NRF3-POMP-20S Proteasome Assembly Axis Promotes Cancer Development via Ubiquitin-Independent Proteolysis of p53 and Retinoblastoma Protein

REFERENCES

• Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646–674. https://doi.org/10.1016/j.cell.2011.02.013.
   PubMed Web of Science ®Google Scholar
• Luo J, Solimini NL, Elledge SJ. 2009. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136:823–837. https://doi.org/10.1016/j.cell.2009.02.024.
   PubMed Web of Science ®Google Scholar
• Collins GA, Goldberg AL. 2017. The logic of the 26S proteasome. Cell 169:792–806. https://doi.org/10.1016/j.cell.2017.04.023.
   PubMed Web of Science ®Google Scholar
• Asher G, Tsvetkov P, Kahana C, Shaul Y. 2005. A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev 19:316–321. https://doi.org/10.1101/gad.319905.
   PubMed Web of Science ®Google Scholar
• Sdek P, Ying H, Chang DLF, Qiu W, Zheng H, Touitou R, Allday MJ, Xiao Z-XJ. 2005. MDM2 promotes proteasome-dependent ubiquitin-independent degradation of retinoblastoma protein. Mol Cell 20:699–708. https://doi.org/10.1016/j.molcel.2005.10.017.
   PubMed Web of Science ®Google Scholar
• Koizumi S, Irie T, Hirayama S, Sakurai Y, Yashiroda H, Naguro I, Ichijo H, Hamazaki J, Murata S. 2016. The aspartyl protease DDI2 activates Nrf1 to compensate for proteasome dysfunction. Elife 5:e18357. https://doi.org/10.7554/eLife.18357.
   Google Scholar
• Chowdhury AMMA, Katoh H, Hatanaka A, Iwanari H, Nakamura N, Hamakubo T, Natsume T, Waku T, Kobayashi A. 2017. Multiple regulatory mechanisms of the biological function of NRF3 (NFE2L3) control cancer cell proliferation. Sci Rep 7:12494. https://doi.org/10.1038/s41598-017-12675-y.
   PubMed Web of Science ®Google Scholar
• Radhakrishnan SK, Lee CS, Young P, Beskow A, Chan JY, Deshaies RJ. 2010. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol Cell 38:17–28. https://doi.org/10.1016/j.molcel.2010.02.029.
   PubMed Web of Science ®Google Scholar
• Tsuchiya Y, Taniguchi H, Ito Y, Morita T, Karim MR, Ohtake N, Fukagai K, Ito T, Okamuro S, Iemura S, Natsume T, Nishida E, Kobayashi A. 2013. The casein kinase 2-Nrf1 axis controls the clearance of ubiquitinated proteins by regulating proteasome gene expression. Mol Cell Biol 33:3461–3472. https://doi.org/10.1128/MCB.01271-12.
   PubMed Web of Science ®Google Scholar
• Sha Z, Goldberg AL. 2014. Proteasome-mediated processing of Nrf1 is essential for coordinate induction of all proteasome subunits and p97. Curr Biol 24:1573–1583. https://doi.org/10.1016/j.cub.2014.06.004.
   PubMed Web of Science ®Google Scholar
• Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, Xie M, Zhang Q, McMichael JF, Wyczalkowski MA, Leiserson MDM, Miller CA, Welch JS, Walter MJ, Wendl MC, Ley TJ, Wilson RK, Raphael BJ, Ding L. 2013. Mutational landscape and significance across 12 major cancer types. Nature 502:333–339. https://doi.org/10.1038/nature12634.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Kensler TW, Motohashi H. 2018. The KEAP1-NRF2 system: a thiol-based sensor-effector apparatus for maintaining redox homeostasis. Physiol Rev 98:1169–1203. https://doi.org/10.1152/physrev.00023.2017.
   PubMed Web of Science ®Google Scholar
• Tanahashi N, Murakami Y, Minami Y, Shimbara N, Hendil KB, Tanaka K. 2000. Hybrid proteasomes. J Biol Chem 275:14336–14345. https://doi.org/10.1074/jbc.275.19.14336.
   PubMed Web of Science ®Google Scholar
• Fricke B, Heink S, Steffen J, Kloetzel PM, Krüger E. 2007. The proteasome maturation protein POMP facilitates major steps of 20S proteasome formation at the endoplasmic reticulum. EMBO Rep 8:1170–1175. https://doi.org/10.1038/sj.embor.7401091.
   PubMed Web of Science ®Google Scholar
• Kobayashi A, Ito E, Toki T, Kogame K, Takahashi S, Igarashi K, Hayashi N, Yamamoto M. 1999. Molecular cloning and functional characterization of a new cap’n’ collar family transcription factor Nrf3. J Biol Chem 274:6443–6452. https://doi.org/10.1074/jbc.274.10.6443.
   PubMed Web of Science ®Google Scholar
• Ben-Nissan G, Sharon M. 2014. Regulating the 20S proteasome ubiquitin-independent degradation pathway. Biomolecules 4:862–884. https://doi.org/10.3390/biom4030862.
   PubMedGoogle Scholar
• Hyer ML, Milhollen MA, Ciavarri J, Fleming P, Traore T, Sappal D, Huck J, Shi J, Gavin J, Brownell J, Yang Y, Stringer B, Griffin R, Bruzzese F, Soucy T, Duffy J, Rabino C, Riceberg J, Hoar K, Lublinsky A, Menon S, Sintchak M, Bump N, Pulukuri SM, Langston S, Tirrell S, Kuranda M, Veiby P, Newcomb J, Li P, Wu JT, Powe J, Dick LR, Greenspan P, Galvin K, Manfredi M, Claiborne C, Amidon BS, Bence NF. 2018. A small-molecule inhibitor of the ubiquitin activating enzyme for cancer treatment. Nat Med 24:186–193. https://doi.org/10.1038/nm.4474.
   PubMed Web of Science ®Google Scholar
• Manasanch EE, Orlowski RZ. 2017. Proteasome inhibitors in cancer therapy. Nat Rev Clin Oncol 14:417–433. https://doi.org/10.1038/nrclinonc.2016.206.
   PubMed Web of Science ®Google Scholar
• Milacic V, Banerjee S, Landis-Piwowar KR, Sarkar FH, Majumdar APN, Dou QP. 2008. Curcumin inhibits the proteasome activity in human colon cancer cells in vitro and in vivo. Cancer Res 68:7283–7292. https://doi.org/10.1158/0008-5472.CAN-07-6246.
   PubMed Web of Science ®Google Scholar
• Groll M, Berkers CR, Ploegh HL, Ovaa H. 2006. Crystal structure of the boronic acid-based proteasome inhibitor bortezomib in complex with the yeast 20S proteasome. Structure 14:451–456. https://doi.org/10.1016/j.str.2005.11.019.
   PubMed Web of Science ®Google Scholar
• Wang H, Zhan M, Yang R, Shi Y, Liu Q, Wang J. 2018. Elevated expression of NFE2L3 predicts the poor prognosis of pancreatic cancer patients. Cell Cycle 17:2164–2174. https://doi.org/10.1080/15384101.2018.1520558.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Flesken-Nikitin A, Corney DC, Wang W, Goodrich DW, Roy-Burman P, Nikitin AY. 2006. Synergy of p53 and Rb deficiency in a conditional mouse model for metastatic prostate cancer. Cancer Res 66:7889–7898. https://doi.org/10.1158/0008-5472.CAN-06-0486.
   PubMed Web of Science ®Google Scholar
• Soares KC, Foley K, Olino K, Leubner A, Mayo SC, Jain A, Jaffee E, Schulick RD, Yoshimura K, Edil B, Zheng L. 2014. A preclinical murine model of hepatic metastases. J Vis Exp 2014:51677. https://doi.org/10.3791/51677.
   Google Scholar
• Kajiro M, Hirota R, Nakajima Y, Kawanowa K, So-Ma K, Ito I, Yamaguchi Y, Ohie SH, Kobayashi Y, Seino Y, Kawano M, Kawabe YI, Takei H, Hayashi SI, Kurosumi M, Murayama A, Kimura K, Yanagisawa J. 2009. The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat Cell Biol 11:312–319. https://doi.org/10.1038/ncb1839.
   PubMed Web of Science ®Google Scholar
• Liu Y, Sethi NS, Hinoue T, Schneider BG, Cherniack AD, Sanchez-Vega F, Seoane JA, Farshidfar F, Bowlby R, Islam M, Kim J, Chatila W, Akbani R, Kanchi RS, Rabkin CS, Willis JE, Wang KK, McCall SJ, Mishra L, Ojesina AI, Bullman S, Pedamallu CS, Lazar AJ, Sakai R, Cancer Genome Atlas Research Network, Thorsson V, Bass AJ, Laird PW. 2018. Comparative molecular analysis of gastrointestinal adenocarcinomas. Cancer Cell 33:721–735. https://doi.org/10.1016/j.ccell.2018.03.010.
   PubMed Web of Science ®Google Scholar
• Aono S, Hatanaka A, Hatanaka A, Gao Y, Hippo Y, Taketo MM, Waku T, Kobayashi A. 2019. β-Catenin/TCF4 complex-mediated induction of the NRF3 (NFE2L3) gene in cancer cells. Int J Mol Sci 20:E3344. https://doi.org/10.3390/ijms20133344.
   Google Scholar
• Zhang X, Schulz R, Edmunds S, Krüger E, Markert E, Gaedcke J, Cormet-Boyaka E, Ghadimi M, Beissbarth T, Levine AJ, Moll UM, Dobbelstein M. 2015. MicroRNA-101 suppresses tumor cell proliferation by acting as an endogenous proteasome inhibitor via targeting the proteasome assembly factor POMP. Mol Cell 59:243–258. https://doi.org/10.1016/j.molcel.2015.05.036.
   PubMed Web of Science ®Google Scholar
• Maki CG, Huibregtse JM, Howley PM. 1996. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res 56:2649–2654.
   PubMed Web of Science ®Google Scholar
• Rubin SM. 2013. Deciphering the retinoblastoma protein phosphorylation code. Trends Biochem Sci 38:12–19. https://doi.org/10.1016/j.tibs.2012.10.007.
   PubMed Web of Science ®Google Scholar
• Ghebranious N, Donehower LA. 1998. Mouse models in tumor suppression. Oncogene 17:3385–3400. https://doi.org/10.1038/sj.onc.1202573.
   PubMed Web of Science ®Google Scholar
• Sherr CJ, McCormick F. 2002. The RB and p53 pathways in cancer. Cancer Cell 2:103–112. https://doi.org/10.1016/s1535-6108(02)00102-2.
   PubMed Web of Science ®Google Scholar
• Bardeesy N, Bastian BC, Hezel A, Pinkel D, DePinho RA, Chin L. 2001. Dual inactivation of RB and p53 pathways in RAS-induced melanomas. Mol Cell Biol 21:2144–2153. https://doi.org/10.1128/MCB.21.6.2144-2153.2001.
   PubMed Web of Science ®Google Scholar
• Kwak M-K, Wakabayashi N, Greenlaw JL, Yamamoto M, Kensler TW. 2003. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol Cell Biol 23:8786–8794. https://doi.org/10.1128/mcb.23.23.8786-8794.2003.
   PubMed Web of Science ®Google Scholar
• Walerych D, Lisek K, Sommaggio R, Piazza S, Ciani Y, Dalla E, Rajkowska K, Gaweda-Walerych K, Ingallina E, Tonelli C, Morelli MJ, Amato A, Eterno V, Zambelli A, Rosato A, Amati B, Wiśniewski JR, Del Sal G. 2016. Proteasome machinery is instrumental in a common gain-of-function program of the p53 missense mutants in cancer. Nat Cell Biol 18:897–909. https://doi.org/10.1038/ncb3380.
   PubMed Web of Science ®Google Scholar
• Li B, Fu J, Chen P, Ge X, Li Y, Kuiatse I, Wang H, Wang H, Zhang X, Orlowski RZ. 2015. The nuclear factor (erythroid-derived 2)-like 2 and proteasome maturation protein axis mediate bortezomib resistance in multiple myeloma. J Biol Chem 290:29854–29868. https://doi.org/10.1074/jbc.M115.664953.
   PubMed Web of Science ®Google Scholar
• Derjuga A, Gourley TS, Holm TM, Heng HHQ, Shivdasani RA, Ahmed R, Andrews NC, Blank V. 2004. Complexity of CNC transcription factors as revealed by gene targeting of the Nrf3 locus. Mol Cell Biol 24:3286–3294. https://doi.org/10.1128/mcb.24.8.3286-3294.2004.
   PubMed Web of Science ®Google Scholar
• Kobayashi A, Ohta T, Yamamoto M. 2004. Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes. Methods Enzymol 378:273–286. https://doi.org/10.1016/S0076-6879(04)78021-0.
   PubMed Web of Science ®Google Scholar
• Sivá M, Svoboda M, Veverka V, Trempe JF, Hofmann K, Kožíšek M, Hexnerová R, Sedlák F, Belza J, Brynda J, Šácha P, Hubálek M, Starková J, Flaisigová I, Konvalinka J, Šašková KG. 2016. Human DNA-damage-inducible 2 protein is structurally and functionally distinct from its yeast ortholog. Sci Rep 6:30443. https://doi.org/10.1038/srep30443.
   PubMed Web of Science ®Google Scholar
• Kraus M, Müller-Ide H, Rückrich T, Bader J, Overkleeft H, Driessen C. 2014. Ritonavir, nelfinavir, saquinavir and lopinavir induce proteotoxic stress in acute myeloid leukemia cells and sensitize them for proteasome inhibitor treatment at low micromolar drug concentrations. Leuk Res 38:383–392. https://doi.org/10.1016/j.leukres.2013.12.017.
   PubMed Web of Science ®Google Scholar
• Kawabata S, Gills JJ, Mercado-Matos JR, LoPiccolo J, Wilson W, III, Hollander MC, Dennis PA. 2012. Synergistic effects of nelfinavir and bortezomib on proteotoxic death of NSCLC and multiple myeloma cells. Cell Death Dis 3:e353. https://doi.org/10.1038/cddis.2012.87.
   Google Scholar
• Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW, Vogelstein B. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282:1497–1501. https://doi.org/10.1126/science.282.5393.1497.
   PubMed Web of Science ®Google Scholar
• Hamazaki J, Iemura SI, Natsume T, Yashiroda H, Tanaka K, Murata S. 2006. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J 25:4524–4536. https://doi.org/10.1038/sj.emboj.7601338.
   PubMed Web of Science ®Google Scholar
• Murata S, Sasaki K, Kishimoto T, Niwa SI, Hayashi H, Takahama Y, Tanaka K. 2007. Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316:1349–1353. https://doi.org/10.1126/science.1141915.
   PubMed Web of Science ®Google Scholar
• Kaneko T, Hamazaki J, Iemura S, Sasaki K, Furuyama K, Natsume T, Tanaka K, Murata S. 2009. Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137:914–925. https://doi.org/10.1016/j.cell.2009.05.008.
   PubMed Web of Science ®Google Scholar
• Wu W, Sahara K, Hirayama S, Zhao X, Watanabe A, Hamazaki J, Yashiroda H, Murata S. 2018. PAC1-PAC2 proteasome assembly chaperone retains the core α4-α7 assembly intermediates in the cytoplasm. Genes Cells 23:839–848. https://doi.org/10.1111/gtc.12631.
   PubMed Web of Science ®Google Scholar
• Murata S, Udono H, Tanahashi N, Hamada N, Watanabe K, Adachi K, Yamano T, Yui K, Kobayashi N, Kasahara M, Tanaka K, Chiba T. 2001. Immunoproteasome assembly and antigen presentation in mice lacking both PA28α and PA28β. EMBO J 20:5898–5907. https://doi.org/10.1093/emboj/20.21.5898.
   PubMed Web of Science ®Google Scholar
• Nakajima Y, Osakabe A, Waku T, Suzuki T, Akaogi K, Fujimura T, Homma Y, Inoue S, Yanagisawa J. 2016. Estrogen exhibits a biphasic effect on prostate tumor growth through the ERβ-KLF5 pathway. Mol Cell Biol 36:144–156. https://doi.org/10.1128/MCB.00625-15.
   PubMed Web of Science ®Google Scholar
• Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z. 2017. GEPIA: a Web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res 45:W98–W102. https://doi.org/10.1093/nar/gkx247.
   PubMed Web of Science ®Google Scholar