Overexpression of the TRIM24 E3 Ubiquitin Ligase is Linked to Genetic Instability and Predicts Unfavorable Prognosis in Prostate Cancer.

Aged Carrier Proteins / biosynthesis Disease-Free Survival Follow-Up Studies Gene Expression Regulation, Enzymologic Gene Expression Regulation, Neoplastic Genomic Instability Humans Male Middle Aged Neoplasm Proteins / biosynthesis Prostatic Neoplasms / enzymology Retrospective Studies Survival Rate Ubiquitin-Protein Ligases / biosynthesis

Journal

Applied immunohistochemistry & molecular morphology : AIMM

ISSN: 1533-4058

Titre abrégé: Appl Immunohistochem Mol Morphol

Pays: United States

ID NLM: 100888796

Informations de publication

Date de publication:
01 04 2021

Historique:

received: 24 09 2020

accepted: 25 11 2020

pubmed: 26 1 2021

medline: 15 12 2021

entrez: 25 1 2021

Statut: ppublish

Résumé

Tripartite motif containing 24 (TRIM24) is a multifunctional protein involved in p53 degradation, chromatin binding, and transcriptional modulation of nuclear receptors. Emerging research has revealed that upregulation of TRIM24 in numerous tumor types is linked to poor prognosis, attributing an important role to TRIM24 in tumor biology. In order to better understand the role of TRIM24 in prostate cancer, we analyzed its immunohistochemical expression on a tissue microarray containing >17,000 prostate cancer specimens. TRIM24 immunostaining was detectable in 61% of 15,321 interpretable cancers, including low expression in 46% and high expression in 15% of cases. TRIM24 upregulation was associated with high Gleason grade, advanced pathologic tumor stage, lymph node metastasis, higher preoperative prostate-specific antigen level, increased cell proliferation as well as increased genomic instability, and predicted prognosis independent of clinicopathologic parameters available at the time of the initial biopsy (all P<0.0001). TRIM24 upregulation provides additional prognostic information in prostate cancer, particularly in patients with low Gleason grade tumors who may be eligible for active surveillance strategies, suggesting promising potential for TRIM24 in the routine diagnostic work-up of these patients.

Identifiants

DOI: 10.1097/PAI.0000000000000901 PMID: 33491944

pubmed: 33491944

doi: 10.1097/PAI.0000000000000901

pii: 00129039-202104000-00013

doi:

Substances chimiques

Carrier Proteins 0

Neoplasm Proteins 0

TRIM24 protein, human 0

Ubiquitin-Protein Ligases EC 2.3.2.27

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

e29-e38

Informations de copyright

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

Références

Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.

Fenton JJ, Weyrich MS, Durbin S, et al. Prostate-specific antigen-based screening for prostate cancer: evidence report and systematic review for the US Preventive Services Task Force. JAMA. 2018;319:1914–1931.

Wilt TJ, Jones KM, Barry MJ, et al. Follow-up of prostatectomy versus observation for early prostate cancer. N Engl J Med. 2017;377:132–142.

Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.

Ozato K, Shin DM, Chang TH, et al. TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol. 2008;8:849–860.

Hatakeyama S. TRIM proteins and cancer. Nat Rev Cancer. 2011;11:792–804.

Meroni G, Diez-Roux G. TRIM/RBCC, a novel class of ‘single protein RING finger’ E3 ubiquitin ligases. BioEssays. 2005;27:1147–1157.

Zhang J, Xu Z, Yu B, et al. Tripartite motif containing 35 contributes to the proliferation, migration, and invasion of lung cancer cells in vitro and in vivo. Biosci Rep. 2020;40:4.

Han Y, Tan Y, Zhao Y, et al. TRIM23 overexpression is a poor prognostic factor and contributes to carcinogenesis in colorectal cancer. J Cell Mol Med. 2020;24:5491–5500.

Jaworska AM, Wlodarczyk NA, Mackiewicz A, et al. The role of TRIM family proteins in the regulation of cancer stem cell self-renewal. Stem Cells. 2020;38:165–173.

Appikonda S, Thakkar KN, Shah PK, et al. Cross-talk between chromatin acetylation and SUMOylation of tripartite motif-containing protein 24 (TRIM24) impacts cell adhesion. J Biol Chem. 2018;293:7476–7485.

Le Douarin B, Zechel C, Garnier JM, et al. The N-terminal part of TIF1, a putative mediator of the ligand-dependent activation function (AF-2) of nuclear receptors, is fused to B-raf in the oncogenic protein T18. EMBO J. 1995;14:2020–2033.

Le Douarin B, Nielsen AL, Garnier JM, et al. A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J. 1996;15:6701–6715.

Allton K, Jain AK, Herz HM, et al. Trim24 targets endogenous p53 for degradation. Proc Natl Acad Sci USA. 2009;106:11612–11616.

Jain AK, Barton MC. Regulation of p53: TRIM24 enters the RING. Cell Cycle. 2009;8:3668–3674.

Bennett J, Fedorov O, Tallant C, et al. Discovery of a Chemical Tool Inhibitor Targeting the Bromodomains of TRIM24 and BRPF. J Med Chem. 2016;59:1642–1647.

Palmer WS, Poncet-Montange G, Liu G, et al. Structure-Guided Design of IACS-9571, a Selective High-Affinity Dual TRIM24-BRPF1 Bromodomain Inhibitor. J Med Chem. 2016;59:1440–1454.

Wang J, Zhu J, Dong M, et al. Knockdown of tripartite motif containing 24 by lentivirus suppresses cell growth and induces apoptosis in human colorectal cancer cells. Oncol Res. 2014;22:39–45.

Chambon M, Orsetti B, Berthe ML, et al. Prognostic significance of TRIM24/TIF-1alpha gene expression in breast cancer. Am J Pathol. 2011;178:1461–1469.

Tsai WW, Wang Z, Yiu TT, et al. TRIM24 links a non-canonical histone signature to breast cancer. Nature. 2010;468:927–932.

Li H, Sun L, Tang Z, et al. Overexpression of TRIM24 correlates with tumor progression in non-small cell lung cancer. PLoS One. 2012;7:e37657.

Xue D, Zhang X, Zhang X, et al. Clinical significance and biological roles of TRIM24 in human bladder carcinoma. Tumour Biol. 2015;36:6849–6855.

Miao ZF, Wang ZN, Zhao TT, et al. TRIM24 is upregulated in human gastric cancer and promotes gastric cancer cell growth and chemoresistance. Virchows Archiv. 2015;466:525–532.

Groner AC, Cato L, de Tribolet-Hardy J, et al. TRIM24 is an oncogenic transcriptional activator in prostate cancer. Cancer Cell. 2016;29:846–858.

Offermann A, Roth D, Hupe MC, et al. TRIM24 as an independent prognostic biomarker for prostate cancer. Urol Oncol. 2019;37:576 e1–576 e10.

Schlomm T, Iwers L, Kirstein P, et al. Clinical significance of p53 alterations in surgically treated prostate cancers. Mod Pathol. 2008;21:1371–1378.

Kononen J, Bubendorf L, Kallioniemi A, et al. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med. 1998;4:844–847.

Weischenfeldt J, Simon R, Feuerbach L, et al. Integrative genomic analyses reveal an androgen-driven somatic alteration landscape in early-onset prostate cancer. Cancer Cell. 2013;23:159–170.

Minner S, Enodien M, Sirma H, et al. ERG status is unrelated to PSA recurrence in radically operated prostate cancer in the absence of antihormonal therapy. Clinical cancer research: an official journal of the American Association for. Cancer Res. 2011;17:5878–5888.

Burkhardt L, Fuchs S, Krohn A, et al. CHD1 is a 5q21 tumor suppressor required for ERG rearrangement in prostate cancer. Cancer Res. 2013;73:2795–2805.

Kluth M, Hesse J, Heinl A, et al. Genomic deletion of MAP3K7 at 6q12-22 is associated with early PSA recurrence in prostate cancer and absence of TMPRSS2:ERG fusions. Mod Pathol. 2013;26:975–983.

Krohn A, Diedler T, Burkhardt L, et al. Genomic deletion of PTEN is associated with tumor progression and early PSA recurrence in ERG fusion-positive and fusion-negative prostate cancer. Am J Pathol. 2012;181:401–412.

Krohn A, Seidel A, Burkhardt L, et al. Recurrent deletion of 3p13 targets multiple tumour suppressor genes and defines a distinct subgroup of aggressive ERG fusion-positive prostate cancers. J Pathol. 2013;231:130–141.

Epstein JI, Feng Z, Trock BJ, et al. Upgrading and downgrading of prostate cancer from biopsy to radical prostatectomy: incidence and predictive factors using the modified Gleason grading system and factoring in tertiary grades. Eur Urol. 2012;61:1019–1024.

Cui Z, Cao W, Li J, et al. TRIM24 overexpression is common in locally advanced head and neck squamous cell carcinoma and correlates with aggressive malignant phenotypes. PLoS One. 2013;8:e63887.

McCall P, Witton CJ, Grimsley S, et al. Is PTEN loss associated with clinical outcome measures in human prostate cancer? Br J Cancer. 2008;99:1296–1301.

Sircar K, Yoshimoto M, Monzon FA, et al. PTEN genomic deletion is associated with p-Akt and AR signalling in poorer outcome, hormone refractory prostate cancer. J Pathol. 2009;218:505–513.

Tosoian JJ, Trock BJ, Landis P, et al. Active surveillance program for prostate cancer: an update of the Johns Hopkins experience. J Clin Oncol. 2011;29:2185–2190.

Thompson I, Thrasher JB, Aus G, et al. Guideline for the management of clinically localized prostate cancer: 2007 update. J Urol. 2007;177:2106–2131.

Klotz L, Zhang L, Lam A, et al. Clinical results of long-term follow-up of a large, active surveillance cohort with localized prostate cancer. J Clin Oncol. 2010;28:126–131.

Sauter G, Steurer S, Clauditz TS, et al. Clinical utility of quantitative Gleason Grading in prostate biopsies and prostatectomy specimens. Eur Urol. 2016;69:592–598.

Jain AK, Allton K, Duncan AD, et al. TRIM24 is a p53-induced E3-ubiquitin ligase that undergoes ATM-mediated phosphorylation and autodegradation during DNA damage. Mol Cell Biol. 2014;34:2695–2709.

Liu X, Huang Y, Yang D, et al. Overexpression of TRIM24 is associated with the onset and progress of human hepatocellular carcinoma. PLoS One. 2014;9:e85462.

Appikonda S, Thakkar KN, Barton MC. Regulation of gene expression in human cancers by TRIM24. Drug Discov Today Technol. 2016;19:57–63.

Kikuchi M, Okumura F, Tsukiyama T, et al. TRIM24 mediates ligand-dependent activation of androgen receptor and is repressed by a bromodomain-containing protein, BRD7, in prostate cancer cells. Biochim Biophys Acta. 2009;1793:1828–1836.

vom Baur E, Zechel C, Heery D, et al. Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1. EMBO J. 1996;15:110–124.

Tomlins SA, Rhodes DR, Perner S, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644–648.

Brase JC, Johannes M, Mannsperger H, et al. TMPRSS2-ERG-specific transcriptional modulation is associated with prostate cancer biomarkers and TGF-beta signaling. BMC Cancer. 2011;11:507.

Kim JH, Dhanasekaran SM, Mehra R, et al. Integrative analysis of genomic aberrations associated with prostate cancer progression. Cancer Res. 2007;67:8229–8239.

Sun J, Liu W, Adams TS, et al. DNA copy number alterations in prostate cancers: a combined analysis of published CGH studies. Prostate. 2007;67:692–700.

Taylor BS, Schultz N, Hieronymus H, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell. 2010;18:11–22.

Baliou E, Nonni A, Keramopoulos D, et al. Deregulation of p53-MDM2 auto-regulatory pathway in breast carcinoma. J BUON. 2016;21:1099–1103.

Rayburn E, Zhang R, He J, et al. MDM2 and human malignancies: expression, clinical pathology, prognostic markers, and implications for chemotherapy. Curr Cancer Drug Targets. 2005;5:27–41.

Momand J, Jung D, Wilczynski S, et al. The MDM2 gene amplification database. Nucleic Acids Res. 1998;26:3453–3459.

Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 1997;420:25–27.

Carroll PE, Okuda M, Horn HF, et al. Centrosome hyperamplification in human cancer: chromosome instability induced by p53 mutation and/or Mdm2 overexpression. Oncogene. 1999;18:1935–1944.

Ravindranathan P, Lee TK, Yang L, et al. Peptidomimetic targeting of critical androgen receptor-coregulator interactions in prostate cancer. Nat Commun. 2013;4:1923.

Skaar JR, Pagan JK, Pagano M. SCF ubiquitin ligase-targeted therapies. Nat Rev Drug Discov. 2014;13:889–903.

Sauter G. Representativity of TMA studies. Methods Mol Biol. 2010;664:27–35.