2024, Number 3
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Rev Educ Bioquimica 2024; 43 (3)
TRIM25: un regulador transcripcional, postranscripcional y postraduccional desregulado en cáncer
Palacios-Serrato EG, Medina-Abreu KH, Oropeza-Martínez E, Macías-Silva M, Tecalco-Cruz ÁC
Language: Spanish
References: 87
Page: 151-165
PDF size: 725.14 Kb.
ABSTRACT
The protein family containing tripartite motif (TRIM) is involved in several
cellular processes because of its functional versatility due to its different
domains. TRIM proteins are mainly characterized by their enzymatic function
as E3-ubiquitin ligases. TRIM25 is a member of the TRIM protein family that
acts as E3-ubiquitin ligase and E3 ligase for ISG15 in a post-translational
process known as ISGylation. Moreover, TRIM25 can associate with DNA
and RNA and modulate gene expression at transcriptional and posttranscriptional
levels. In this paper, we review the characteristics of TRIM25 and the relevance of its multifunctionality in cancer development and progression.
REFERENCES
Vunjak M, Versteeg GA. TRIM proteins. CurrBiol. 2019; 29(2):42–44.
Hatakeyama S. TRIM Family Proteins: Roles inAutophagy, Immunity, and Carcinogenesis. TrendsBiochem Sci. 2017;42(4):297–311.
Li Y, Wu H, Wu W, Zhuo W, Liu W, Zhang Y, etal. Structural insights into the TRIM family ofubiquitin E3 ligases. Cell Res. 2014;24(6):762–765.
Van Gent M, Sparrer KMJ, Gack MU. TRIMProteins and Their Roles in Antiviral Host Defenses.Annu Rev Virol. 2018;5(1):385–405.
Wang L, Ning S. TRIMming Type I Interferon-Mediated Innate Immune Response in Antiviral andAntitumor Defense. Viruses. 2021;13(2):279.
Takayama K ichi, Suzuki T, Tanaka T, FujimuraT, Takahashi S, Urano T, et al. TRIM25 enhancescell growth and cell survival by modulating p53signals via interaction with G3BP2 in prostatecancer. Oncogene. 2018; 37(16):2165–80.
Zhang P, Elabd S, Hammer S, Solozobova V,Yan H, Bartel F, et al. TRIM25 has a dual functionin the p53/Mdm2 circuit. Oncogene. 2015;34(46):5729–38.
García-Sastre A, Miorin L. Intrinsic CellularDefenses (TRIMS) in Modulating Viral Infectionand Immunity. En: Encyclopedia of Immunobiology[Internet]. Elsevier; 2016 [citado el 28 de enero de2023]. p. 235–242. Disponible en:https://linkinghub.elsevier.com/retrieve/pii/B9780123742797140044
Rahimi-Tesiye M, Zaersabet M, Salehiyeh S,Jafari SZ. The role of TRIM25 in the occurrence anddevelopment of cancers and inflammatory diseases.Biochim Biophys Acta BBA - Rev Cancer.2023;1878(5):188954.
Inoue S, Orimo A, Hosoi T, Kondo S,Toyoshima H, Kondo T, et al. Genomic binding-sitecloning reveals an estrogen-responsive gene thatencodes a RING finger protein. Proc Natl Acad Sci.1993;90(23):11117–21.
The UniProt Consortium, Bateman A, MartinMJ, Orchard S, Magrane M, Ahmad S, et al.UniProt: the Universal Protein Knowledgebase in2023. Nucleic Acids Res. 2023;51(D1):D523–31.
Zody MC, Garber M, Adams DJ, Sharpe T,Harrow J, Lupski JR, et al. DNA sequence of humanchromosome 17 and analysis of rearrangement in thehuman lineage. Nature. 2006;440(7087):1045–9.
Meroni G, Desagher S. Cellular Function ofTRIM E3 Ubiquitin Ligases in Health and Disease.Cells. 2022;11(2):250.
Gómez‐Tortosa E, Baradaran‐Heravi Y, DillenL, Choudhury NR, Agüero Rabes P, Pérez‐Pérez J,et al. TRIM25 mutation (p.C168*), coding for an E3ubiquitin ligase, is a cause of early‐onset autosomaldominant dementia with amyloid load andparkinsonism. Alzheimers Dement.2023;19(7):2805–15.
Shimada N, Suzuki T, Inoue S, Kato K, ImataniA, Sekine H, et al. Systemic distribution of estrogenresponsivefinger protein (Efp) in human tissues. MolCell Endocrinol. 2004;218(1–2):147–53.
Oshiumi H, Miyashita M, Matsumoto M, SeyaT. A Distinct Role of Riplet-Mediated K63-LinkedPolyubicuitination of the RIG-I Repressor Domainin Human Antiviral Innate Immune Responses. GaleM, editor. PLoS Pathog. 2013;9(8):e1003533.
Stevens RV, Esposito D, Rittinger K.Characterisation of class VI TRIM RING domains:linking RING activity to C-terminal domainidentity. Life Sci Alliance. 2019;2(3):e201900295.
Borden KL, Freemont PS. The RING fingerdomain: a recent example of a sequence—structurefamily. Curr Opin Struct Biol. 1996;6(3):395–401.
Anthony Massiah M. Zinc-Binding B-BoxDomains with RING Folds Serve Critical Roles inthe Protein Ubicuitination Pathways in Plants andAnimals. En: Summers M, editor. UbiquitinProteasome System - Current Insights intoMechanism Cellular Regulation and Disease[Internet]. IntechOpen; 2019 [citado el 30 de enerode 2023]. Disponible en:https://www.intechopen.com/books/ubiquitinproteasome-system-current-insights-intomechanism-cellular-regulation-and-disease/zincbinding-b-box-domains-with-ring-folds-servecritical-roles-in-the-protein-ubicuitination-pathway
Choudhury NR, Heikel G, Trubitsyna M, KubikP, Nowak JS, Webb S, et al. RNA-binding activityof TRIM25 is mediated by its PRY/SPRY domainand is required for ubicuitination. BMC Biol.2017;15(1):105.
Koliopoulos MG, Lethier M, Van Der Veen AG,Haubrich K, Hennig J, Kowalinski E, et al.Molecular mechanism of influenza A NS1-mediatedTRIM25 recognition and inhibition. Nat Commun.2018;9(1):1820.
Williams FP, Haubrich K, Perez-Borrajero C,Hennig J. Emerging RNA-binding roles in theTRIM family of ubiquitin ligases. Biol Chem. el 26de noviembre de 2019;400(11):1443–64.
Haubrich K, Augsten S, Álvarez L, Huppertz I,Simon B, Perez K, et al. Mechanistic insights intoRNA binding and RNA-regulated RIG-Iubicuitination by TRIM25 [Internet]. MolecularBiology; 2020 may [citado el 29 de noviembre de2023]. Disponible en:http://biorxiv.org/lookup/doi/10.1101/2020.05.04.070177
Yang E, Huang S, Jami-Alahmadi Y, McInerneyGM, Wohlschlegel JA, Li MMH. Elucidation ofTRIM25 ubicuitination targets involved in diversecellular and antiviral processes. Heise MT, editor.PLOS Pathog. 2022;18(9):e1010743.
Zheng X, Wang X, Tu F, Wang Q, Fan Z, GaoG. TRIM25 Is Required for the Antiviral Activity ofZinc Finger Antiviral Protein. Diamond MS, editor.J Virol. 2017;91(9):e00088-17.
Choudhury NR, Nowak JS, Zuo J, Rappsilber J,Spoel SH, Michlewski G. Trim25 Is an RNASpecificActivator of Lin28a/TuT4-MediatedUridylation. Cell Rep. 2014;9(4):1265–72.
Liu Y, Tao S, Liao L, Li Y, Li H, Li Z, et al.TRIM25 promotes the cell survival and growth ofhepatocellular carcinoma through targeting Keap1-Nrf2 pathway. Nat Commun. 2020;11(1):348.
Chiang C, Dvorkin S, Chiang JJ, Potter RB,Gack MU. The Small t Antigen of JC VirusAntagonizes RIG-I-Mediated Innate Immunity byInhibiting TRIM25’s RNA Binding Ability. HornerSM, editor. mBio. 2021;12(2):e00620-21.
Sanchez JG, Chiang JJ, Sparrer KMJ, Alam SL,Chi M, Roganowicz MD, et al. Mechanism ofTRIM25 Catalytic Activation in the Antiviral RIG-IPathway. Cell Rep. 2016;16(5):1315–25.
Wu SF, Xia L, Shi XD, Dai YJ, Zhang WN,Zhao JM, et al. RIG-I regulates myeloiddifferentiation by promoting TRIM25-mediatedISGylation. Proc Natl Acad Sci.2020;117(25):14395–404.
Gack MU, Shin YC, Joo CH, Urano T, Liang C,Sun L, et al. TRIM25 RING-finger E3 ubiquitinligase is essential for RIG-I-mediated antiviralactivity. Nature. 2007;446(7138):916–20.
Gupta S, Ylä-Anttila P, Callegari S, Tsai MH,Delecluse HJ, Masucci MG. Herpesvirusdeconjugases inhibit the IFN response by promotingTRIM25 autoubicuitination and functionalinactivation of the RIG-I signalosome. Feng P,editor. PLOS Pathog. 2018;14(1):e1006852.
Zou W, Wang J, Zhang DE. Negative regulationof ISG15 E3 ligase EFP through its autoISGylation.Biochem Biophys Res Commun. 2007;354(1):321–7.
Zou W, Zhang DE. The Interferon-inducibleUbiquitin-protein Isopeptide Ligase (E3) EFP AlsoFunctions as an ISG15 E3 Ligase. J Biol Chem.2006;281(7):3989–94.
Urano T, Saito T, Tsukui T, Fujita M, Hosoi T,Muramatsu M, et al. Efp targets 14-3-3j forproteolysis and promotes breast tumour growth.2002;417.
Klug A. The discovery of zinc fingers and theirdevelopment for practical applications in generegulation and genome manipulation. Q RevBiophys. 2010;43(1):1–21.
Koliopoulos MG, Esposito D, Christodoulou E,Taylor IA, Rittinger K. Functional role of TRIM E3ligase oligomerization and regulation of catalyticactivity. EMBO J. 2016;35(11):1204–18.
Li F, Sun Q, Liu K, Zhang L, Lin N, You K, etal. OTUD5 cooperates with TRIM25 intranscriptional regulation and tumor progression viadeubicuitination activity. Nat Commun.2020;11(1):4184.
Walsh LA, Alvarez MJ, Sabio EY, Reyngold M,Makarov V, Mukherjee S, et al. An IntegratedSystems Biology Approach Identifies TRIM25 as aKey Determinant of Breast Cancer Metastasis. CellRep. 2017;20(7):1623–40.
Woolfson DN. Coiled-Coil Design: Updated andUpgraded. En: Parry DAD, Squire JM, editores.Fibrous Proteins: Structures and Mechanisms[Internet]. Cham: Springer International Publishing;2017 [citado el 25 de noviembre de 2023]. p. 35–61.(Subcellular Biochemistry; vol. 82). Disponible en:http://link.springer.com/10.1007/978-3-319-496740_2
Choudhury NR, Heikel G, Michlewski G. TRIM25and its emerging RNA‐binding roles in antiviraldefense. WIREs RNA [Internet]. julio de 2020 [citadoel 28 de enero de 2023];11(4). Disponible en:https://onlinelibrary.wiley.com/doi/10.1002/wrna.1588
Sanchez JG, Okreglicka K, Chandrasekaran V,Welker JM, Sundquist WI, Pornillos O. Thetripartite motif coiled-coil is an elongatedantiparallel hairpin dimer. Proc Natl Acad Sci.2014;111(7):2494–9.
D’Cruz AA, Kershaw NJ, Hayman TJ, LinossiEM, Chiang JJ, Wang MK, et al. Identification of asecond binding site on the TRIM25 B30.2 domain.Biochem J. 2018;475(2):429–40.
D’Cruz AA, Babon JJ, Norton RS, Nicola NA,Nicholson SE. Structure and function of theSPRY/B30.2 domain proteins involved in innateimmunity. Protein Sci. 2013;22(1):1–10.
Baltz AG, Munschauer M, Schwanhäusser B,Vasile A, Murakawa Y, Schueler M, et al. ThemRNA-Bound Proteome and Its Global OccupancyProfile on Protein-Coding Transcripts. Mol Cell.2012;46(5):674–90.
Castello A, Fischer B, Eichelbaum K, Horos R,Beckmann BM, Strein C, et al. Insights into RNABiology from an Atlas of Mammalian mRNABindingProteins. Cell. 2012;149(6):1393–406.
Kwon SC, Yi H, Eichelbaum K, Föhr S, FischerB, You KT, et al. The RNA-binding proteinrepertoire of embryonic stem cells. Nat Struct MolBiol. 2013;20(9):1122–30.
D’Cruz AA, Kershaw NJ, Chiang JJ, Wang MK,Nicola NA, Babon JJ, et al. Crystal structure of theTRIM25 B30.2 (PRYSPRY) domain: a keycomponent of antiviral signalling. Biochem J.2013;456(2):231–40.
Lian H, Zang R, Wei J, Ye W, Hu MM, ChenYD, et al. The Zinc-Finger Protein ZCCHC3 BindsRNA and Facilitates Viral RNA Sensing andActivation of the RIG-I-like Receptors. Immunity.2018;49(3):438-448.e5.
Sanchez JG, Sparrer KMJ, Chiang C, Reis RA,Chiang JJ, Zurenski MA, et al. TRIM25 Binds RNAto Modulate Cellular Anti-viral Defense. J Mol Biol.2018;430(24):5280–93.
Nakasato N, Ikeda K, Urano T, Horie-Inoue K,Takeda S, Inoue S. A ubiquitin E3 ligase Efp is upregulatedby interferons and conjugated with ISG15.Biochem Biophys Res Commun. 2006;351(2):540–6.
Han Q, Cheng P, Yang H, Liang H, Lin F.Altered expression of microRNA‐365 is related tothe occurrence and development of non‐small‐celllung cancer by inhibiting TRIM25 expression. JCell Physiol. 2019;234(12):22321–30.
Wang Z, Tong D, Han C, Zhao Z, Wang X, JiangT, et al. Blockade of miR-3614 maturation byIGF2BP3 increases TRIM25 expression andpromotes breast cancer cell proliferation.EBioMedicine. 2019;41:357–69.
Wang J, Yin G, Bian H, Yang J, Zhou P, Yan K,et al. LncRNA XIST upregulates TRIM25 vianegatively regulating miR-192 in hepatitis B virusrelatedhepatocellular carcinoma. Mol Med.2021;27(1):41.
Zhang W, Zhu L, Yang G, Zhou B, Wang J, QuX, et al. Hsa_circ_0026134 expression promotedTRIM25- and IGF2BP3-mediated hepatocellularcarcinoma cell proliferation and invasion viasponging miR-127-5p. Biosci Rep.2020;40(7):BSR20191418.
Yu L, Ren Y. Long Noncoding RNA SmallNucleolar RNA Host Gene 3 Mediates ProstateCancer Migration, Invasion, and Epithelial-Mesenchymal Transition by Sponging miR-487a-3pto Regulate TRIM25. Cancer Biother Radiopharm.2022;37(6):451–65.
Lee NR, Choi JY, Yoon IH, Lee JK, Inn KS.Positive regulatory role of c-Src-mediated TRIM25tyrosine phosphorylation on RIG-I ubicuitinationand RIG-I-mediated antiviral signaling pathway.Cell Immunol. 2018;332:94–100.
Azuma K, Inoue S. Efp/TRIM25 and Its RelatedProtein, TRIM47, in Hormone-Dependent Cancers.Cells. 2022;11(15):2464.
GEPIA. Gene Expression Profiling InteractiveAnalysis [Internet]. 2023. Disponible en:http://gepia.cancer-pku.cn/
Katsura C, Ogunmwonyi I, Kankam HK, SahaS. Breast cancer: presentation, investigation andmanagement. Br J Hosp Med. 2022;83(2):1–7.
Tecalco-Cruz AC, Abraham-Juárez MJ,Solleiro-Villavicencio H, Ramírez-Jarquín JO.TRIM25: A central factor in breast cancer. World JClin Oncol. 2021;12(8):646–55.
Dong XY, Fu X, Fan S, Guo P, Su D, Dong JT.Oestrogen causes ATBF1 protein degradationthrough the oestrogen-responsive E3 ubiquitinligase EFP. Biochem J. 2012;444(3):581–90.
Cao F, Li DP, Wang L, Li M, Zhang H, Tao M.TRIM25 promotes oncogenic activities throughregulation of ZEB1 in breast cancer. Int J Clin ExpPathol. 2016;10(9):9751–60.
Qin H, Yuan Y, Yuan M, Wang H, Yang Y.Degradation of AZGP1 suppresses the progressionof breast cancer cells via TRIM25. Environ Toxicol.2023;tox.24016.
Wang Z, Jing X, Li F, Chen Y, Huang C. miR-3614-3p suppresses cell aggressiveness of humanbreast cancer by targeting AKT3 and HDAC1expression. Transl Cancer Res. 2022;11(6):1565–75.
Sakuma M, Akahira J ichi, Suzuki T, Inoue S,Ito K, Moriya T, et al. Expression of estrogenresponsivefinger protein (Efp) is associated withadvanced disease in human epithelial ovariancancer. Gynecol Oncol. 2005;99(3):664–70.
Sato W, Ikeda K, Urano T, Abe Y, Nakasato N,Horie-Inoue K, et al. Efp promotes in vitro and invivo growth of endometrial cancer cells along withthe activation of nuclear factor-κB signaling.Ahmad A, editor. PLOS ONE.2018;13(12):e0208351.
Wang S, Kollipara RK, Humphries CG, Ma SH,Hutchinson R, Li R, et al. The ubiquitin ligaseTRIM25 targets ERG for degradation in prostatecancer. Oncotarget. 2016;7(40):64921–31.
Llovet JM, Kelley RK, Villanueva A, SingalAG, Pikarsky E, Roayaie S, et al. Hepatocellularcarcinoma. Nat Rev Dis Primer. 2021;7(1):6.
Zang H liang, Ren S nan, Cao H, Tian X feng.The ubiquitin ligase TRIM25 inhibits hepatocellularcarcinoma progression by targeting metastasisassociated 1 protein: TRIM25 InhibitsHepatocellular Carcinoma. IUBMB Life. 2017;69(10):795–801.
Yun H, Jeong H, Kim DY, You J, Lee J, Kang D,et al. Degradation of AZGP1 suppresses apoptosisand facilitates cholangiocarcinoma tumorigenesisvia TRIM25. J Cell Mol Med. 2024;28(3):e18104.
Khwaja A, Bjorkholm M, Gale RE, Levine RL,Jordan CT, Ehninger G, et al. Acute myeloidleukaemia. Nat Rev Dis Primer. 2016;2(1):16010.
Wang S, Zhang BS, Yang Y, Li Y, Lv JL, ChengY. TRIM25 contributes to the malignancy of acutemyeloid leukemia and is negatively regulated bymicroRNA-137. Open Med. 2020;16(1):095–103.
Louis DN, Perry A, Reifenberger G, VonDeimling A, Figarella-Branger D, Cavenee WK, etal. The 2016 World Health OrganizationClassification of Tumors of the Central NervousSystem: a summary. Acta Neuropathol (Berl).2016;131(6):803–20.
Louis DN, Perry A, Wesseling P, Brat DJ, CreeIA, Figarella-Branger D, et al. The 2021 WHOClassification of Tumors of the Central NervousSystem: a summary. Neuro-Oncol.2021;23(8):1231–51.
Ge M xu, Shi Y kang, Liu D. Tripartite motifcontaining25 facilitates immunosuppression andinhibits apoptosis of glioma via activating NF-κB.Exp Biol Med. 2022;247(17):1529–41.
Chen Y, Xu X, Ding K, Tang T, Cai F, Zhang H,et al. TRIM25 promotes glioblastoma cell growthand invasion via regulation of the PRMT1/c-MYCpathway by targeting the splicing factor NONO. JExp Clin Cancer Res. 2024;43(1):39.
Ma Q, Jiang H, Ma L, Zhao G, Xu Q, Guo D, etal. The moonlighting function of glycolytic enzymeenolase-1 promotes choline phospholipidmetabolism and tumor cell proliferation. Proc NatlAcad Sci. 2023;120(15):e2209435120.
Wei J, Wang L, Zhang Y, Sun T, Zhang C, Hu Z,et al. TRIM25 promotes temozolomide resistance inglioma by regulating oxidative stress and ferroptoticcell death via the ubicuitination of keap1.Oncogene. 2023;42(26):2103–12.
Yan Y, Zhou S, Chen X, Yi Q, Feng S, Zhao Z,et al. Suppression of ITPKB degradation by Trim25confers TMZ resistance in glioblastoma throughROS homeostasis. Signal Transduct Target Ther.2024;9(1):58.
Pilleron S, Gower H, Janssen-Heijnen M, SignalVC, Gurney JK, Morris EJ, et al. Patterns of agedisparities in colon and lung cancer survival: asystematic narrative literature review. BMJ Open.2021;11(3):e044239.
Nasrullah U, Haeussler K, Biyanee A, Wittig I,Pfeilschifter J, Eberhardt W. Identification ofTRIM25 as a Negative Regulator of Caspase-2Expression Reveals a Novel Target for SensitizingColon Carcinoma Cells to Intrinsic Apoptosis.Cells. 2019;8(12):1622.
Nasrullah U, Stanke K, Recknagel V, Bozkurt S,Wurzel P, Gauer S, et al. The E3 Ligase TRIM25Impairs Apoptotic Cell Death in Colon CarcinomaCells via Destabilization of Caspase-7 mRNA: APossible Role of hnRNPH1. Cells. 2023;12(1):201.
Zhou S, Peng J, Xiao L, Zhou C, Fang Y, Ou Q,et al. TRIM25 regulates oxaliplatin resistance incolorectal cancer by promoting EZH2 stability. CellDeath Dis. 2021;12(5):463.
Qin Y, Cui H, Zhang H. Overexpression ofTRIM25 in Lung Cancer Regulates Tumor CellProgression. Technol Cancer Res Treat.2016;15(5):707–15.
He Y ming, Zhou X min, Jiang S yi, Zhang Zbin, Cao B yin, Liu J bao, et al. TRIM25 activatesAKT/mTOR by inhibiting PTEN via K63-linkedpolyubicuitination in non-small cell lung cancer.Acta Pharmacol Sin. 2022;43(3):681–91.
Li B, Zhu L, Lu C, Wang C, Wang H, Jin H, etal. circNDUFB2 inhibits non-small cell lung cancerprogression via destabilizing IGF2BPs andactivating anti-tumor immunity. Nat Commun.2021;12(1):295.