Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Letters
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-1074 Online ISSN: 1792-1082
Journal Cover
February-2024 Volume 27 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
February-2024 Volume 27 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review Open Access

Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review)

  • Authors:
    • Yun Tao
    • Xiaohong Xu
    • Rong Shen
    • Xiaobing Miao
    • Song He
  • View Affiliations / Copyright

    Affiliations: Department of Pathology, Affiliated Tumor Hospital of Nantong University, Nantong, Jiangsu 226000, P.R. China, Department of Hematological Oncology, Affiliated Tumor Hospital of Nantong University, Nantong, Jiangsu 226000, P.R. China, Department of Pathology, Affiliated Tumor Hospital of Nantong University, Nantong, Jiangsu 226000, P.R. China
    Copyright: © Tao et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 58
    |
    Published online on: December 14, 2023
       https://doi.org/10.3892/ol.2023.14191
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Ubiquitin‑specific protease 13 (USP13) is one of the most important deubiquitinases involved in various diseases. As deubiquitinases are components of the deubiquitination process, a significant post‑translational modification, they are potential treatment targets for different diseases. With recent technological developments, the structure of USP13 and its pathological and physiological functions have been investigated. However, USP13 expression and function differ in various diseases, especially in tumors, and the associated mechanisms are complex and remain to be fully investigated. The present review summarized the recent discoveries and the current understanding of the USP13 function in tumors.
View Figures

Figure 1

Figure 2

View References

1 

Akutsu M, Dikic I and Bremm A: Ubiquitin chain diversity at a glance. J Cell Sci. 129:875–880. 2016.PubMed/NCBI

2 

Zhang YH, Zhou CJ, Zhou ZR, Song AX and Hu HY: Domain analysis reveals that a deubiquitinating enzyme USP13 performs non-activating catalysis for Lys63-linked polyubiquitin. PLoS One. 6:e293622011. View Article : Google Scholar : PubMed/NCBI

3 

Talreja J, Bauerfeld C, Wang X, Hafner M, Liu Y and Samavati L: MKP-1 modulates ubiquitination/phosphorylation of TLR signaling. Life Sci Alliance. 4:e2021011372021. View Article : Google Scholar : PubMed/NCBI

4 

Liu X and Moussa C: Regulatory role of ubiquitin specific protease-13 (USP13) in misfolded protein clearance in neurodegenerative diseases. Neuroscience. 460:161–166. 2021. View Article : Google Scholar : PubMed/NCBI

5 

Loix M, Zelcer N, Bogie JFJ and Hendriks JJA: The ubiquitous role of ubiquitination in lipid metabolism. Trends Cell Biol. S0962-8924(23)00192-7. 2023. View Article : Google Scholar : PubMed/NCBI

6 

Ciechanover A and Ben-Saadon R: N-terminal ubiquitination: More protein substrates join in. Trends Cell Biol. 14:103–106. 2004. View Article : Google Scholar : PubMed/NCBI

7 

Wang X, Herr RA, Chua WJ, Lybarger L, Wiertz EJ and Hansen TH: Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol. 177:613–624. 2007. View Article : Google Scholar : PubMed/NCBI

8 

Nathan JA, Kim HT, Ting L, Gygi SP and Goldberg AL: Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? EMBO J. 32:552–565. 2013. View Article : Google Scholar : PubMed/NCBI

9 

Liu P, Gan W, Su S, Hauenstein AV, Fu TM, Brasher B, Schwerdtfeger C, Liang AC, Xu M and Wei W: K63-linked polyubiquitin chains bind to DNA to facilitate DNA damage repair. Sci Signal. 11:eaar81332018. View Article : Google Scholar : PubMed/NCBI

10 

Wing SS: Deubiquitinating enzymes-the importance of driving in reverse along the ubiquitin-proteasome pathway. Int J Biochem Cell Biol. 35:590–605. 2003. View Article : Google Scholar : PubMed/NCBI

11 

Scortegagna M, Subtil T, Qi J, Kim H, Zhao W, Gu W, Kluger H and Ronai ZA: USP13 enzyme regulates Siah2 ligase stability and activity via noncatalytic ubiquitin-binding domains. J Biol Chem. 286:27333–27341. 2011. View Article : Google Scholar : PubMed/NCBI

12 

Clague MJ, Urbe S and Komander D: Breaking the chains: Deubiquitylating enzyme specificity begets function. Nat Rev Mol Cell Biol. 20:338–352. 2019. View Article : Google Scholar : PubMed/NCBI

13 

Morgan EL, Patterson MR, Barba-Moreno D, Scarth JA, Wilson A and Macdonald A: The deubiquitinase (DUB) USP13 promotes Mcl-1 stabilisation in cervical cancer. Oncogene. 40:2112–2129. 2021. View Article : Google Scholar : PubMed/NCBI

14 

Zeng Q, Li Z, Zhao X, Guo L, Yu C, Qin J, Zhang S, Zhang Y and Yang X: Ubiquitin-specific protease 7 promotes osteosarcoma cell metastasis by inducing epithelial-mesenchymal transition. Oncol Rep. 41:543–551. 2019.PubMed/NCBI

15 

Timms KM, Ansari-Lari MA, Morris W, Brown SN and Gibbs RA: The genomic organization of isopeptidase T-3(ISOT-3), a new member of the ubiquitin specific protease family (UBP). Gene. 217:101–106. 1998. View Article : Google Scholar : PubMed/NCBI

16 

Ren H, Mu W and Xu Q: miR-19a-3p inhibition alleviates sepsis-induced lung injury via enhancing USP13 expression. Acta Biochim Pol. 68:201–206. 2021.PubMed/NCBI

17 

Biterge Sut B: Molecular profiling of immune cell-enriched Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) interacting protein USP13. Life Sci. 258:1181702020. View Article : Google Scholar : PubMed/NCBI

18 

Yu F, Li Y, Ye Q, Miao J, Taleb SJ, Zhao Y and Zhao J: Lipopolysaccharide reduces USP13 stability through c-Jun N-terminal kinase activation in Kupffer cells. J Cell Physiol. 236:4360–4368. 2021. View Article : Google Scholar : PubMed/NCBI

19 

Darling S, Fielding AB, Sabat-Pospiech D, Prior IA and Coulson JM: Regulation of the cell cycle and centrosome biology by deubiquitylases. Biochem Soc Trans. 45:1125–1136. 2017. View Article : Google Scholar : PubMed/NCBI

20 

Sun H, Zhang Q, Jing YY, Zhang M, Wang HY, Cai Z, Liuyu T, Zhang ZD, Xiong TC, Wu Y, et al: USP13 negatively regulates antiviral responses by deubiquitinating STING. Nat Commun. 8:155342017. View Article : Google Scholar : PubMed/NCBI

21 

Wang J, Liu Y, Tang L, Qi S, Mi Y, Liu D and Tian Q: Identification of candidate substrates of ubiquitin-specific protease 13 using 2D-DIGE. Int J Mol Med. 40:47–56. 2017. View Article : Google Scholar : PubMed/NCBI

22 

Xie X, Matsumoto S, Endo A, Fukushima T, Kawahara H, Saeki Y and Komada M: Deubiquitinases USP5 and USP13 are recruited to and regulate heat-induced stress granules by deubiquitinating activities. J Cell Sci. 131:jcs2108562018. View Article : Google Scholar : PubMed/NCBI

23 

Zhang Y, Jiang C, Li H, Lv F, Li X, Qian X, Fu L, Xu B and Guo X: Elevated Aurora B expression contributes to chemoresistance and poor prognosis in breast cancer. Int J Clin Exp Pathol. 8:751–757. 2015.PubMed/NCBI

24 

Antao AM, Kaushal K, Das S, Singh V, Suresh B, Kim KS and Ramakrishna S: USP48 governs cell cycle progression by regulating the protein level of Aurora B. Int J Mol Sci. 22:85082021. View Article : Google Scholar : PubMed/NCBI

25 

Borah NA and Reddy MM: Aurora Kinase B Inhibition: A potential therapeutic strategy for cancer. Molecules. 26:19812021. View Article : Google Scholar : PubMed/NCBI

26 

Punt S, Malu S, McKenzie JA, Manrique SZ, Doorduijn EM, Mbofung RM, Williams L, Silverman DA, Ashkin EL, Dominguez AL, et al: Aurora kinase inhibition sensitizes melanoma cells to T-cell-mediated cytotoxicity. Cancer Immunol Immunother. 70:1101–1113. 2021. View Article : Google Scholar : PubMed/NCBI

27 

Gonzalez-Loyola A, Fernandez-Miranda G, Trakala M, Partida D, Samejima K, Ogawa H, Cañamero M, de Martino A, Martínez-Ramírez Á, de Cárcer G, et al: Aurora B overexpression causes aneuploidy and p21Cip1 repression during tumor development. Mol Cell Biol. 35:3566–3578. 2015. View Article : Google Scholar : PubMed/NCBI

28 

Chen M, Gutierrez GJ and Ronai ZA: Ubiquitin-recognition protein Ufd1 couples the endoplasmic reticulum (ER) stress response to cell cycle control. Proc Natl Acad Sci USA. 108:9119–9124. 2011. View Article : Google Scholar : PubMed/NCBI

29 

Esposito M, Akman HB, Giron P, Ceregido MA, Schepers R, Ramos Paez LC, La Monaca E, De Greve J, Coux O, De Trez C, et al: USP13 controls the stability of Aurora B impacting progression through the cell cycle. Oncogene. 39:6009–6023. 2020. View Article : Google Scholar : PubMed/NCBI

30 

Bigot N, Day M, Baldock RA, Watts FZ, Oliver AW and Pearl LH: Phosphorylation-mediated interactions with TOPBP1 couple 53BP1 and 9-1-1 to control the G1 DNA damage checkpoint. Elife. 8:e443532019. View Article : Google Scholar : PubMed/NCBI

31 

Liu K, Graves JD, Lee YJ, Lin FT and Lin WC: Cell Cycle-Dependent Switch of TopBP1 Functions by Cdk2 and Akt. Mol Cell Biol. 40:e005992020. View Article : Google Scholar : PubMed/NCBI

32 

Kanginakudru S, DeSmet M, Thomas Y, Morgan IM and Androphy EJ: Levels of the E2 interacting protein TopBP1 modulate papillomavirus maintenance stage replication. Virology. 478:129–135. 2015. View Article : Google Scholar : PubMed/NCBI

33 

Kim W, Zhao F, Gao H, Qin S, Hou J, Deng M, Kloeber JA, Huang J, Zhou Q, Guo G, et al: USP13 regulates the replication stress response by deubiquitinating TopBP1. DNA Repair (Amst). 100:1030632021. View Article : Google Scholar : PubMed/NCBI

34 

He X, Kim JS, Diaz-Martinez LA, Han C, Lane WS, Budnik B and Waldman T: USP13 interacts with cohesin and regulates its ubiquitination in human cells. J Biol Chem. 296:1001942021. View Article : Google Scholar : PubMed/NCBI

35 

Liu Q, Yang X, Long G, Hu Y, Gu Z, Boisclair YR and Long Q: ERAD deficiency promotes mitochondrial dysfunction and transcriptional rewiring in human hepatic cells. J Biol Chem. 295:16743–16753. 2020. View Article : Google Scholar : PubMed/NCBI

36 

Byun H, Gou Y, Zook A, Lozano MM and Dudley JP: ERAD and how viruses exploit it. Front Microbiol. 5:3302014. View Article : Google Scholar : PubMed/NCBI

37 

Liu Y, Soetandyo N, Lee JG, Liu L, Xu Y, Clemons WM Jr and Ye Y: USP13 antagonizes gp78 to maintain functionality of a chaperone in ER-associated degradation. Elife. 3:e013692014. View Article : Google Scholar : PubMed/NCBI

38 

Devis-Jauregui L, Eritja N, Davis ML, Matias-Guiu X and Llobet-Navas D: Autophagy in the physiological endometrium and cancer. Autophagy. 17:1077–1095. 2021. View Article : Google Scholar : PubMed/NCBI

39 

Yang G, Song W, Postoak JL, Chen J, Martinez J, Zhang J, Wu L and Van Kaer L: Autophagy-related protein PIK3C3/VPS34 controls T cell metabolism and function. Autophagy. 17:1193–1204. 2021. View Article : Google Scholar : PubMed/NCBI

40 

Liu H, Zhao Z, Wu T, Zhang Q, Lu F, Gu J, Jiang T and Xue J: Inhibition of autophagy-dependent pyroptosis attenuates cerebral ischaemia/reperfusion injury. J Cell Mol Med. 25:5060–5069. 2021. View Article : Google Scholar : PubMed/NCBI

41 

Xie W, Jin S and Cui J: The NEDD4-USP13 axis facilitates autophagy via deubiquitinating PIK3C3. Autophagy. 16:1150–1151. 2020. View Article : Google Scholar : PubMed/NCBI

42 

Snyder NA and Silva GM: Deubiquitinating enzymes (DUBs): Regulation, homeostasis, and oxidative stress response. J Biol Chem. 297:1010772021. View Article : Google Scholar : PubMed/NCBI

43 

Wang Y and Wang F: Post-Translational modifications of deubiquitinating enzymes: Expanding the ubiquitin code. Front Pharmacol. 12:6850112021. View Article : Google Scholar : PubMed/NCBI

44 

Elsocht M, Giron P, Maes L, Versees W, Gutierrez GJ, De Greve J and Ballet S: Structure-Activity Relationship (SAR) Study of Spautin-1 to Entail the Discovery of Novel NEK4 Inhibitors. Int J Mol Sci. 22:6352021. View Article : Google Scholar : PubMed/NCBI

45 

Cheung HH, Yang Y, Lee TL, Rennert O and Chan WY: Hypermethylation of genes in testicular embryonal carcinomas. Br J Cancer. 114:230–236. 2016. View Article : Google Scholar : PubMed/NCBI

46 

Liu Z, Xu Y, Zhang W, Gao X, Luo G, Song H, Liu J and Wang H: Identification of targets of JS-K against HBV-positive human hepatocellular carcinoma HepG2.2.15 cells with iTRAQ proteomics. Sci Rep. 11:103812021. View Article : Google Scholar : PubMed/NCBI

47 

Wang J, Lin W, Li R, Cheng H, Sun S, Shao F, Yang Y, Zhang L, Feng X, Gao S, et al: The Deubiquitinase USP13 maintains cancer cell stemness by promoting FASN stability in small cell lung cancer. Front Oncol. 12:8999872022. View Article : Google Scholar : PubMed/NCBI

48 

Forghanifard MM, Azaraz S, Ardalan Khales S, Morshedi Rad D and Abbaszadegan MR: MAML1 promotes ESCC aggressiveness through upregulation of EMT marker TWIST1. Mol Biol Rep. 47:2659–2668. 2020. View Article : Google Scholar : PubMed/NCBI

49 

Han C, Yang L, Choi HH, Baddour J, Achreja A, Liu Y, Li Y, Li J, Wan G, Huang C, et al: Amplification of USP13 drives ovarian cancer metabolism. Nat Commun. 7:135252016. View Article : Google Scholar : PubMed/NCBI

50 

Qu Z, Zhang R, Su M and Liu W: UsP13 serves as a tumor suppressor via the PTEN/AKT pathway in oral squamous cell carcinoma. Cancer Manag Res. 11:9175–9183. 2019. View Article : Google Scholar : PubMed/NCBI

51 

Zhang J, Zhang P, Wei Y, Piao HL, Wang W, Maddika S, Wang M, Chen D, Sun Y, Hung MC, et al: Deubiquitylation and stabilization of PTEN by USP13. Nat Cell Biol. 15:1486–1494. 2013. View Article : Google Scholar : PubMed/NCBI

52 

Liu J, Xia H, Kim M, Xu L, Li Y, Zhang L, Cai Y, Norberg HV, Zhang T, Furuya T, et al: Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell. 147:223–234. 2011. View Article : Google Scholar : PubMed/NCBI

53 

Wu Y, Zhang Y, Liu C, Zhang Y, Wang D, Wang S, Wu Y, Liu F, Li Q, Liu X, et al: Amplification of USP13 drives non-small cell lung cancer progression mediated by AKT/MAPK signaling. Biomed Pharmacother. 114:1088312019. View Article : Google Scholar : PubMed/NCBI

54 

Meng LB, Hu GF, Shan MJ, Zhang YM, Yu ZM, Liu YQ, Xu HX, Wang L, Gong T and Liu DP: Citrate Synthase and OGDH as potential biomarkers of atherosclerosis under chronic stress. Oxid Med Cell Longev. 2021:99579082021. View Article : Google Scholar : PubMed/NCBI

55 

Wang J, Ye W, Yan X, Guo Q, Ma Q, Lin F, Huang J and Jin J: Low expression of ACLY associates with favorable prognosis in acute myeloid leukemia. J Transl Med. 17:1492019. View Article : Google Scholar : PubMed/NCBI

56 

Wei X, Shi J, Lin Q, Ma X, Pang Y, Mao H, Li R, Lu W, Wang Y and Liu P: Targeting ACLY Attenuates Tumor Growth and Acquired Cisplatin Resistance in Ovarian Cancer by Inhibiting the PI3K-AKT Pathway and Activating the AMPK-ROS Pathway. Front Oncol. 11:6422292021. View Article : Google Scholar : PubMed/NCBI

57 

Zhou Q, Zhan H, Lin F, Liu Y, Yang K, Gao Q, Ding M, Liu Y, Huang W and Cai Z: LincRNA-p21 suppresses glutamine catabolism and bladder cancer cell growth through inhibiting glutaminase expression. Biosci Rep. 39:BSR201823722019. View Article : Google Scholar : PubMed/NCBI

58 

Zhou X, Liu K, Cui J, Xiong J, Wu H, Peng T and Guo Y: Circ-MBOAT2 knockdown represses tumor progression and glutamine catabolism by miR-433-3p/GOT1 axis in pancreatic cancer. J Exp Clin Cancer Res. 40:1242021. View Article : Google Scholar : PubMed/NCBI

59 

Han C, Lu X and Nagrath D: Regulation of protein metabolism in cancer. Mol Cell Oncol. 5:e12853842018. View Article : Google Scholar : PubMed/NCBI

60 

De Blasio A, Vento R and Di Fiore R: Mcl-1 targeting could be an intriguing perspective to cure cancer. J Cell Physiol. 233:8482–8498. 2018. View Article : Google Scholar : PubMed/NCBI

61 

Zhang S, Zhang M, Jing Y, Yin X, Ma P, Zhang Z, Wang X, Di W and Zhuang G: Deubiquitinase USP13 dictates MCL1 stability and sensitivity to BH3 mimetic inhibitors. Nat Commun. 9:2152018. View Article : Google Scholar : PubMed/NCBI

62 

Abdul Rahman SF, Muniandy K, Soo YK, Tiew EYH, Tan KX, Bates TE and Mohana-Kumaran N: Co-inhibition of BCL-XL and MCL-1 with selective BCL-2 family inhibitors enhances cytotoxicity of cervical cancer cell lines. Biochem Biophys Rep. 22:1007562022.PubMed/NCBI

63 

Chen Y, Sun XX, Sears RC and Dai MS: Writing and erasing MYC ubiquitination and SUMOylation. Genes Dis. 6:359–371. 2019. View Article : Google Scholar : PubMed/NCBI

64 

Fang X, Zhou W, Wu Q, Huang Z, Shi Y, Yang K, Chen C, Xie Q, Mack SC, Wang X, et al: Deubiquitinase USP13 maintains glioblastoma stem cells by antagonizing FBXL14-mediated Myc ubiquitination. J Exp Med. 214:245–267. 2017. View Article : Google Scholar : PubMed/NCBI

65 

Zhao X, Fiske B, Kawakami A, Li J and Fisher DE: Regulation of MITF stability by the USP13 deubiquitinase. Nat Commun. 2:4142011. View Article : Google Scholar : PubMed/NCBI

66 

Hu S, Bai S, Dai Y, Yang N, Li J, Zhang X, Wang F, Zhao B, Bao G, Chen Y and Wu X: Deubiquitination of MITF-M regulates melanocytes proliferation and apoptosis. Front Mol Biosci. 8:6927242021. View Article : Google Scholar : PubMed/NCBI

67 

Zhou Q, Lin M, Feng X, Ma F, Zhu Y, Liu X, Qu C, Sui H, Sun B, Zhu A, et al: Targeting CLK3 inhibits the progression of cholangiocarcinoma by reprogramming nucleotide metabolism. J Exp Med. 217:e201917792020. View Article : Google Scholar : PubMed/NCBI

68 

Xie H, Zhou J, Liu X, Xu Y, Hepperla AJ, Simon JM, Wang T, Yao H, Liao C, Baldwin AS, et al: USP13 promotes deubiquitination of ZHX2 and tumorigenesis in kidney cancer. Proc Natl Acad Sci USA. 119:e21198541192022. View Article : Google Scholar : PubMed/NCBI

69 

Xie W, Jin S, Wu Y, Xian H, Tian S, Liu DA, Guo Z and Cui J: Auto-ubiquitination of NEDD4-1 Recruits USP13 to facilitate autophagy through deubiquitinating VPS34. Cell Rep. 30:2807–2819. e42020. View Article : Google Scholar : PubMed/NCBI

70 

Wijshake T, Zou Z, Chen B, Zhong L, Xiao G, Xie Y, Doench JG, Bennett L and Levine B: Tumor-suppressor function of Beclin 1 in breast cancer cells requires E-cadherin. Proc Natl Acad Sci USA. 118:e20204781182021. View Article : Google Scholar : PubMed/NCBI

71 

Matthew-Onabanjo AN, Janusis J, Mercado-Matos J, Carlisle AE, Kim D, Levine F, Cruz-Gordillo P, Richards R, Lee MJ and Shaw LM: Beclin 1 promotes endosome recruitment of hepatocyte growth factor tyrosine kinase substrate to suppress tumor proliferation. Cancer Res. 80:249–262. 2020. View Article : Google Scholar : PubMed/NCBI

72 

Huang J, Ye Z, Wang J, Chen Q, Huang D and Liu H: USP13 mediates PTEN to ameliorate osteoarthritis by restraining oxidative stress, apoptosis and inflammation via AKT-dependent manner. Biomed Pharmacother. 133:1110892021. View Article : Google Scholar : PubMed/NCBI

73 

He Y, Jiang S, Mao C, Zheng H, Cao B, Zhang Z, Zhao J, Zeng Y and Mao X: The deubiquitinase USP10 restores PTEN activity and inhibits non-small cell lung cancer cell proliferation. J Biol Chem. 297:1010882021. View Article : Google Scholar : PubMed/NCBI

74 

Wang Y, Wang Z, Lu J and Zhang H: Circular RNA circ-PTEN elevates PTEN inhibiting the proliferation of non-small cell lung cancer cells. Hum Cell. 34:1174–1184. 2021. View Article : Google Scholar : PubMed/NCBI

75 

Geng J, Huang X, Li Y, Xu X, Li S, Jiang D, Liang J, Jiang D, Wang C and Dai H: Down-regulation of USP13 mediates phenotype transformation of fibroblasts in idiopathic pulmonary fibrosis. Respir Res. 16:1242015. View Article : Google Scholar : PubMed/NCBI

76 

Che K, Han W, Li D, Cui S, Zhang M, Yang X and Niu H: Correlations between glycolysis with clinical traits and immune function in bladder urothelial carcinoma. Biosci Rep. 41:BSR202039822021. View Article : Google Scholar : PubMed/NCBI

77 

Li W, Xu M, Li Y, Huang Z, Zhou J, Zhao Q, Le K, Dong F, Wan C and Yi P: Comprehensive analysis of the association between tumor glycolysis and immune/inflammation function in breast cancer. J Transl Med. 18:922020. View Article : Google Scholar : PubMed/NCBI

78 

Xiang S, Fang J, Wang S, Deng B and Zhu L: MicroRNA135b regulates the stability of PTEN and promotes glycolysis by targeting USP13 in human colorectal cancers. Oncol Rep. 33:1342–1348. 2015. View Article : Google Scholar : PubMed/NCBI

79 

Zhao B, Huo W, Yu X, Shi X, Lv L, Yang Y, Kang J, Li S and Wu H: USP13 promotes breast cancer metastasis through FBXL14-induced Twist1 ubiquitination. Cell Oncol (Dordr). 46:717–733. 2023. View Article : Google Scholar : PubMed/NCBI

80 

Zhang T, Zheng J, Qiao L and Zhao W: Deubiquitinase USP13 promotes the epithelial-mesenchymal transition and metastasis in gastric cancer by maintaining Snail protein. Pathol Res Pract. 229:1537052022. View Article : Google Scholar : PubMed/NCBI

81 

Gao S, Chen T, Li L, Liu X, Liu Y, Zhao J, Lu Q, Zeng Z, Xu Q, Huang D and Tu K: Hypoxia-Inducible ubiquitin specific peptidase 13 contributes to tumor growth and metastasis via enhancing the toll-like receptor 4/Myeloid differentiation primary response gene 88/Nuclear Factor-κB pathway in hepatocellular carcinoma. Front Cell Dev Biol. 8:5873892020. View Article : Google Scholar : PubMed/NCBI

82 

Eluard B, Thieblemont C and Baud V: NF-κB in the New Era of cancer therapy. Trends Cancer. 6:677–687. 2020. View Article : Google Scholar : PubMed/NCBI

83 

Hiramatsu T, Yoshizawa J, Miyaguni K, Sugihara T, Harada A, Kaji S, Uchida G, Kanamori D, Baba Y, Ashizuka S and Ohki T: Thalidomide potentiates etoposide-induced apoptosis in murine neuroblastoma through suppression of NF-κB activation. Pediatr Surg Int. 34:443–450. 2018. View Article : Google Scholar : PubMed/NCBI

84 

Man X, Piao C, Lin X, Kong C, Cui X and Jiang Y: USP13 functions as a tumor suppressor by blocking the NF-kB-mediated PTEN downregulation in human bladder cancer. J Exp Clin Cancer Res. 38:2592019. View Article : Google Scholar : PubMed/NCBI

85 

Wang Y, Ou Z, Sun Y, Yeh S, Wang X, Long J and Chang C: Androgen receptor promotes melanoma metastasis via altering the miRNA-539-3p/USP13/MITF/AXL signals. Oncogene. 36:1644–1654. 2017. View Article : Google Scholar : PubMed/NCBI

86 

Lim Y and Lee DY: Identification of genetic mutations related to invasion and metastasis of acral melanoma via whole-exome sequencing. J Dermatol. 48:999–1006. 2021. View Article : Google Scholar : PubMed/NCBI

87 

Parag-Sharma K, Tasoulas J, Musicant AM, do Nascimento-Filho CHV, Zhu Z, Twomey C, Liu P, Castilho RM and Amelio AL: Synergistic efficacy of combined EGFR and HDAC inhibitors overcomes tolerance to EGFR monotherapy in salivary mucoepidermoid carcinoma. Oral Oncol. 115:1051662021. View Article : Google Scholar : PubMed/NCBI

88 

Tang W, Li X, Xie X, Sun X, Liu J, Zhang J, Wang C, Yu J and Xie P: EGFR inhibitors as adjuvant therapy for resected non-small cell lung cancer harboring EGFR mutations. Lung Cancer. 136:6–14. 2019. View Article : Google Scholar : PubMed/NCBI

89 

Giron P, Eggermont C, Noeparast A, Vandenplas H, Teugels E, Forsyth R, De Wever O, Aza-Blanc P, Gutierrez GJ and De Grève J: Targeting USP13-mediated drug tolerance increases the efficacy of EGFR inhibition of mutant EGFR in non-small cell lung cancer. Int J Cancer. 148:2579–2593. 2021. View Article : Google Scholar : PubMed/NCBI

90 

Zheng S, Shu Y, Lu Y and Sun Y: Chloroquine combined with imatinib overcomes imatinib resistance in gastrointestinal stromal tumors by inhibiting autophagy via the MAPK/ERK Pathway. Onco Targets Ther. 13:6433–6441. 2020. View Article : Google Scholar : PubMed/NCBI

91 

Gao Z, Li C, Sun H, Bian Y, Cui Z, Wang N, Wang Z, Yang Y, Liu Z, He Z, et al: N6-methyladenosine-modified USP13 induces pro-survival autophagy and imatinib resistance via regulating the stabilization of autophagy-related protein 5 in gastrointestinal stromal tumors. Cell Death Differ. 30:544–559. 2023. View Article : Google Scholar : PubMed/NCBI

92 

Li Y, Luo K, Yin Y, Wu C, Deng M, Li L, Li L, Chen Y, Nowsheen S, Lou Z and Yuan J: USP13 regulates the RAP80-BRCA1 complex dependent DNA damage response. Nat Commun. 8:157522017. View Article : Google Scholar : PubMed/NCBI

93 

Guo J, Zhang J, Liang L, Liu N, Qi M, Zhao S, Su J, Liu J, Peng C, Chen X and Liu H: Potent USP10/13 antagonist spautin-1 suppresses melanoma growth via ROS-mediated DNA damage and exhibits synergy with cisplatin. J Cell Mol Med. 24:4324–4340. 2020. View Article : Google Scholar : PubMed/NCBI

94 

Liu X, Balaraman K, Lynch CC, Hebron M, Wolf C and Moussa C: Novel ubiquitin specific protease-13 inhibitors alleviate neurodegenerative pathology. Metabolites. 11:6222021. View Article : Google Scholar : PubMed/NCBI

95 

Jacomin AC, Taillebourg E and Fauvarque MO: Deubiquitinating enzymes related to autophagy: New therapeutic opportunities? Cells. 7:1122018. View Article : Google Scholar : PubMed/NCBI

96 

Liu J, Shaik S, Dai X, Wu Q, Zhou X, Wang Z and Wei W: Targeting the ubiquitin pathway for cancer treatment. Biochim Biophys Acta. 1855:50–60. 2015.PubMed/NCBI

97 

Kaushal K, Antao AM, Kim KS and Ramakrishna S: Deubiquitinating enzymes in cancer stem cells: Functions and targeted inhibition for cancer therapy. Drug Discov Today. 23:1974–1982. 2018. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Tao Y, Xu X, Shen R, Miao X and He S: Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review). Oncol Lett 27: 58, 2024.
APA
Tao, Y., Xu, X., Shen, R., Miao, X., & He, S. (2024). Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review). Oncology Letters, 27, 58. https://doi.org/10.3892/ol.2023.14191
MLA
Tao, Y., Xu, X., Shen, R., Miao, X., He, S."Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review)". Oncology Letters 27.2 (2024): 58.
Chicago
Tao, Y., Xu, X., Shen, R., Miao, X., He, S."Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review)". Oncology Letters 27, no. 2 (2024): 58. https://doi.org/10.3892/ol.2023.14191
Copy and paste a formatted citation
x
Spandidos Publications style
Tao Y, Xu X, Shen R, Miao X and He S: Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review). Oncol Lett 27: 58, 2024.
APA
Tao, Y., Xu, X., Shen, R., Miao, X., & He, S. (2024). Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review). Oncology Letters, 27, 58. https://doi.org/10.3892/ol.2023.14191
MLA
Tao, Y., Xu, X., Shen, R., Miao, X., He, S."Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review)". Oncology Letters 27.2 (2024): 58.
Chicago
Tao, Y., Xu, X., Shen, R., Miao, X., He, S."Roles of ubiquitin‑specific protease 13 in normal physiology and tumors (Review)". Oncology Letters 27, no. 2 (2024): 58. https://doi.org/10.3892/ol.2023.14191
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team