. Emerging roles of immunoproteasomes beyond MHC class I antigen processing. Cell Mol Life Sci 2012; 69: 2543–2558.
19. Padmanabhan A, Anh-Thu Vuong S, Hochstrasser M., Assembly of an evolutionarily conserved alternative proteasome isoform in human cells. Cell Rep 2016; 14: 1–13.
20. Murata S, Yashiroda H, Tanaka K., Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol 2009; 10: 104–115.
21. Tran JR, Brodsky JL., The Cdc48–Vms1 complex maintains 26S proteasome architecture. Biochem J 2014; 458: 459–467.
22. Schröter F, Adjaye J., The proteasome complex and the maintenance of pluripotency: sustain the fate by mopping up? Stem Cell Res Ther 2014; 5: 24.
23. Finley D, Chen X, Walters KJ., Gates, channels, and switches: elements of the proteasome machine. Trends Biochem Sci 2016; 41: 77–93.
24. Tanahashi N, Murakami Y, Minami Y. Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J Biol Chem 2000; 275: 9055–9061.
25. Sun S-C., The noncanonical NF-κB pathway. Immunol Rev 2012; 246: 125–140.
26. Vlashi E, Kim K, Lagadec C. In vivo imaging, tracking, and targeting of cancer stem cells. J Natl Cancer Inst 2009; 101: 350–359.
27. Vlashi E, Lagadec C, Chan M. Targeted elimination of breast cancer cells with low proteasome activity is sufficient for tumor regression. Breast Cancer Res Treat 2013; 141: 197–203.
28. Tamari K, Hayashi K, Ishii H. Identification of chemoradiation-resistant osteosarcoma stem cells using an imaging system for proteasome activity. Int J Oncol 2014; 45: 2349–2354.
29. Lagadec C, Vlashi E, Bhuta S. Tumor cells with low proteasome subunit expression predict overall survival in head and neck cancer patients. BMC Cancer 2014; 14: 152.
30. Pan J, Zhang Q, Wang Y. 26S proteasome activity is down-regulated in lung cancer stem-like cells propagated in vitro. PLoS ONE 2010; 5: e13298.
31. Della Donna L, Lagadec C, Pajonk F. Radioresistance of prostate cancer cells with low proteasome activity. Prostate 2012; 72: 868–874.
32. Stacer AC, Wang H, Fenner J. Imaging reporters for proteasome activity identify tumor- and metastasis-initiating cells. Mol Imaging 2015; 14: 414–428.
33. Vlashi E, Mattes M, Lagadec C. Differential effects of the proteasome inhibitor NPI-0052 against glioma cells. Transl Oncol 2010; 3: 50–55.
34. Munakata K, Uemura M, Tanaka S. Cancer stem-like properties in colorectal cancer cells with low proteasome activity. Clin Cancer Res 2016; 22: 5277–5286.
35. Banno A, Garcia DA, van Baarsel ED. Downregulation of 26S proteasome catalytic activity promotes epithelial-mesenchymal transition. Oncotarget 2016; 7: 21527–21541.
36. Fellerhoff B, Gu S, Laumbacher B. The LMP7-K allele of the immunoproteasome exhibits reduced transcript stability and predicts high risk of colon cancer. Cancer Res 2011; 71: 7145–7154.
37. Voutsadakis IA., Pluripotency transcription factors in the pathogenesis of colorectal cancer and implications for prognosis. Biomark Med 2015; 9: 349–361.
38. Pilarsky C, Wenzig M, Specht T. Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia 2004; 6: 744–750.
39. Chen L, Madura K., Increased proteasome activity, ubiquitin-conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. Cancer Res 2005; 65: 5599–5606.
40. Bazzaro M, Lee MK, Zoso A. Ubiquitin-proteasome system stress sensitizes ovarian cancer to proteasome inhibitor-induced apoptosis. Cancer Res 2006; 66: 3754–3763.
41. Jia Z, Ai X, Sun F. Identification of new hub genes associated with bladder carcinoma via bioinformatics analysis. Tumori 2015; 101: 117–122.
42. Qi T, Zhang W, Luan Y. Proteomic profiling identified multiple short-lived members of the central proteome as the direct targets of the addicted oncogenes in cancer cells. Mol Cell Proteomics 2014; 13: 49–62.
43. Vilchez D, Boyer L, Morantte I. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 2012; 489: 304–308.
44. Atkinson SP, Collin J, Neganova I. A putative role for the immunoproteasome in the maintenance of pluripotency in human embryonic stem cells. Stem Cells 2012; 30: 1373–1384.
45. Buckley SM, Aranda-Orgilles B, Strikoudis A. Regulation of pluripotency and cellular reprogramming by the ubiquitin-proteasome system. Cell Stem Cell 2012; 11: 783–798.
46. Szutorisz H, Georgiou A, Tora L. The proteasome restricts permissive transcription at tissue-specific gene loci in embryonic stem cells. Cell 2006; 127: 1375–1388.
47. Hernebring M, Fredriksson Å, Liljevald M. Removal of damaged proteins during ES cell fate specification requires the proteasome activator PA28. Sci Rep 2013; 3: 1381.
48. Dai C, Miao CX, Xu XM. Transcriptional activation of human CDCA8 gene regulated by transcription factor NF-Y in embryonic stem cells and cancer cells. J Biol Chem 2015; 290: 22423–22434.
49. Dolfini D, Minuzzo M, Pavesi G. The short isoform of NF-YA belongs to the embryonic stem cell transcription factor circuitry. Stem Cells 2012; 30: 2450–2459.
50. Saez I, Viltchez D., The mechanistic links between proteasome activity, aging and age-related diseases. Curr Genomics 2014; 15: 38–51.
51. Imbriano C, Gnesutta N, Mantovani R., The NF-Y/p53 liaison: well beyond repression. Biochim Biophys Acta 2012; 1825: 131–139.
52. Ying S, Dünnebier T, Si J. Estrogen receptor alpha and nuclear factor Y coordinately regulate the transcription of the SUMO-conjugating UBC9 gene in MCF-7 breast cancer cells. PLoS ONE 2013; 8: e75695.
53. Xu H, Fu J, Ha S-W. The CCAAT box-binding transcription factor NF-Y regulates basal expression of human proteasome genes. Biochim Biophys Acta 2012; 1823: 818–825.
54. Su B, Luo T, Zhu J. Interleukin-1β/Interleukin-1 receptor-associated kinase 1 inflammatory signalling contributes to persistent Gankyrin activation during hepatocarcinogenesis. Hepatology 2015; 61: 585–597.
55. Lagadec C, Vlashi E, Frohnen P. The RNA-binding protein Musashi-1 regulates proteasome subunit expression in breast cancer- and glioma-initiating cells. Stem Cells 2014; 32: 135–144.
56. Carter S, Vousden KH., A role for Numb in p53 stabilization. Genome Biol 2008; 9: 221.
57. Plateroti M, de Araujo PR, Eduardo da, Silva A. The RNA-binding protein Musashi1: a major player in intestinal epithelium renewal and colon cancer development. Curr Colorectal Cancer Rep 2012; 8: 290–297.
58. Katz Y, Li F, Lambert NJ. Musashi proteins are post-transcriptional regulators of the epithelial-luminal cell state. Elife 2014; 3: e03915.
59. Okano H, Kawahara H, Toriya M. Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 2005; 306: 349–356.
60. Pastò A, Serafin V, Pilotto G. NOTCH3 signaling regulates MUSASHI-1 expression in metastatic colorectal cancer cells. Cancer Res 2014; 74: 2106–2118.
61. Voutsadakis IA., Epithelial-mesenchymal transition (EMT) and regulation of EMT factors by steroid nuclear receptors in breast cancer: a review and in silico investigation. J Clin Med 2016; 5: 1.
62. Powers GL, Ellison-Zelski SJ, Casa AJ. Proteasome inhibition represses ERalpha gene expression in ER+ cells: a new link between proteasome activity and estrogen signaling in breast cancer. Oncogene 2010; 29: 1509–1518.
63. Schmidt M, Finley D., Regulation of proteasome activity in health and disease. Biochim Biophys Acta 2014; 1843: 13–25.
64. Radhakrishnan SK, Lee CS, Young P. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol Cell 2010; 38: 17–28.
65. Steffen J, Seeger M, Koch A. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol Cell 2010; 40: 147–158.
66. Zhang Y, Nicholatos J, Dreier JR. Coordinated regulation of protein synthesis and degradation by mTORC1. Nature 2014; 513: 440–443.
67. Zhao J, Zhai B, Gygi SP. mTOR inhibition activates overall protein degradation by the ubiquitin proteasome system as well as by autophagy. Proc Natl Acad Sci USA 2015; 112: 15790–15797.
68. Vomhof-DeKrey EE, Picklo MJ, Sr. The Nrf2-antioxidant response element pathway: a target for regulating energy metabolism. J Nutr Biochem 2012; 23: 1201–1206.
69. Jang J, Wang Y, Kim H-S. Nrf2, a regulator of the proteasome, controls self-renewal and pluripotency in human embryonic stem cells. Stem Cells 2014; 32: 2616–2625.
70. Kapeta S, Chondrogianni N, Gonos ES., Nuclear erythroid factor 2-mediated proteasome activation delays senescence in human fibroblasts. J Biol Chem 2010; 285: 8171–8184.
71. Jaiswal AK., Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004; 36: 1199–1207.
72. Kwak M-K, Wakabayashi N, Greenlaw JL. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 2003; 23: 8786–8794.
73. Pickering AM, Linder RA, Zhang H. Nrf2-dependent induction of proteasome and Pa28αβ regulator are required for adaptation to oxidative stress. J Biol Chem 2012; 287: 10021–10031.
74. Achuthan S, Santhoshkumar TR, Prabhakar J. Drug-induced senescence generates chemoresistant stemlike cells with low reactive oxygen species. J Biol Chem 2011; 286: 37813–37829.
75. Zhu J, Wang H, Sun Q. Nrf2 is required to maintain the self-renewal of glioma stem cells. BMC Cancer 2013; 13: 380.
76. Kraft DC, Deocaris CC, Rattan SIS. Proteasomal oscillation during mild heat shock in aging human skin fibroblasts. Ann N Y Acad Sci 2006; 1067: 224–227.
77. Niture SK, Khatri R, Jaiswal AK., Regulation of Nrf2—an update. Free Radic Biol Med 2014; 66: 36–44.
78. Hayes JD, McMahon M., NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 2009; 34: 176–188.
79. Chang MT, Asthana S, Gao SP. Identifying recurrent mutations in cancer reveals widespread lineage diversity and mutational specificity. Nat Biotechnol 2016; 34: 155–163.
80. Moon EJ, Giaccia A., Dual roles of NRF2 in tumor prevention and progression: possible implications in cancer treatment. Free Radic Biol Med 2015; 79: 292–299.
81. Lecomte S, Desmots F, Le Masson F. Roles of heat shock factor 1 and 2 in response to proteasome inhibition: consequence on p53 stability. Oncogene 2010; 29: 4216–4224.
82. de Thonel A, Mezger V, Garrido C. Implication of heat shock factors in tumorigenesis: therapeutical potential. Cancers 2011; 3: 1158–1181.
83. Dai C, Whitesell L, Rogers AB. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007; 130: 1005–1018.
84. Björk JK, Åkerfelt M, Joutsen J. Heat-shock factor 2 is a suppressor of prostate cancer invasion. Oncogene 2016; 35: 1770–1784.
85. Mani SA, Guo W, Liao MJ. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704–715.
86. Voutsadakis IA., The network of pluripotency, epithelial–mesenchymal transition and prognosis of breast cancer. Breast Cancer 2015; 7: 303–319.
87. Vilchez D, Morantte I, Liu Z. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 2012; 489: 263–268.
88. Vilchez D, Boyer L, Lutz M. FOXO4 is necessary for neural differentiation of human embryonic stem cells. Aging Cell 2013; 12: 518–522.
89. Thomson M, Liu SJ, Zou L-N. Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 2011; 145: 875–889.
90. Paik J-H, Kollipara R, Chu G. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007; 128: 309–323.
91. Zhao J, Brault JJ, Schild A. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6: 472–483.
92. Reed SA, Sandesara PB, Senf SM. Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB J 2012; 26: 987–1000.
93. Milan G, Romanello V, Pescatore F. Regulation of autophagy and the ubiquitin-proteasome system by the FoxO transcriptional network during muscle atrophy. Nat Commun 2015; 6: 6670.
94. Matilainen O, Arpalahti L, Rantanen V. Insulin/IGF-1 signaling regulates proteasome activity through the deubiquitinating enzyme UBH-4. Cell Rep 2013; 3: 1980–1995.
95. Hughes R, Kristiansen M, Lassot I. NF-Y is essential for expression of the proapoptotic bim gene in sympathetic neurons. Cell Death Differ 2011; 18: 937–947.
96. Kip1. BMC Cancer 2011; 11: 99.
97. 12/13 inhibition enhances the anticancer effect of bortezomib through PSMB5 downregulation. Carcinogenesis 2010; 31: 1230–1237.
98. Vangala JR, Dudem S, Jain N. Regulation of PSMB5 protein and β subunits of mammalian proteasome by constitutively activated Signal Transducer and Activator of Transcription 3 (STAT3). J Biol Chem 2014; 289: 12612–12622.
99. Shao C, Sullivan JP, Girard L. Essential role of aldehyde dehydrogenase 1A3 for the maintenance of non-small cell lung cancer stem cells is associated with the STAT3 pathway. Clin Cancer Res 2014; 20: 4154–4166.
100. Silva KAS, Dong J, Dong Y. Inhibition of Stat3 activation suppresses caspase-3 and the ubiquitin-proteasome system, leading to preservation of muscle mass in cancer cachexia. J Biol Chem 2015; 290: 11177–11187.
101. Mine H, Sakurai T, Kashida H. Association of gankyrin and stemness factor expression in human colorectal cancer. Dig Dis Sci 2013; 58: 2337–2344.
102. Sun W, Ding J, Wu K. Gankyrin-mediated dedifferentiation facilitates the tumorigenicity of rat hepatocytes and hepatoma cells. Hepatology 2011; 54: 1259–1272.
103. GANK establishes a positive feedback loop in β-catenin signalling. Cell Res 2011; 21: 1248–1261.
104. Yang C, Tan Y, Yang G. Gankyrin has an antioxidative role through the feedback regulation of Nrf2 in hepatocellular carcinoma. J Exp Med 2016; 213: 859–875.
105. Lozano G, Zambetti GP., Gankyrin: an intriguing name for a novel regulator of p53 and RB. Cancer Cell 2005; 8: 3–4.
106. Qian Y-W, Chen Y, Yang W. p28(GANK) prevents degradation of Oct4 and promotes expansion of tumor-initiating cells in hepatocarcinogenesis. Gastroenterology 2012; 142: 1547–1558.
107. Xie Y., Feedback regulation of proteasome gene expression and its implications in cancer therapy. Cancer Metastasis Rev 2010; 29: 687–693.
108. Pritts TA, Hungness ES, Hershko DD. Proteasome inhibitors induce heat shock response and increase IL-6 expression in human intestinal epithelial cells. Am J Physiol Regul Integr Comp Physiol 2002; 282: R1016–R1026.
109. Luo X, Chen L, Dai J. Gankyrin gene deletion followed by proteomic analysis: insight into the roles of Gankyrin in tumorigenesis and metastasis. BMC Med Genomics 2012; 5: 36.
110. Zheng T, Hong X, Wang J. Gankyrin promotes tumor growth and metastasis through activation of IL-6/STAT3 signaling in human cholangiocarcinoma. Hepatology 2014; 59: 935–946.
111. Gatta R, Dolfini D, Mantovani R., NF-Y joins E2Fs, p53 and other stress transcription factors at the apoptosis table. Cell Death Dis 2011; 2: e162.
112. Moreno D, Viana R, Sanz P., Two-hybrid analysis identifies PSMD11, a non-ATPase subunit of the proteasome, as a novel interaction partner of AMP-activated protein kinase. Int J Biochem Cell Biol 2009; 41: 2431–2439.
113. Moiseeva TN, Bottrill A, Melino G. DNA damage-induced ubiquitylation of proteasome controls its proteolytic activity. Oncotarget 2013; 4: 1338–1348.
114. Besche HC, Sha Z, Kukushkin NV. Autoubiquitination of the 26S proteasome on Rpn13 regulates breakdown of ubiquitin conjugates. EMBO J 2014; 33: 1160–1176.
115. Ryu H, Gygi SP, Azuma Y. SUMOylation of Psmd1 controls Adrm1 interaction with the proteasome. Cell Rep 2014; 7: 1842–1848.
116. Rivett AJ, Bose S, Brooks P. Regulation of proteasome complexes by gamma-interferon and phosphorylation. Biochimie 2001; 83: 363–366.
117. Livneh I, Cohen-Kaplan V, Cohen-Rosenzweig C. The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Cell Res 2016; 26: 869–885.
118. Yang CH, Gonzalez-Angulo AM, Reuben JM. Bortezomib (VELCADE) in metastatic breast cancer: pharmacodynamics, biological effects, and prediction of clinical benefits. Ann Oncol 2006; 17: 813–817.
119. Markovic SN, Geyer SM, Dawkins F. A phase II study of Bortezomib in the treatment of metastatic malignant melanoma. Cancer 2005; 103: 2584–2589.
120. Chattopadhyay A, O’Connor CJ, Zhang F. Discovery of a small-molecule binder of the oncoprotein gankyrin that modulates gankyrin activity in the cell. Sci Rep 2016; 6: 23732.
121. Chapman AM, McNaughton BR., Synthetic proteins potently and selectively bind the oncoprotein gankyrin, modulate its interaction with S6 ATPase, and suppress gankyrin/MDM2-dependent ubiquitination of p53. ACS Chem Biol 2015; 10: 1880–1886.
122. Lee BH, Lee MJ, Park S. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 2010; 467: 179–184.
123. Nijhawan D, Zack TI, Ren Y. Cancer vulnerabilities unveiled by genomic loss. Cell 2012; 150: 842–854.
124. Zheng P, Zhou Z., Human cancer immunotherapy with PD-1/PD-L1 blockade. Biomark Cancer 2015; 7: 15–18.