Abstract
The review describes the characteristics of the ubiquitin-proteasome system involved in proteins degradation and its role in the transition of pretumor changes of the epithelium to cancer. According to modern concepts, the ubiquitin-proteasome system is actively involved in the regulation of numerous intracellular processes, such as proliferation, apoptosis, differentiation, which play an important role in the development of tumors. Main target proteins which have been shown to be cleaved in proteasomes, can participate in carcinogenesis. Detailed research of the ubiquitin-proteasome system will reveal the specific mechanisms involved in the transition of precancerous diseases to malignant neoplasms.
Authors and affiliations
E.A. Sidenko, G.V. Kakurina, O.V. Cheremisina, E.E. Shashova, E.S. Kolegova, I.V. Kondakova Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Kooperativny Street, 5, Tomsk, 634050, Russian Federation E-mail: sidenkoevgeniyaaleksandrovna@gmail.com
References
Bray F., Ferlay J., Soerjomataram I., Siegel R. L., Torre L. A., Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: a cancer journal for clinicians. 2015; 68 (6): 394–424. https://doi.org/10.3322/caac.2149
Kaprin A.D., Starinskij V.V., Petrova G.V. Zlokachestvennye novoobrazovanija v Rossii v 2017 g. (zabolevaemost' i smertnost'). M.: MNIOI im. P.A. Gertsena – filial FGBU «NMITs radiologii» Minzdrava Rossii, 2018; 250. [Kaprin A.D., Starinskij V.V., Petrova G.V. Malignant neoplasms in Russia in 2017 (morbidity and mortality). M.: Moscow Research Institute of Oncology named after P.A. Herzen – branch of the FSBI «NMITs radiology» of the Ministry of Health of Rus- sia, 2018; 250 (in Russian)]
Hu J.X., Helleberg M., Jensen A.B., Brunak S., Lundgren J.A Large-Cohort, Longitudi- nal Study Determines Precancer Disease Routes across Different Cancer Types. Can- cer research. 2019; 79 (4): 864–72. https:// doi.org/10.1158/0008 5472.CAN-18-1677
Sycheva N.L., Faustov L.A. Endokrinnyj komponent rannej onkologicheskoj patologii pri eksperimental'nom rake kishechnika. Nauchnyj rezul'tat. Meditsina i farmatsija. 2017; 3 (1): 15–23. https:// doi.org/10.18413/2313-8955-2017-3-1-15-23 [Sycheva N.L., Faustov L.A. Endocrine component of early oncologic pathol- ogy in experimental cancer of bowels. Research result. Medicine and pharmacy. 2017; 3 (1): 15–23 (in Russian). https://doi. org/10.18413/2313-8955-2017-3-1-15-23]
Rajalekshmi M., Shreedhara C.S., Lobo R., Rao P.P. The Review on Genetics, Epigenetics, Risk Factors and Diagnosis of Colon Cancer. Research J. Pharm. and Tech. 2018; 11 (11): 5147–51. https://doi. org/10.5958/0974-360X.2018.00940.X
Tabakman Ju.Ju., Solopova A.G., Bishtavi A., Idrisova L.E. Predrak endometrija: opredelenie ponjatija, taktika. Akusher- stvo, ginekologija i reproduktsija. 2016; 10 (2): 32–6. https://doi.org/10.17749/2313- 7347.2016.10.2.032-036 [Tabakman Yu.Yu., Solopova A.G., Bishtavi A.Kh., Idrisova L.E. Endometrial precancer: definition of concepts, tactics. Akush- erstvo, ginekologiya i reproduktsiya / Obstetrics, gynecology and reproduction. 2016; 10 (2): 32–6 (in Russian). https://doi. org/10.17749/2313-7347.2016.10.2.032-036]
Avila D.D., D’Ávila J., Góis C., Barretto L. Premalignant laryngeal lesions: twenty- year experience in specialized service. Int. Arch. Otorhinolaryngol. 2014; 18 (4): 352–6. https://doi.org/10.1055/s-0034-1376431
Mihaleva L.M., Birjukov A.E., Poljanko N.I. Predrakovye porazhenija i rannij rak zheludka: sovremennye kliniko- morfologicheskie dannye. Klinicheskaja meditsina. 2017; 95 (10): 881–7. https://doi. org/10.18821/0023-2149-2017-95-10-881-887 [Mikhaleva L.M., Birukov A.E., Polyanko N.I. Precancerous lesions and early gastric cancer: modern clinical-morphological data. 2017; 95 (10): 881–7 (in Russian). https://doi.org/10.18821/0023-2149-2017- 95-10-881-887]
Varshavsky A. The ubiquitin system, autophagy, and regulated protein deg- radation. Annu. Rev. Biochem. 2017; 86: 123–8. https://doi.org/10.1146/annurev- biochem-061516-044859
Tsimoha A.S. Proteasomy: uchastie v kletochnyh protsessah. Tsitologija. 2010; 52 (4): 277–300. [Tsimokha A.S. Proteasomes: their role in cellular processes. Cytology. 2010; 52 (4): 277–300 (in Russian)]
Schmidt M., Finley D. Regulation of pro- teasome activity in health and disease. Biochimica et Biophysica Acta. 2014; 1843 (1): 13–25. https://doi.org/10.1016/j. bbamcr.2013.08.012
Kish-Trier E., Hill C.P. Structural biology of the proteasome. Annu. Rev. Biophys. 2013; 42: 29–49. https://doi.org/10.1146/annurev- biophys-083012-130417
Sorokin A.V., Kim E.R., Ovchinnikov L.P. Proteasomnaja sistema degradatsii i protsessinga belkov. Uspehi biologicheskoj himii. 2009; 49: 3–76. [Sorokin A.V., Kim E.R., Ovchinnikov L.P. Proteasome system of degradation and processing of proteins. Uspekhi Biologich- eskoi Khimii. 2009; 49: 3–76 (in Russian)]
Baugh J.M., Viktorova E.G., Pilipenko E.V. Proteasomes can degrade a significant proportion of cellular proteins independ- ent of ubiquitination. J. Mol. Biol. 2009; 386 (3): 814–27. https://doi.org/10.1016/j. jmb.2008.12.081
Kumar Deshmukh F., Yaffe D., Olshina M.A., Ben-Nissan G., Sharon M. The Contribu- tion of the 20S Proteasome to Proteostasis. Biomolecules. 2019; 9 (5): 190. https://doi. org/10.3390/biom9050190
Raynes R., Pomatto L.C., Davies K.J. Degra- dation of oxidized proteins by the protea- some: distinguishing between the 20S, 26S, and immunoproteasome proteolytic pathways. Mol. Asp. Med. 2016; 50: 41–55. https://doi.org/10.1016/j.mam.2016.05.001
Ben-Nissan G., Sharon M. Regulating the 20S proteasome ubiquitin-independent degradation pathway. Biomolecules. 2014; 4 (3): 862–84. https://doi.org/10.3390/ biom4030862
Silva G.M., Netto L.E., Simoes V., Santos L.F., Gozzo F.C., Demasi M.A., Oliveira C.L., Bicev R.N., Klitzke C.F., Sogayar M.C., Demasi M. Redox control of 20S protea- some gating. Antioxidants & redox signal- ing. 2012; 16 (11): 1183–94. https://doi. org/10.1089/ars.2011.4210
Olshina M.A., Ben-Nissan G., Sharon M. Functional regulation of proteins by 20S proteasome proteolytic processing. Cell Cycle. 2018; 17 (4): 393–4. https://doi.org/1 0.1080/15384101.2017.1414682
Chen S., Wu J., Lu Y., Ma Y.B., Lee B.H., Yu Z., Ouyang Q., Finley D.J., Kirschner M.W., Mao Y. Structural basis for dynamic regulation of the human 26S proteasome. PNAS. 2016; 113 (46): 12991–6. https://doi.org/10.1073/ pnas.1614614113
Schweitzer A., Aufderheide A., Rudack T., Beck F., Pfeifer G., Plitzko J.M., Sakata E., Schulten K., Förster F., Baumeister W. Structure of the human 26S proteasome at a resolution of 3.9 Å. PNAS. 2016; 113 (28): 7816–21. https://doi.org/10.1073/ pnas.1608050113
Kondakova I.V., Spirina L.V., Koval' V.D., Shashova E.E., Chojnzonov E.L., Ivano- va E.V., Kolomiets L.A., Chernyshova A.L., Slonimskaja E.M., Usynin E.A., Afanas'ev S.G. Himotripsinpodobnaja aktivnost' i sub'edinichnyj sostav proteasom v zlokachestvennyh opuholjah cheloveka. Mo lekuljarnaja biologija. 2014; 48 (3): 444–51. https://doi.org/10.7868/S0026898414030112 [Kondakova I.V., Spirina L.V., Koval V.D., Shashova E.E., Choinzonov E.L., Ivanova E.V., Kolomiets L.A., Chernyshova A.L., Slonimskaya E.M., Usynin E.A., Afanas’ev S.G. Chymotripsin-like activity and subunit composition of proteasomes in human cancers. Molecular biology. 2014; 48 (3): 444–51 (in Russian). https://doi.org/10.7868/ S0026898414030112]
Ivanova E.V., Kondakova I.V., Spirina L.V., Afanas’ev S.G., Avgustinovich A.V., Cher- emisina O.V. Chymotrypsin-like activity of proteasomes and total calpain activity in gastric and colorectal cancer. Bulletin of Experimental Biology and Medicine. 2014; 157 (6): 781–4. https://doi.org/10.1007/ s10517-014-2666-y
Shashova E. E., Astahova T.M., Plehanova A.S., Bogomjagkova Ju.V., Ljupina Ju.V., Sumedi I.R., Slonimskaja E.M., Erohov P.A., Abramova E.B., Rodoman G.V., Kuznetsov N.A., Kondakova I.V., Sharova N.P., Chojnzonov E.L. Izmenenie himotripsinpodobnoj aktivnosti proteasom v razvitii kartsinom molochnoj i schitovidnoj zhelez cheloveka. Bjulleten' eksperimental'noj biologii i meditsiny. 2013; 156 (8): 209–11. [Shashova E. E., Astahova T.M., Plehanova A.S., Bogomjagkova Ju.V., Ljupina Ju.V., Sumedi I.R., Slonimskaja E.M., Erohov P.A., Abramova E.B., Rodoman G.V., Kuznecov N.A., Kondakova I.V., Sharova N.P., Chojnzo- nov E.L. Changes in proteasome chymot- rypsin-like activity during the development of human mammary and thyroid carcino- mas. Bulletin of Experimental Biology and Medicine. 2013; 156 (8): 209–11 (in Russian)]
Le-Bel G., Benhassine M., Landreville S., Guérin S.L. Analysis of the proteasome activity and the turnover of the seroto- nin receptor 2B (HTR2B) in human uveal melanoma. Exp. Eye Res. 2019; 184: 72–7. https://doi.org/10.1016/j.exer.2019.04.013
Shashova E.E., Lyupina Y.V., Glushchenko S.A., Slonimskaya E.M., Savenkova O.V., Kulikov A.M., Gornostaev N.G., Kondakova I.V., Sharova N.P. Proteasome functioning in breast cancer: connection with clinical- pathological factors. PLoS One. 2014; 9 (10): e109933. https://doi.org/10.1371/jour- nal.pone.0109933
FeiFei W., HongHai X., YongRong Y., PingXi- ang W., JianHua W., XiaoHui Z., JiaoYing L., JingBo S., Kun Z., XiaoLi R., Lu Q., XiaoLiang L., ZhiQiang C., Na T., WenTing L., YanQing D., Li L. FBX8 degrades GSTP1 through ubiq- uitination to suppress colorectal cancer progression. Cell death & disease. 2019; 10 (5): 351. https://doi.org/10.1038/s41419- 019-1588-z
Chen L., Zhu G., Johns E.M., Yang, X. TRIM11 activates the proteasome and promotes overall protein degradation by regulating USP14. Nature communications. 2018; 9 (1): 1223. https://doi.org/10.1038/s41467-018- 03499-z
Cai M.J., Cui Y., Fang M., Wang Q., Zhang A.J., Kuai J.H., Pang F., Cui X.D. Inhibition of PSMD4 blocks the tumorigenesis of hepatocellular carcinoma. Gene. 2019; 702: 66–74. https://doi.org/10.1016/j. gene.2019.03.063
Shashova E.E., Kolegova E.S., Kondakova I.V., Zav'jalov A.A. Vnutrikletochnyj i tsirkulirujuschij puly proteasom: znache- nie pri zlokachestvennyh novoobrazova- nijah razlichnyh lokalizatsij. Sibirskij onkologicheskij zhurnal. 2015; 6: 76–82. [Shashova E.E., Kolegova E.S., Kondakova I.V., Zav’jalov A.A. The intracellular and circulating pools of proteasomes: the value at cancer in different locations. Siberian journal of oncology. 2015; 6: 76–82 (in Rus )]
Pecci A., Necchi V., Barozzi S., Vitali A., Boveri E., Elena C., Bernasconi P., Noris P., Solcia E. Particulate cytoplasmic structures with high concentration of ubiquitin- proteasome accumulate in myeloid neo- plasms. Journal of hematology & oncol- ogy. 2015; 8 (1): 71. https://doi.org/10.1186/ s13045-015-0169-6
Kondakova I.V., Kakurina G.V., Spirina L.V., Cheremisina O.V., Pankova O.V., Men'shikov K.Ju. Otsenka vnekletochnogo i vnutrikletochnogo proteoliza pri predopuholevyh i opuholevyh zabolevanijah gortani. Sibirskij onkologicheskij zhurnal. 2014; 3: 45–50. [Kondakova I.V., Kakurina G.V., Spirina L.V., Cheremisina O.V., Pankova O.V., Men’shikov K.Ju. Assessment of extracellu lar and intracellular proteolysis in pretumor and tumor diseases of the larynx. Siberian J. of oncology. 2014; 3: 45–50 (in Russian)]
Spirina L.V., Kondakova I.V., Kolomiets L.A., Chernyshova A.L., Asadchikova O.N., Sharova N.P., Koval' V.D. Aktivnost' proteasom i ih sub'edinichnyj sostav pri giperplasticheskih protsessah i rake endometrija. Opuholi zhenskoj reproduktivnoj sistemy. 2011; 4: 64–8. [Spirina L.V., Kondakova I.V., Kolomiec L.A., Chernyshova A.L., Asadchikova O.N., Sharova N.P., Koval’ V.D. Proteasome activ- ity and subunit composition in endometrial hyperplasia and cancer. Opuholi ženskoj reproduktivnoj sistemy. 2011; 4: 64–8 (in Russian)]
Furuyama T., Tanaka S., Shimada S., Akiy- ama Y., Matsumura S., Mitsunori Y., Aihara A., Ban D., Ochiai T., Kudo A., Fukamachi1 H., Arii S., Kawaguchi Y., Tanabe M. Protea- some activity is required for the initiation of precancerous pancreatic lesions. Sci- entific reports. 2016; 6: 27044. https://doi. org/10.1038/srep27044
Zhong J.L., Huang C.Z. Ubiquitin protea- some system research in gastrointestinal cancer. World J. Gastrointest. Oncol. 2016; 8 (2): 198–206. https://doi.org/10.4251/ wjgo.v8.i2.198
Kunjappu M.J., Hochstrasser M. Assembly of the 20S proteasome. Biochimica et Bio- physica Acta. 2014; 1843 (1): 2–12. https:// doi.org/10.1016/j.bbamcr.2013.03.008
Nosareva O.L., Stepovaja E.A., Rjazantseva N.V., Shahristova E.V., Orlov D. S., Novitskij V.V. Ubikvitin i reguljatsija apoptoza opuholevyh kletok linii Jurkat. Bjulleten' sibirskoj meditsiny. 2018; 17 (3): 96–104. https://doi. org/10.20538/1682-0363-2018-3-96–104. [Nosareva O.L., Stepovaja E.A., Rjazance- va N.V., Shahristova E.V., Orlov D. S., Novickij V.V. Ubiquitin and regulation of apoptosis in Jurkat cells. Bulletin of Siberian Medicine. 2018; 17 (3): 96–104 (in Russian). https://doi. org/10.20538/1682-0363-2018-3-96–104]
Zeng W., Wei X., Xie K., Diao P., Tang P. Potential use of chymotrypsin-like proteasomal activity as a biomarker for prostate cancer. Oncology letters. 2018; 15 (4): 5149–54. https://doi.org/10.3892/ ol.2018.7936
Pavlides S.C., Lecanda J., Daubriac J., Pandya U.M., Gama P., Blank S., Mittal K., Shukla P., Gold L.I. TGF-β activates APC through Cdh1 binding for Cks1 and Skp2 proteasomal destruction stabilizing p27kip1 for normal endometrial growth. Cell Cycle. 2016; 15 (7): 931–47. https://doi.org/10.1080 /15384101.2016.1150393
Chen H., Liu H., Qing G. Targeting oncogenic Myc as a strategy for can- cer treatment. Signal transduction andtargeted therapy. 2018; 3 (1): 5. https://doi. org/10.1038/s41392-018-0008-7
Schoedel J., Grampp S., Maher E.R., Moch H., Ratcliffe P.J., Russo P., Mole D.R. Hypox- ia, hypoxia-inducible transcription factors, and renal cancer. European urology. 2016; 69 (4): 646–57. https://doi.org/10.1016/j. eururo.2015.08.007
Rorsman C., Tsioumpekou M., Heldin C.H., Lennartsson J. The ubiquitin ligases c-Cbl and Cbl-b negatively regulate platelet- derived growth factor (PDGF) BB-induced chemotaxis by affecting PDGF receptor β (PDGFRβ) internalization and signaling. Journal of Biological Chemistry. 2016; 291 (22): 11608–18. https://doi.org/10.1074/jbc. M115.705814
Kravtsova-Ivantsiv Y., Shomer I., Cohen-Ka- plan V., Snijder B., Superti-Furga G., Gonen H., Sommer T., Ziv T., Admon A., Naroditsky I., Jbara M., Brik Ashraf., Pikarsky E., Tae Kwon Y., Doweck I., Ciechanover A. KPC1- mediated ubiquitination and proteasomal processing of NF-κB1 p105 to p50 restricts tumor growth. Cell. 2015; 161 (2): 333–47.
Helzer K.T., Hooper C., Miyamoto S., Alarid E.T. Ubiquitylation of nuclear receptors: new linkagesandtherapeuticimplications.Journal of molecular endocrinology. 2015; 54 (3): 151–67.https://doi.org/10.1530/JME-14-0308
Ibañez-Vega J., Batalla F.D. V., Saez J.J., Soza A., Yuseff M.I. Proteasome depend- ent actin remodeling facilitates antigen extraction at the immune synapse of B cells. Frontiers in immunology. 2019; 10: 225. https://doi.org/10.3389/fim- mu.2019.00225
Jeong D.H., Choi Y.N., Seo T.W., Lee J.S., Yoo S.J. Ubiquitin-proteasome dependent regulation of Profilin2 (Pfn2) by a cellular inhibitor of apoptotic protein 1 (cIAP1). Biochemical and Biophysical Research Communications. 2018; 506 (3): 423–8. https://doi.org/10.1016/j.bbrc.2018.10.11