E3 ubiquitin ligase-dependent regulatory mechanism of TRIM family in carcinogenesis
DOI:
https://doi.org/10.58567/ci02010007Keywords:
TRIM proteins; Ubiquitination; Cancer; Protein degradation; Signaling pathwayAbstract
Tripartite motif-containing (TRIM) proteins consist of over 80 proteins, the majority of which exhibit E3 ubiquitin ligase activity. E3 ligases have a critical role in various cellular processes by specifically recognizing and ubiquitinating substrate proteins to promote their proteasomal degradation or alter their activities. Numerous studies have indicated that TRIMs are involved in carcinogenesis through various mechanisms. However, the regulatory mechanisms delimitating TRIMs’ function as E3 ligases has not yet been specifically addressed in a previous review article. In this review, we focus on recent advancements in understanding how certain TRIMs function solely as E3 ligases during cancer cell proliferation, apoptosis, and metastasis. We comprehensively summarize the target proteins of TRIMs involved in disordered signaling pathways such as Wnt/β-catenin, PI3K/AKT, NF-κB, p53, ERK, and STAT3, as well as those regulating the cell cycle and glycolysis. Following ubiquitination modification by TRIM E3 ligases, these target proteins either undergo proteasome-mediating degradation, maintain steady levels, or get activated/inactivated. This review provides a foundation for the development of E3 ligase-based cancer treatments.
References
Toma-Fukai S, Shimizu T: Structural Diversity of Ubiquitin E3 Ligase. Molecules, 2021, 26(21).
Ikeda F, Crosetto N, Dikic I: What determines the specificity and outcomes of ubiquitin signaling? Cell, 2010, 143(5): 677-681.
Grice GL, Nathan JA: The recognition of ubiquitinated proteins by the proteasome. Cell Mol Life Sci, 2016, 73(18): 3497-3506.
Muller L, Kutzner CE, Balaji V, Hoppe T: In Vitro Analysis of E3 Ubiquitin Ligase Function. J Vis Exp, 2021, (171).
Gong X, Du D, Deng Y, Zhou Y, Sun L, Yuan S: The structure and regulation of the E3 ubiquitin ligase HUWE1 and its biological functions in cancer. Invest New Drugs, 2020, 38(2): 515-524.
Ikeda F: Ubiquitin conjugating enzymes in the regulation of the autophagy-dependent degradation pathway. Matrix Biol, 2021, 100-10123-29.
Haas AL, Warms JV, Hershko A, Rose IA: Ubiquitin-activating enzyme. Mechanism and role in protein-ubiquitin conjugation. J Biol Chem, 1982, 257(5): 2543-2548.
Zheng N, Shabek N: Ubiquitin Ligases: Structure, Function, and Regulation. Annu Rev Biochem, 2017, 86129-157.
Jevtic P, Haakonsen DL, Rape M: An E3 ligase guide to the galaxy of small-molecule-induced protein degradation. Cell Chem Biol, 2021, 28(7): 1000-1013.
Liu J, Zhang C, Wang X, Hu W, Feng Z: Tumor suppressor p53 cross-talks with TRIM family proteins. Genes Dis, 2021, 8(4): 463-474.
Zhang Y, Zhang W, Zheng L, Guo Q: The roles and targeting options of TRIM family proteins in tumor. Front Pharmacol, 2022, 13999380.
Huang N, Sun X, Li P, Liu X, Zhang X, Chen Q, Xin H: TRIM family contribute to tumorigenesis, cancer development, and drug resistance. Exp Hematol Oncol, 2022, 11(1): 75.
Zhao G, Liu C, Wen X, Luan G, Xie L, Guo X: The translational values of TRIM family in pan-cancers: From functions and mechanisms to clinics. Pharmacol Ther, 2021, 227107881.
Li X, Pu W, Zheng Q, Ai M, Chen S, Peng Y: Proteolysis-targeting chimeras (PROTACs) in cancer therapy. Mol Cancer, 2022, 21(1): 99.
Hatakeyama S: TRIM Family Proteins: Roles in Autophagy, Immunity, and Carcinogenesis. Trends Biochem Sci, 2017, 42(4): 297-311.
Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, Riganelli D, Zanaria E, Messali S, Cainarca S et al: The tripartite motif family identifies cell compartments. EMBO J, 2001, 20(9): 2140-2151.
Wang HT, Hur S: Substrate recognition by TRIM and TRIM-like proteins in innate immunity. Semin Cell Dev Biol, 2021, 11176-85.
Meroni G, Diez-Roux G: TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. Bioessays, 2005, 27(11): 1147-1157.
Zhu Y, Afolabi LO, Wan X, Shim JS, Chen L: TRIM family proteins: roles in proteostasis and neurodegenerative diseases. Open Biol, 2022, 12(8): 220098.
Li Y, Wu H, Wu W, Zhuo W, Liu W, Zhang Y, Cheng M, Chen YG, Gao N, Yu H et al: Structural insights into the TRIM family of ubiquitin E3 ligases. Cell Res, 2014, 24(6): 762-765.
Koliopoulos MG, Esposito D, Christodoulou E, Taylor IA, Rittinger K: Functional role of TRIM E3 ligase oligomerization and regulation of catalytic activity. EMBO J, 2016, 35(11): 1204-1218.
Kawai T, Akira S: Regulation of innate immune signalling pathways by the tripartite motif (TRIM) family proteins. EMBO Mol Med, 2011, 3(9): 513-527.
Gu J, Chen J, Xiang S, Zhou X, Li J: Intricate confrontation: Research progress and application potential of TRIM family proteins in tumor immune escape. J Adv Res, 2023.
Nisole S, Stoye JP, Saib A: TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol, 2005, 3(10): 799-808.
D'Cruz AA, Babon JJ, Norton RS, Nicola NA, Nicholson SE: Structure and function of the SPRY/B30.2 domain proteins involved in innate immunity. Protein Sci, 2013, 22(1): 1-10.
Yap MW, Nisole S, Stoye JP: A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol, 2005, 15(1): 73-78.
Rhodes DA, de Bono B, Trowsdale J: Relationship between SPRY and B30.2 protein domains. Evolution of a component of immune defence? Immunology, 2005, 116(4): 411-417.
Yang J, Ye J, Ma T, Tang F, Huang L, Liu Z, Tian S, Cheng X, Zhang L, Guo Z et al: Tripartite motif-containing protein 11 promotes hepatocellular carcinogenesis through ubiquitin-proteasome-mediated degradation of pleckstrin homology domain leucine-rich repeats protein phosphatase 1. Hepatology, 2022, 76(3): 612-629.
Zhang LH, Yin AA, Cheng JX, Huang HY, Li XM, Zhang YQ, Han N, Zhang X: TRIM24 promotes glioma progression and enhances chemoresistance through activation of the PI3K/Akt signaling pathway. Oncogene, 2015, 34(5): 600-610.
Park HH, Kim HR, Park SY, Hwang SM, Hong SM, Park S, Kang HC, Morgan MJ, Cha JH, Lee D et al: RIPK3 activation induces TRIM28 derepression in cancer cells and enhances the anti-tumor microenvironment. Mol Cancer, 2021, 20(1): 107.
van Gent M, Sparrer KMJ, Gack MU: TRIM Proteins and Their Roles in Antiviral Host Defenses. Annu Rev Virol, 2018, 5(1): 385-405.
Pauletto E, Eickhoff N, Padrao NA, Blattner C, Zwart W: TRIMming Down Hormone-Driven Cancers: The Biological Impact of TRIM Proteins on Tumor Development, Progression and Prognostication. Cells, 2021, 10(6).
Zhan W, Zhang S: TRIM proteins in lung cancer: Mechanisms, biomarkers and therapeutic targets. Life Sci, 2021, 268118985.
Esposito D, Koliopoulos MG, Rittinger K: Structural determinants of TRIM protein function. Biochem Soc Trans, 2017, 45(1): 183-191.
Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. Cell, 2011, 144(5): 646-674.
Zheng S, Zhou C, Wang Y, Li H, Sun Y, Shen Z: TRIM6 promotes colorectal cancer cells proliferation and response to thiostrepton by TIS21/FoxM1. J Exp Clin Cancer Res, 2020, 39(1): 23.
Urano T, Saito T, Tsukui T, Fujita M, Hosoi T, Muramatsu M, Ouchi Y, Inoue S: Efp targets 14-3-3 sigma for proteolysis and promotes breast tumour growth. Nature, 2002, 417(6891): 871-875.
Qin X, Qiu F, Zou Z: TRIM25 is associated with cisplatin resistance in non-small-cell lung carcinoma A549 cell line via downregulation of 14-3-3sigma. Biochem Biophys Res Commun, 2017, 493(1): 568-572.
Zhang RY, Liu ZK, Wei D, Yong YL, Lin P, Li H, Liu M, Zheng NS, Liu K, Hu CX et al: UBE2S interacting with TRIM28 in the nucleus accelerates cell cycle by ubiquitination of p27 to promote hepatocellular carcinoma development. Signal Transduct Target Ther, 2021, 6(1): 64.
Izumi H, Kaneko Y: Trim32 facilitates degradation of MYCN on spindle poles and induces asymmetric cell division in human neuroblastoma cells. Cancer Res, 2014, 74(19): 5620-5630.
Liu TY, Chen J, Shang CL, Shen HW, Huang JM, Liang YC, Wang W, Zhao YH, Liu D, Shu M et al: Tripartite motif containing 62 is a novel prognostic marker and suppresses tumor metastasis via c-Jun/Slug signaling-mediated epithelial-mesenchymal transition in cervical cancer. J Exp Clin Cancer Res, 2016, 35(1): 170.
Hu X, Tang Z, Ma S, Yu Y, Chen X, Zang G: Tripartite motif-containing protein 7 regulates hepatocellular carcinoma cell proliferation via the DUSP6/p38 pathway. Biochem Biophys Res Commun, 2019, 511(4): 889-895.
Liu Y, Dong Y, Zhao L, Su L, Diao K, Mi X: TRIM59 overexpression correlates with poor prognosis and contributes to breast cancer progression through AKT signaling pathway. Mol Carcinog, 2018, 57(12): 1792-1802.
Yang J YJ, Ma T: TRIM11 promotes hepatocellular carcinogenesis through ubiquitin-proteasome mediated degradation of PHLPP1. Hepatology (Baltimore, Md), 2021.
Jiang T, Wang H, Liu L, Song H, Zhang Y, Wang J, Liu L, Xu T, Fan R, Xu Y et al: CircIL4R activates the PI3K/AKT signaling pathway via the miR-761/TRIM29/PHLPP1 axis and promotes proliferation and metastasis in colorectal cancer. Mol Cancer, 2021, 20(1): 167.
Shen W, Jin Z, Tong X, Wang H, Zhuang L, Lu X, Wu S: TRIM14 promotes cell proliferation and inhibits apoptosis by suppressing PTEN in colorectal cancer. Cancer Manag Res, 2019, 115725-5735.
Chen S, He Z, Zhu C, Liu Y, Li L, Deng L, Wang J, Yu C, Sun C: TRIM37 Mediates Chemoresistance and Maintenance of Stemness in Pancreatic Cancer Cells via Ubiquitination of PTEN and Activation of the AKT-GSK-3beta-beta-Catenin Signaling Pathway. Front Oncol, 2020, 10554787.
He R, Liu H: TRIM59 knockdown blocks cisplatin resistance in A549/DDP cells through regulating PTEN/AKT/HK2. Gene, 2020, 747144553.
Tantai J, Pan X, Chen Y, Shen Y, Ji C: TRIM46 activates AKT/HK2 signaling by modifying PHLPP2 ubiquitylation to promote glycolysis and chemoresistance of lung cancer cells. Cell Death Dis, 2022, 13(3): 285.
He Y, Jiang S, Mao C, Zheng H, Cao B, Zhang Z, Zhao J, Zeng Y, Mao X: The deubiquitinase USP10 restores PTEN activity and inhibits non-small cell lung cancer cell proliferation. J Biol Chem, 2021, 297(3): 101088.
He YM, Zhou XM, Jiang SY, Zhang ZB, Cao BY, Liu JB, Zeng YY, Zhao J, Mao XL: TRIM25 activates AKT/mTOR by inhibiting PTEN via K63-linked polyubiquitination in non-small cell lung cancer. Acta Pharmacol Sin, 2022, 43(3): 681-691.
Yuan P, Zheng A, Tang Q: Tripartite motif protein 25 is associated with epirubicin resistance in hepatocellular carcinoma cells via regulating PTEN/AKT pathway. Cell Biol Int, 2020, 44(7): 1503-1513.
Lee JT, Shan J, Zhong J, Li M, Zhou B, Zhou A, Parsons R, Gu W: RFP-mediated ubiquitination of PTEN modulates its effect on AKT activation. Cell Res, 2013, 23(4): 552-564.
Ma L, Yao N, Chen P, Zhuang Z: TRIM27 promotes the development of esophagus cancer via regulating PTEN/AKT signaling pathway. Cancer Cell Int, 2019, 19283.
Wang X, Cheng H, Zhao J, Li J, Chen Y, Cui K, Tian L, Zhang J, Li C, Sun S et al: Long noncoding RNA DLGAP1-AS2 promotes tumorigenesis and metastasis by regulating the Trim21/ELOA/LHPP axis in colorectal cancer. Mol Cancer, 2022, 21(1): 210.
Guo P, Ma X, Zhao W, Huai W, Li T, Qiu Y, Zhang Y, Han L: TRIM31 is upregulated in hepatocellular carcinoma and promotes disease progression by inducing ubiquitination of TSC1-TSC2 complex. Oncogene, 2018, 37(4): 478-488.
Yang C, Jin X, Liu X, Wu G, Yang W, Pang B, Jiang J, Liao D, Zhang Y: TRIM15 forms a regulatory loop with the AKT/FOXO1 axis and LASP1 to modulate the sensitivity of HCC cells to TKIs. Cell Death Dis, 2023, 14(1): 47.
Joo HM, Kim JY, Jeong JB, Seong KM, Nam SY, Yang KH, Kim CS, Kim HS, Jeong M, An S et al: Ret finger protein 2 enhances ionizing radiation-induced apoptosis via degradation of AKT and MDM2. Eur J Cell Biol, 2011, 90(5): 420-431.
Xian J, Liang D, Zhao C, Chen Y, Zhu Q: TRIM21 inhibits the osteogenic differentiation of mesenchymal stem cells by facilitating K48 ubiquitination-mediated degradation of Akt. Exp Cell Res, 2022, 412(2): 113034.
Yuan C, Liu J, Liu L, Jia H, Gao Q, Wang X, Zhao J: TRIM7 suppresses cell invasion and migration through inhibiting HIF-1alpha accumulation in clear cell renal cell carcinoma. Cell Biol Int, 2022, 46(4): 554-567.
Zhu L, Qin C, Li T, Ma X, Qiu Y, Lin Y, Ma D, Qin Z, Sun C, Shen X et al: The E3 ubiquitin ligase TRIM7 suppressed hepatocellular carcinoma progression by directly targeting Src protein. Cell Death Differ, 2020, 27(6): 1819-1831.
Lee JH, Liu R, Li J, Zhang C, Wang Y, Cai Q, Qian X, Xia Y, Zheng Y, Piao Y et al: Stabilization of phosphofructokinase 1 platelet isoform by AKT promotes tumorigenesis. Nat Commun, 2017, 8(1): 949.
Wang R, Huang KL, Xing LX: TRIM35 functions as a novel tumor suppressor in breast cancer by inducing cell apoptosis through ubiquitination of PDK1. Neoplasma, 2022, 69(2): 370-382.
Tian H, Lian R, Li Y, Liu C, Liang S, Li W, Tao T, Wu X, Ye Y, Yang X et al: AKT-induced lncRNA VAL promotes EMT-independent metastasis through diminishing Trim16-dependent Vimentin degradation. Nat Commun, 2020, 11(1): 5127.
Vasan N, Cantley LC: At a crossroads: how to translate the roles of PI3K in oncogenic and metabolic signalling into improvements in cancer therapy. Nat Rev Clin Oncol, 2022, 19(7): 471-485.
Ren H, Xu Y, Wang Q, Jiang J, Wudumuli, Hui L, Zhang Q, Zhang X, Wang E, Sun L et al: E3 ubiquitin ligase tripartite motif-containing 71 promotes the proliferation of non-small cell lung cancer through the inhibitor of kappaB-alpha/nuclear factor kappaB pathway. Oncotarget, 2018, 9(13): 10880-10890.
Gatt ME, Takada K, Mani M, Lerner M, Pick M, Hideshima T, Carrasco DE, Protopopov A, Ivanova E, Sangfelt O et al: TRIM13 (RFP2) downregulation decreases tumour cell growth in multiple myeloma through inhibition of NF Kappa B pathway and proteasome activity. Br J Haematol, 2013, 162(2): 210-220.
Xiao C, Zhang W, Hua M, Chen H, Yang B, Wang Y, Yang Q: TRIM27 interacts with Ikappabalpha to promote the growth of human renal cancer cells through regulating the NF-kappaB pathway. BMC Cancer, 2021, 21(1): 841.
Ji J, Ding K, Luo T, Zhang X, Chen A, Zhang D, Li G, Thorsen F, Huang B, Li X et al: TRIM22 activates NF-kappaB signaling in glioblastoma by accelerating the degradation of IkappaBalpha. Cell Death Differ, 2021, 28(1): 367-381.
Li Y, Deng L, Zhao X, Li B, Ren D, Yu L, Pan H, Gong Q, Song L, Zhou X et al: Tripartite motif-containing 37 (TRIM37) promotes the aggressiveness of non-small-cell lung cancer cells by activating the NF-kappaB pathway. J Pathol, 2018, 246(3): 366-378.
Yu C, Chen S, Guo Y, Sun C: Oncogenic TRIM31 confers gemcitabine resistance in pancreatic cancer via activating the NF-kappaB signaling pathway. Theranostics, 2018, 8(12): 3224-3236.
Wu G, Song L, Zhu J, Hu Y, Cao L, Tan Z, Zhang S, Li Z, Li J: An ATM/TRIM37/NEMO Axis Counteracts Genotoxicity by Activating Nuclear-to-Cytoplasmic NF-kappaB Signaling. Cancer Res, 2018, 78(22): 6399-6412.
Azuma K, Ikeda K, Suzuki T, Aogi K, Horie-Inoue K, Inoue S: TRIM47 activates NF-kappaB signaling via PKC-epsilon/PKD3 stabilization and contributes to endocrine therapy resistance in breast cancer. Proc Natl Acad Sci U S A, 2021, 118(35).
Jin J, Lu Z, Wang X, Liu Y, Han T, Wang Y, Wang T, Gan M, Xie C, Wang J et al: E3 ubiquitin ligase TRIM7 negatively regulates NF-kappa B signaling pathway by degrading p65 in lung cancer. Cell Signal, 2020, 69109543.
Xu L, Wu Q, Zhou X, Wu Q, Fang M: TRIM13 inhibited cell proliferation and induced cell apoptosis by regulating NF-kappaB pathway in non-small-cell lung carcinoma cells. Gene, 2019, 715144015.
Huang B, Baek SH: Trim13 Potentiates Toll-Like Receptor 2-Mediated Nuclear Factor kappaB Activation via K29-Linked Polyubiquitination of Tumor Necrosis Factor Receptor-Associated Factor 6. Mol Pharmacol, 2017, 91(4): 307-316.
Zhu J, Wu G, Ke Z, Cao L, Tang M, Li Z, Li Q, Zhou J, Tan Z, Song L et al: Targeting TRIM3 deletion-induced tumor-associated lymphangiogenesis prohibits lymphatic metastasis in esophageal squamous cell carcinoma. Oncogene, 2019, 38(15): 2736-2749.
Albor A, El-Hizawi S, Horn EJ, Laederich M, Frosk P, Wrogemann K, Kulesz-Martin M: The interaction of Piasy with Trim32, an E3-ubiquitin ligase mutated in limb-girdle muscular dystrophy type 2H, promotes Piasy degradation and regulates UVB-induced keratinocyte apoptosis through NFkappaB. J Biol Chem, 2006, 281(35): 25850-25866.
Albor A, Kulesz-Martin M: Novel initiation genes in squamous cell carcinomagenesis: a role for substrate-specific ubiquitylation in the control of cell survival. Mol Carcinog, 2007, 46(8): 585-590.
Jiang W, Cai X, Xu T, Liu K, Yang D, Fan L, Li G, Yu X: Tripartite Motif-Containing 46 Promotes Viability and Inhibits Apoptosis of Osteosarcoma Cells by Activating NF-B Signaling Through Ubiquitination of PPAR. Oncol Res, 2020, 28(4): 409-421.
Ding X, Xu J, Wang C, Feng Q, Wang Q, Yang Y, Lu H, Wang F, Zhu K, Li W et al: Suppression of the SAP18/HDAC1 complex by targeting TRIM56 and Nanog is essential for oncogenic viral FLICE-inhibitory protein-induced acetylation of p65/RelA, NF-kappaB activation, and promotion of cell invasion and angiogenesis. Cell Death Differ, 2019, 26(10): 1970-1986.
Zhou C, Zhang Z, Zhu X, Qian G, Zhou Y, Sun Y, Yu W, Wang J, Lu H, Lin F et al: N6-Methyladenosine modification of the TRIM7 positively regulates tumorigenesis and chemoresistance in osteosarcoma through ubiquitination of BRMS1. EBioMedicine, 2020, 59102955.
Liu Y, Mayo MW, Xiao A, Hall EH, Amin EB, Kadota K, Adusumilli PS, Jones DR: Loss of BRMS1 promotes a mesenchymal phenotype through NF-kappaB-dependent regulation of Twist1. Mol Cell Biol, 2015, 35(1): 303-317.
Caratozzolo MF, Micale L, Turturo MG, Cornacchia S, Fusco C, Marzano F, Augello B, D'Erchia AM, Guerrini L, Pesole G et al: TRIM8 modulates p53 activity to dictate cell cycle arrest. Cell Cycle, 2012, 11(3): 511-523.
Wang X, Zhang Y, Pei X, Guo G, Xue B, Duan X, Dou D: TRIM3 inhibits P53 signaling in breast cancer cells. Cancer Cell Int, 2020, 20(1): 559.
Han Y, Tan Y, Zhao Y, Zhang Y, He X, Yu L, Jiang H, Lu H, Tian H: TRIM23 overexpression is a poor prognostic factor and contributes to carcinogenesis in colorectal cancer. J Cell Mol Med, 2020, 24(10): 5491-5500.
Allton K, Jain AK, Herz HM, Tsai WW, Jung SY, Qin J, Bergmann A, Johnson RL, Barton MC: Trim24 targets endogenous p53 for degradation. Proc Natl Acad Sci U S A, 2009, 106(28): 11612-11616.
Liu J, Zhang C, Wang XL, Ly P, Belyi V, Xu-Monette ZY, Young KH, Hu W, Feng Z: E3 ubiquitin ligase TRIM32 negatively regulates tumor suppressor p53 to promote tumorigenesis. Cell Death Differ, 2014, 21(11): 1792-1804.
Han Y, Tian H, Chen P, Lin Q: TRIM47 overexpression is a poor prognostic factor and contributes to carcinogenesis in non-small cell lung carcinoma. Oncotarget, 2017, 8(14): 22730-22740.
Zhou Z, Ji Z, Wang Y, Li J, Cao H, Zhu HH, Gao WQ: TRIM59 is up-regulated in gastric tumors, promoting ubiquitination and degradation of p53. Gastroenterology, 2014, 147(5): 1043-1054.
Liang J, Xing D, Li Z, Shen J, Zhao H, Li S: TRIM59 is upregulated and promotes cell proliferation and migration in human osteosarcoma. Mol Med Rep, 2016, 13(6): 5200-5206.
Li Y, Ma C, Zhou T, Liu Y, Sun L, Yu Z: TRIM65 negatively regulates p53 through ubiquitination. Biochem Biophys Res Commun, 2016, 473(1): 278-282.
Liu R, Li H, Xu Y, Li X, Guo X, Shi J, Cui Y, Wang Z, Liu J: Blockade of TRIM59 enhances esophageal cancer cell chemosensitivity to cisplatin by upregulating p53. Oncol Lett, 2021, 21(1): 6.
Guo P, Qiu Y, Ma X, Li T, Ma X, Zhu L, Lin Y, Han L: Tripartite motif 31 promotes resistance to anoikis of hepatocarcinoma cells through regulation of p53-AMPK axis. Exp Cell Res, 2018, 368(1): 59-66.
Zhang L, Huang NJ, Chen C, Tang W, Kornbluth S: Ubiquitylation of p53 by the APC/C inhibitor Trim39. Proc Natl Acad Sci U S A, 2012, 109(51): 20931-20936.
Doyle JM, Gao J, Wang J, Yang M, Potts PR: MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol Cell, 2010, 39(6): 963-974.
Mao H, Du Y, Zhang Z, Cao B, Zhao J, Zhou H, Mao X: Nitroxoline shows antimyeloma activity by targeting the TRIM25/p53 axle. Anticancer Drugs, 2017, 28(4): 376-383.
Chen JX, Xu D, Cao JW, Zuo L, Han ZT, Tian YJ, Chu CM, Zhou W, Pan XW, Cui XG: TRIM47 promotes malignant progression of renal cell carcinoma by degrading P53 through ubiquitination. Cancer Cell Int, 2021, 21(1): 129.
Chen Y, Hao Q, Wang J, Li J, Huang C, Zhang Y, Wu X, Lu H, Zhou X: Ubiquitin ligase TRIM71 suppresses ovarian tumorigenesis by degrading mutant p53. Cell Death Dis, 2019, 10(10): 737.
Sho T, Tsukiyama T, Sato T, Kondo T, Cheng J, Saku T, Asaka M, Hatakeyama S: TRIM29 negatively regulates p53 via inhibition of Tip60. Biochim Biophys Acta, 2011, 1813(6): 1245-1253.
Wang J, Yang F, Zhuang J, Huo Q, Li J, Xie N: TRIM58 inactivates p53/p21 to promote chemoresistance via ubiquitination of DDX3 in breast cancer. Int J Biochem Cell Biol, 2022, 143106140.
Su X, Feng C, Wang S, Shi L, Gu Q, Zhang H, Lan X, Zhao Y, Qiang W, Ji M et al: The noncoding RNAs SNORD50A and SNORD50B-mediated TRIM21-GMPS interaction promotes the growth of p53 wild-type breast cancers by degrading p53. Cell Death Differ, 2021, 28(8): 2450-2464.
Guha A, Ahuja D, Das Mandal S, Parasar B, Deyasi K, Roy D, Sharma V, Willard B, Ghosh A, Ray PS: Integrated Regulation of HuR by Translation Repression and Protein Degradation Determines Pulsatile Expression of p53 Under DNA Damage. iScience, 2019, 15342-359.
Reddy BA, van der Knaap JA, Bot AG, Mohd-Sarip A, Dekkers DH, Timmermans MA, Martens JW, Demmers JA, Verrijzer CP: Nucleotide biosynthetic enzyme GMP synthase is a TRIM21-controlled relay of p53 stabilization. Mol Cell, 2014, 53(3): 458-470.
Guo Y, Li Q, Zhao G, Zhang J, Yuan H, Feng T, Ou D, Gu R, Li S, Li K et al: Loss of TRIM31 promotes breast cancer progression through regulating K48- and K63-linked ubiquitination of p53. Cell Death Dis, 2021, 12(10): 945.
Zhang J, Zhang C, Cui J, Ou J, Han J, Qin Y, Zhi F, Wang RF: TRIM45 functions as a tumor suppressor in the brain via its E3 ligase activity by stabilizing p53 through K63-linked ubiquitination. Cell Death Dis, 2017, 8(5): e2831.
Piao MY, Cao HL, He NN, Xu MQ, Dong WX, Wang WQ, Wang BM, Zhou B: Potential role of TRIM3 as a novel tumour suppressor in colorectal cancer (CRC) development. Scand J Gastroenterol, 2016, 51(5): 572-582.
Tong X, Mu P, Zhang Y, Zhao J, Wang X: TRIM59, amplified in ovarian cancer, promotes tumorigenesis through the MKP3/ERK pathway. J Cell Physiol, 2020, 235(11): 8236-8245.
Chakraborty A, Diefenbacher ME, Mylona A, Kassel O, Behrens A: The E3 ubiquitin ligase Trim7 mediates c-Jun/AP-1 activation by Ras signalling. Nat Commun, 2015, 66782.
Zhu H, Chen Y, Zhang J, Qian C, Qiu W, Shen H, Shen Z: Knockdown of TRIM37 Promotes Apoptosis and Suppresses Tumor Growth in Gastric Cancer by Inactivation of the ERK1/2 Pathway. Onco Targets Ther, 2020, 135479-5491.
Wang XL, Lu SC, Sun C, Jin WG, Fan YW, Shu YS, Shi HC, Min LF: Tripartite motif protein 11 (TRIM11), an oncogene for human lung cancer via the DUSP6-mediated ERK1/2 signaling pathway. Cancer Biol Ther, 2021, 22(4): 324-332.
Zhang J, Li YQ, Guo R, Wang YQ, Zhang PP, Tang XR, Wen X, Hong XH, Lei Y, He QM et al: Hypermethylation of SHISA3 Promotes Nasopharyngeal Carcinoma Metastasis by Reducing SGSM1 Stability. Cancer Res, 2019, 79(4): 747-759.
Liu K, Zhang C, Li B, Xie W, Zhang J, Nie X, Tan P, Zheng L, Wu S, Qin Y et al: Mutual Stabilization between TRIM9 Short Isoform and MKK6 Potentiates p38 Signaling to Synergistically Suppress Glioblastoma Progression. Cell Rep, 2018, 23(3): 838-851.
Okumura F, Matsunaga Y, Katayama Y, Nakayama KI, Hatakeyama S: TRIM8 modulates STAT3 activity through negative regulation of PIAS3. J Cell Sci, 2010, 123(Pt 13): 2238-2245.
Zhang C, Mukherjee S, Tucker-Burden C, Ross JL, Chau MJ, Kong J, Brat DJ: TRIM8 regulates stemness in glioblastoma through PIAS3-STAT3. Mol Oncol, 2017, 11(3): 280-294.
Sun W, Wang Y, Li D, Wu Y, Ji Q, Sun T: Tripartite motif containing 14: An oncogene in papillary thyroid carcinoma. Biochem Biophys Res Commun, 2020, 521(2): 360-367.
Pan S, Deng Y, Fu J, Zhang Y, Zhang Z, Ru X, Qin X: TRIM52 promotes colorectal cancer cell proliferation through the STAT3 signaling. Cancer Cell Int, 2019, 1957.
Zhao H, Huang J, Chen M, Li B, Chen X, Zhou M: Tripartite Motif Protein 6 Promotes Colorectal Cancer Cell Migration and Metastasis via SOCS2-STAT3 Signaling. Front Oncol, 2021, 11695525.
Vogelstein B, Kinzler KW: Cancer genes and the pathways they control. Nat Med, 2004, 10(8): 789-799.
Hou Y, Ding M, Wang C, Yang X, Ye T, Yu H: TRIM11 promotes lymphomas by activating the beta-catenin signaling and Axin1 ubiquitination degradation. Exp Cell Res, 2020, 387(2): 111750.
Zhou L, Wang H, Zhong M, Fang Z, Le Y, Nie F, Zhou J, Xiong J, Xiang X, Fang Z: The E3 Ubiquitin Ligase TRIM11 Facilitates Gastric Cancer Progression by Activating the Wnt/beta-Catenin Pathway via Destabilizing Axin1 Protein. J Oncol, 2022, 20228264059.
Yang YF, Zhang MF, Tian QH, Zhang CZ: TRIM65 triggers beta-catenin signaling via ubiquitylation of Axin1 to promote hepatocellular carcinoma. J Cell Sci, 2017, 130(18): 3108-3115.
Zhang R, Li SW, Liu L, Yang J, Huang G, Sang Y: TRIM11 facilitates chemoresistance in nasopharyngeal carcinoma by activating the beta-catenin/ABCC9 axis via p62-selective autophagic degradation of Daple. Oncogenesis, 2020, 9(5): 45.
Liu S, Tian Y, Zheng Y, Cheng Y, Zhang D, Jiang J, Li S: TRIM27 acts as an oncogene and regulates cell proliferation and metastasis in non-small cell lung cancer through SIX3-beta-catenin signaling. Aging (Albany NY), 2020, 12(24): 25564-25580.
Wang L, Heidt DG, Lee CJ, Yang H, Logsdon CD, Zhang L, Fearon ER, Ljungman M, Simeone DM: Oncogenic function of ATDC in pancreatic cancer through Wnt pathway activation and beta-catenin stabilization. Cancer Cell, 2009, 15(3): 207-219.
Xue J, Chen Y, Wu Y, Wang Z, Zhou A, Zhang S, Lin K, Aldape K, Majumder S, Lu Z et al: Tumour suppressor TRIM33 targets nuclear beta-catenin degradation. Nat Commun, 2015, 66156.
Liu X, Long Z, Cai H, Yu S, Wu J: TRIM58 suppresses the tumor growth in gastric cancer by inactivation of beta-catenin signaling via ubiquitination. Cancer Biol Ther, 2020, 21(3): 203-212.
Zhao B, Qiao G, Li J, Wang Y, Li X, Zhang H, Zhang L: TRIM36 suppresses cell growth and promotes apoptosis in human esophageal squamous cell carcinoma cells by inhibiting Wnt/beta-catenin signaling pathway. Hum Cell, 2022, 35(5): 1487-1498.
Li R, Xu P, Jin X, Shi Z, Zhang Q, Ye F, Yu W, Ji T: TRIM50 Inhibits Proliferation and Metastasis of Gastric Cancer via Promoting beta-Catenin Degradation. J Oncol, 2022, 20225936753.
Miao C, Liang C, Li P, Liu B, Qin C, Yuan H, Liu Y, Zhu J, Cui Y, Xu A et al: TRIM37 orchestrates renal cell carcinoma progression via histone H2A ubiquitination-dependent manner. J Exp Clin Cancer Res, 2021, 40(1): 195.
Liang Q, Tang C, Tang M, Zhang Q, Gao Y, Ge Z: TRIM47 is up-regulated in colorectal cancer, promoting ubiquitination and degradation of SMAD4. J Exp Clin Cancer Res, 2019, 38(1): 159.
Zhang Y, Tao R, Wu SS, Xu CC, Wang JL, Chen J, Yu YS, Tang ZH, Chen XH, Zang GQ: TRIM52 up-regulation in hepatocellular carcinoma cells promotes proliferation, migration and invasion through the ubiquitination of PPM1A. J Exp Clin Cancer Res, 2018, 37(1): 116.
Chen N, Balasenthil S, Reuther J, Killary AM: DEAR1, a novel tumor suppressor that regulates cell polarity and epithelial plasticity. Cancer Res, 2014, 74(20): 5683-5689.
Chen N, Balasenthil S, Reuther J, Frayna A, Wang Y, Chandler DS, Abruzzo LV, Rashid A, Rodriguez J, Lozano G et al: DEAR1 is a chromosome 1p35 tumor suppressor and master regulator of TGF-beta-driven epithelial-mesenchymal transition. Cancer Discov, 2013, 3(10): 1172-1189.
Chen X, Li Z, Yong H, Wang W, Wang D, Chu S, Li M, Hou P, Zheng J, Bai J: Trim21-mediated HIF-1alpha degradation attenuates aerobic glycolysis to inhibit renal cancer tumorigenesis and metastasis. Cancer Lett, 2021, 508115-126.
Xie P, Peng Z, Chen Y, Li H, Du M, Tan Y, Zhang X, Lu Z, Cui CP, Liu CH et al: Neddylation of PTEN regulates its nuclear import and promotes tumor development. Cell Res, 2021, 31(3): 291-311.
Liu W, Zhao Y, Wang G, Feng S, Ge X, Ye W, Wang Z, Zhu Y, Cai W, Bai J et al: TRIM22 inhibits osteosarcoma progression through destabilizing NRF2 and thus activation of ROS/AMPK/mTOR/autophagy signaling. Redox Biol, 2022, 53102344.
Zhao X, Zhou T, Wang Y, Bao M, Ni C, Ding L, Sun S, Dong H, Li J, Liang C: Trigred motif 36 regulates neuroendocrine differentiation of prostate cancer via HK2 ubiquitination and GPx4 deficiency. Cancer Sci, 2023, 114(6): 2445-2459.
Wang X, He H, Rui W, Zhang N, Zhu Y, Xie X: TRIM38 triggers the uniquitination and degradation of glucose transporter type 1 (GLUT1) to restrict tumor progression in bladder cancer. J Transl Med, 2021, 19(1): 508.
Jin X, Pan Y, Wang L, Zhang L, Ravichandran R, Potts PR, Jiang J, Wu H, Huang H: MAGE-TRIM28 complex promotes the Warburg effect and hepatocellular carcinoma progression by targeting FBP1 for degradation. Oncogenesis, 2017, 6(4): e312.
Li L, Yu Y, Zhang Z, Guo Y, Yin T, Wu H, Yang M: TRIM47 accelerates aerobic glycolysis and tumor progression through regulating ubiquitination of FBP1 in pancreatic cancer. Pharmacol Res, 2021, 166105429.
Pineda CT, Ramanathan S, Fon Tacer K, Weon JL, Potts MB, Ou YH, White MA, Potts PR: Degradation of AMPK by a cancer-specific ubiquitin ligase. Cell, 2015, 160(4): 715-728.
Han J, Zhao Z, Zhang N, Yang Y, Ma L, Feng L, Zhang X, Zuo J, Fan Z, Wang Y et al: Transcriptional dysregulation of TRIM29 promotes colorectal cancer carcinogenesis via pyruvate kinase-mediated glucose metabolism. Aging (Albany NY), 2021, 13(4): 5034-5054.
Tang J, Luo Y, Tian Z, Liao X, Cui Q, Yang Q, Wu G: TRIM11 promotes breast cancer cell proliferation by stabilizing estrogen receptor alpha. Neoplasia, 2020, 22(9): 343-351.
Deng X, Fu X, Teng H, Fang L, Liang B, Zeng R, Chen L, Zou Y: E3 ubiquitin ligase TRIM29 promotes pancreatic cancer growth and progression via stabilizing Yes-associated protein 1. J Transl Med, 2021, 19(1): 332.
Sato T, Okumura F, Iguchi A, Ariga T, Hatakeyama S: TRIM32 promotes retinoic acid receptor alpha-mediated differentiation in human promyelogenous leukemic cell line HL60. Biochem Biophys Res Commun, 2012, 417(1): 594-600.
Sato T, Okumura F, Kano S, Kondo T, Ariga T, Hatakeyama S: TRIM32 promotes neural differentiation through retinoic acid receptor-mediated transcription. J Cell Sci, 2011, 124(Pt 20): 3492-3502.
Yao J, Xu T, Tian T, Fu X, Wang W, Li S, Shi T, Suo A, Ruan Z, Guo H et al: Tripartite motif 16 suppresses breast cancer stem cell properties through regulation of Gli-1 degradation via the ubiquitin-proteasome pathway. Oncol Rep, 2016, 35(2): 1204-1212.
Li L, Dong L, Qu X, Jin S, Lv X, Tan G: Tripartite motif 16 inhibits hepatocellular carcinoma cell migration and invasion. Int J Oncol, 2016, 48(4): 1639-1649.
Ruan L, Liu W, Yang Y, Chu Z, Yang C, Yang T, Sun J: TRIM16 overexpression inhibits the metastasis of colorectal cancer through mediating Snail degradation. Exp Cell Res, 2021, 406(1): 112735.
Qin B, Zou S, Li K, Wang H, Wei W, Zhang B, Xiao L, Choi HH, Tang Q, Huang D et al: CSN6-TRIM21 axis instigates cancer stemness during tumorigenesis. Br J Cancer, 2020, 122(11): 1673-1685.
Jin Y, Zhang Y, Li B, Zhang J, Dong Z, Hu X, Wan Y: TRIM21 mediates ubiquitination of Snail and modulates epithelial to mesenchymal transition in breast cancer cells. Int J Biol Macromol, 2019, 124846-853.
Deng M, Wei W, Duan J, Chen R, Wang N, He L, Peng Y, Ma X, Wu Z, Liu J et al: ZHX3 promotes the progression of urothelial carcinoma of the bladder via repressing of RGS2 and is a novel substrate of TRIM21. Cancer Sci, 2021, 112(5): 1758-1771.
Liu Q, Sheng Z, Cheng C, Zheng H, Lanuti M, Liu R, Wang P, Shen Y, Xie Z: Anesthetic Propofol Promotes Tumor Metastasis in Lungs via GABA(A) R-Dependent TRIM21 Modulation of Src Expression. Adv Sci (Weinh), 2021, 8(18): e2102079.
Ping M, Wang S, Guo Y, Jia J: TRIM21 improves apatinib treatment in gastric cancer through suppressing EZH1 stability. Biochem Biophys Res Commun, 2022, 586177-184.
Feng X, Jiang T, Yang C, Pang S, Ding Z, Hu H, Wang H, Dong L, Yang N: RPRD1A stabilizes NRF2 and aggravates HCC progression through competing with p62 for TRIM21 binding. Cell Death Dis, 2021, 13(1): 6.
Jian Y, Kong L, Xu H, Shi Y, Huang X, Zhong W, Huang S, Li Y, Shi D, Xiao Y et al: Protein phosphatase 1 regulatory inhibitor subunit 14C promotes triple-negative breast cancer progression via sustaining inactive glycogen synthase kinase 3 beta. Clin Transl Med, 2022, 12(1): e725.
Liu Y, Tao S, Liao L, Li Y, Li H, Li Z, Lin L, Wan X, Yang X, Chen L: TRIM25 promotes the cell survival and growth of hepatocellular carcinoma through targeting Keap1-Nrf2 pathway. Nat Commun, 2020, 11(1): 348.
Li B, Zhu L, Lu C, Wang C, Wang H, Jin H, Ma X, Cheng Z, Yu C, Wang S et al: circNDUFB2 inhibits non-small cell lung cancer progression via destabilizing IGF2BPs and activating anti-tumor immunity. Nat Commun, 2021, 12(1): 295.
Wang S, Kollipara RK, Humphries CG, Ma SH, Hutchinson R, Li R, Siddiqui J, Tomlins SA, Raj GV, Kittler R: The ubiquitin ligase TRIM25 targets ERG for degradation in prostate cancer. Oncotarget, 2016, 7(40): 64921-64931.
Chen JJ, Ren YL, Shu CJ, Zhang Y, Chen MJ, Xu J, Li J, Li AP, Chen DY, He JD et al: JP3, an antiangiogenic peptide, inhibits growth and metastasis of gastric cancer through TRIM25/SP1/MMP2 axis. J Exp Clin Cancer Res, 2020, 39(1): 118.
Zang HL, Ren SN, Cao H, Tian XF: The ubiquitin ligase TRIM25 inhibits hepatocellular carcinoma progression by targeting metastasis associated 1 protein. IUBMB Life, 2017, 69(10): 795-801.
Yuan J, Song Y, Pan W, Li Y, Xu Y, Xie M, Shen Y, Zhang N, Liu J, Hua H et al: LncRNA SLC26A4-AS1 suppresses the MRN complex-mediated DNA repair signaling and thyroid cancer metastasis by destabilizing DDX5. Oncogene, 2020, 39(43): 6664-6676.
Ma X, Ma X, Qiu Y, Zhu L, Lin Y, You Y, Ma D, Qin Z, Sun C, Zhao Y et al: TRIM50 suppressed hepatocarcinoma progression through directly targeting SNAIL for ubiquitous degradation. Cell Death Dis, 2018, 9(6): 608.
Qiu Y, Liu P, Ma X, Ma X, Zhu L, Lin Y, You Y, Yu W, Ma D, Sun C et al: TRIM50 acts as a novel Src suppressor and inhibits ovarian cancer progression. Biochim Biophys Acta Mol Cell Res, 2019, 1866(9): 1412-1420.
Chen D, Li Y, Zhang X, Wu H, Wang Q, Cai J, Cui Y, Liu H, Lan P, Wang J et al: Ubiquitin ligase TRIM65 promotes colorectal cancer metastasis by targeting ARHGAP35 for protein degradation. Oncogene, 2019, 38(37): 6429-6444.
Wei WS, Chen X, Guo LY, Li XD, Deng MH, Yuan GJ, He LY, Li YH, Zhang ZL, Jiang LJ et al: TRIM65 supports bladder urothelial carcinoma cell aggressiveness by promoting ANXA2 ubiquitination and degradation. Cancer Lett, 2018, 43510-22.
Chen X, Dong C, Law PT, Chan MT, Su Z, Wang S, Wu WK, Xu H: MicroRNA-145 targets TRIM2 and exerts tumor-suppressing functions in epithelial ovarian cancer. Gynecol Oncol, 2015, 139(3): 513-519.
Thompson S, Pearson AN, Ashley MD, Jessick V, Murphy BM, Gafken P, Henshall DC, Morris KT, Simon RP, Meller R: Identification of a novel Bcl-2-interacting mediator of cell death (Bim) E3 ligase, tripartite motif-containing protein 2 (TRIM2), and its role in rapid ischemic tolerance-induced neuroprotection. J Biol Chem, 2011, 286(22): 19331-19339.
Yin H, Zhu Q, Liu M, Tu G, Li Q, Yuan J, Wen S, Yang G: GPER promotes tamoxifen-resistance in ER+ breast cancer cells by reduced Bim proteins through MAPK/Erk-TRIM2 signaling axis. Int J Oncol, 2017, 51(4): 1191-1198.
Lin Z, Lin X, Zhu L, Huang J, Huang Y: TRIM2 directly deubiquitinates and stabilizes Snail1 protein, mediating proliferation and metastasis of lung adenocarcinoma. Cancer Cell Int, 2020, 20228.
Lu M, Chen W, Zhuang W, Zhan X: Label-free quantitative identification of abnormally ubiquitinated proteins as useful biomarkers for human lung squamous cell carcinomas. EPMA J, 2020, 11(1): 73-94.
Wei C, Wu J, Liu W, Lu J, Li H, Hai B: Tripartite motif-containing protein 6 facilitates growth and migration of breast cancer through degradation of STUB1. Eur J Histochem, 2021, 65(1).
Xie Y, Zhao Y, Shi L, Li W, Chen K, Li M, Chen X, Zhang H, Li T, Matsuzawa-Ishimoto Y et al: Gut epithelial TSC1/mTOR controls RIPK3-dependent necroptosis in intestinal inflammation and cancer. J Clin Invest, 2020, 130(4): 2111-2128.
Yang PB, Hou PP, Liu FY, Hong WB, Chen HZ, Sun XY, Li P, Zhang Y, Ju CY, Luo LJ et al: Blocking PPARgamma interaction facilitates Nur77 interdiction of fatty acid uptake and suppresses breast cancer progression. Proc Natl Acad Sci U S A, 2020, 117(44): 27412-27422.
Yu B, Zhou Y, He J: TRIM13 inhibits cell proliferation and induces autophagy in lung adenocarcinoma by regulating KEAP1/NRF2 pathway. Cell Cycle, 2023, 1-18.
Liang M, Wang L, Sun Z, Chen X, Wang H, Qin L, Zhao W, Geng B: E3 ligase TRIM15 facilitates non-small cell lung cancer progression through mediating Keap1-Nrf2 signaling pathway. Cell Commun Signal, 2022, 20(1): 62.
Sun Y, Ren D, Yang C, Yang W, Zhao J, Zhou Y, Jin X, Wu H: TRIM15 promotes the invasion and metastasis of pancreatic cancer cells by mediating APOA1 ubiquitination and degradation. Biochim Biophys Acta Mol Basis Dis, 2021, 1867(11): 166213.
Endo H, Ikeda K, Urano T, Horie-Inoue K, Inoue S: Terf/TRIM17 stimulates degradation of kinetochore protein ZWINT and regulates cell proliferation. J Biochem, 2012, 151(2): 139-144.
Zhong T, Zhang J, Liu X, Li H: TRIM17-mediated ubiquitination and degradation of RBM38 promotes cisplatin resistance in non-small cell lung cancer. Cell Oncol (Dordr), 2023.
Bian Z, Zhou M, Cui K, Yang F, Cao Y, Sun S, Liu B, Gong L, Li J, Wang X et al: SNHG17 promotes colorectal tumorigenesis and metastasis via regulating Trim23-PES1 axis and miR-339-5p-FOSL2-SNHG17 positive feedback loop. J Exp Clin Cancer Res, 2021, 40(1): 360.
Wei J, Wang L, Zhang Y, Sun T, Zhang C, Hu Z, Zhou L, Liu X, Wan J, Ma L: TRIM25 promotes temozolomide resistance in glioma by regulating oxidative stress and ferroptotic cell death via the ubiquitination of keap1. Oncogene, 2023.
Xing L, Tang X, Wu K, Huang X, Yi Y, Huan J: TRIM27 Functions as a Novel Oncogene in Non-Triple-Negative Breast Cancer by Blocking Cellular Senescence through p21 Ubiquitination. Mol Ther Nucleic Acids, 2020, 22910-923.
Lionnard L, Duc P, Brennan MS, Kueh AJ, Pal M, Guardia F, Mojsa B, Damiano MA, Mora S, Lassot I et al: TRIM17 and TRIM28 antagonistically regulate the ubiquitination and anti-apoptotic activity of BCL2A1. Cell Death Differ, 2019, 26(5): 902-917.
Horn EJ, Albor A, Liu Y, El-Hizawi S, Vanderbeek GE, Babcock M, Bowden GT, Hennings H, Lozano G, Weinberg WC et al: RING protein Trim32 associated with skin carcinogenesis has anti-apoptotic and E3-ubiquitin ligase properties. Carcinogenesis, 2004, 25(2): 157-167.
Kano S, Miyajima N, Fukuda S, Hatakeyama S: Tripartite motif protein 32 facilitates cell growth and migration via degradation of Abl-interactor 2. Cancer Res, 2008, 68(14): 5572-5580.
Ryu YS, Lee Y, Lee KW, Hwang CY, Maeng JS, Kim JH, Seo YS, You KH, Song B, Kwon KS: TRIM32 protein sensitizes cells to tumor necrosis factor (TNFalpha)-induced apoptosis via its RING domain-dependent E3 ligase activity against X-linked inhibitor of apoptosis (XIAP). J Biol Chem, 2011, 286(29): 25729-25738.
Tan X, Cao F, Tang F, Lu C, Yu Q, Feng S, Yang Z, Chen S, He X, He J et al: Suppression of DLBCL Progression by the E3 Ligase Trim35 Is Mediated by CLOCK Degradation and NK Cell Infiltration. J Immunol Res, 2021, 20219995869.
Yu S, Li W, Liu X, Zhang H, Liu X, Zhang LW: TRIM36 enhances lung adenocarcinoma radiosensitivity and inhibits tumorigenesis through promoting RAD51 ubiquitination and antagonizing hsa-miR-376a-5p. Biochem Biophys Res Commun, 2022, 6281-10.
Przanowski P, Lou S, Tihagam RD, Mondal T, Conlan C, Shivange G, Saltani I, Singh C, Xing K, Morris BB et al: Oncogenic TRIM37 Links Chemoresistance and Metastatic Fate in Triple-Negative Breast Cancer. Cancer Res, 2020, 80(21): 4791-4804.
Chen Z, Lin TC, Bi X, Lu G, Dawson BC, Miranda R, Medeiros LJ, McNiece I, McCarty N: TRIM44 promotes quiescent multiple myeloma cell occupancy and survival in the osteoblastic niche via HIF-1alpha stabilization. Leukemia, 2019, 33(2): 469-486.
Hirata Y, Katagiri K, Nagaoka K, Morishita T, Kudoh Y, Hatta T, Naguro I, Kano K, Udagawa T, Natsume T et al: TRIM48 Promotes ASK1 Activation and Cell Death through Ubiquitination-Dependent Degradation of the ASK1-Negative Regulator PRMT1. Cell Rep, 2017, 21(9): 2447-2457.
Li R, Zhu L, Peng Y, Zhang X, Dai C, Liu D: TRIM50 Suppresses Pancreatic Cancer Progression and Reverses the Epithelial-Mesenchymal Transition via Facilitating the Ubiquitous Degradation of Snail1. Front Oncol, 2021, 11695740.
Cao H, Li Y, Chen L, Lu Z, You T, Wang X, Ji B: Tripartite motif-containing 54 promotes gastric cancer progression by upregulating K63-linked ubiquitination of filamin C. Asia Pac J Clin Oncol, 2022, 18(6): 669-677.
Lin M, Fang Z, Lin X, Zhou W, Wang Y, Han S, Ye M, Zhu F: TRIM55 inhibits colorectal cancer development via enhancing protein degradation of c-Myc. Cancer Med, 2023.
Zhao L, Zhang P, Su XJ, Zhang B: The ubiquitin ligase TRIM56 inhibits ovarian cancer progression by targeting vimentin. J Cell Physiol, 2018, 233(3): 2420-2425.
Yang X, Zhang Y, Xue Z, Hu Y, Zhou W, Xue Z, Liu X, Liu G, Li W, Liu X et al: TRIM56 promotes malignant progression of glioblastoma by stabilizing cIAP1 protein. J Exp Clin Cancer Res, 2022, 41(1): 336.
Liang M, Chen X, Wang L, Qin L, Wang H, Sun Z, Zhao W, Geng B: Cancer-derived exosomal TRIM59 regulates macrophage NLRP3 inflammasome activation to promote lung cancer progression. J Exp Clin Cancer Res, 2020, 39(1): 176.
Yin J, Kim TH, Park N, Shin D, Choi HI, Cho S, Park JB, Kim JH: TRIM71 suppresses tumorigenesis via modulation of Lin28B-let-7-HMGA2 signaling. Oncotarget, 2016, 7(48): 79854-79868.
Li X, Yang C, Luo N, Yang Y, Guo Y, Chen P, Cun B: Ubiquitination and degradation of MGMT by TRIM72 increases the sensitivity of uveal melanoma cells to Dacarbazine treatment. Cancer Biomark, 2022, 34(2): 275-284.
Downloads
Published
How to Cite
Issue
Section
