دورية أكاديمية
The correlation between TRIM28 expression and immune checkpoints in CRPC.
| العنوان: | The correlation between TRIM28 expression and immune checkpoints in CRPC. |
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| المؤلفون: | Xue D; Department of Medical, the First Hospital of Changsha, Changsha, P. R. China., Zuo Q; Department of Radiology, the First Hospital of Changsha, Changsha, P. R. China., Chang J; Department of Outpatient, the First Hospital of Changsha, Changsha, P. R. China., Wu X; Department of Urology, the First Hospital of Changsha, Changsha, P. R. China. |
| المصدر: | FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2024 Jul 15; Vol. 38 (13), pp. e23663. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Federation of American Societies for Experimental Biology Country of Publication: United States NLM ID: 8804484 Publication Model: Print Cited Medium: Internet ISSN: 1530-6860 (Electronic) Linking ISSN: 08926638 NLM ISO Abbreviation: FASEB J Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley Original Publication: [Bethesda, Md.] : The Federation, [c1987- |
| مواضيع طبية MeSH: | CD8-Positive T-Lymphocytes*/immunology , CD8-Positive T-Lymphocytes*/metabolism , Membrane Proteins*/genetics , Membrane Proteins*/metabolism , Prostatic Neoplasms, Castration-Resistant*/genetics , Prostatic Neoplasms, Castration-Resistant*/metabolism , Prostatic Neoplasms, Castration-Resistant*/immunology , Prostatic Neoplasms, Castration-Resistant*/pathology , Tripartite Motif-Containing Protein 28*/metabolism , Tripartite Motif-Containing Protein 28*/genetics, Animals ; Humans ; Male ; Mice ; Cell Line, Tumor ; Gene Expression Regulation, Neoplastic ; Macrophages/metabolism ; Macrophages/immunology ; Mice, Inbred C57BL ; Mice, Knockout ; Nucleotidyltransferases/metabolism ; Nucleotidyltransferases/genetics ; Signal Transduction |
| مستخلص: | This study delves into the unexplored realm of castration-resistant prostate cancer (CRPC) by investigating the role of TRIM28 and its intricate molecular mechanisms using high-throughput single-cell transcriptome sequencing and advanced bioinformatics analysis. Our comprehensive examination unveiled dynamic TRIM28 expression changes, particularly in immune cells such as macrophages and CD8+ T cells within CRPC. Correlation analyses with TCGA data highlighted the connection between TRIM28 and immune checkpoint expression and emphasized its pivotal influence on the quantity and functionality of immune cells. Using TRIM28 knockout mouse models, we identified differentially expressed genes and enriched pathways, unraveling the potential regulatory involvement of TRIM28 in the cGAS-STING pathway. In vitro, experiments further illuminated that TRIM28 knockout in prostate cancer cells induced a notable anti-tumor immune effect by inhibiting M2 macrophage polarization and enhancing CD8+ T cell activity. This impactful discovery was validated in an in situ transplant tumor model, where TRIM28 knockout exhibited a deceleration in tumor growth, reduced proportions of M2 macrophages, and enhanced infiltration of CD8+ T cells. In summary, this study elucidates the hitherto unknown anti-tumor immune role of TRIM28 in CRPC and unravels its potential regulatory mechanism via the cGAS-STING signaling pathway. These findings provide novel insights into the immune landscape of CRPC, offering promising directions for developing innovative therapeutic strategies. (© 2024 Federation of American Societies for Experimental Biology.) |
| References: | Ge R, Wang Z, Montironi R, et al. Epigenetic modulations and lineage plasticity in advanced prostate cancer. Ann Oncol. 2020;31(4):470‐479. doi:10.1016/j.annonc.2020.02.002. Dong Y, Sun X, Zhang K, et al. Type IIA topoisomerase (TOP2A) triggers epithelial‐mesenchymal transition and facilitates HCC progression by regulating snail expression. Bioengineered. 2021;12(2):12967‐12979. doi:10.1080/21655979.2021.2012069. Chen X, Chen F, Ren Y, et al. Glucocorticoid receptor upregulation increases radioresistance and triggers androgen independence of prostate cancer [published correction appears in prostate. 2020 Jun;80(9):727]. Prostate. 2019;79(12):1386‐1398. doi:10.1002/pros.23861. Cui Y, Wang H, Wang D, et al. Network pharmacology analysis on the mechanism of Huangqi Sijunzi decoction in treating cancer‐related fatigue [retracted in: J Healthc Eng. 2023 Oct 11;2023:9895186]. J Healthc Eng. 2021;2021:9780677. doi:10.1155/2021/9780677. Li X, Ma S, Deng Y, Yi P, Yu J. Targeting the RNA m6A modification for cancer immunotherapy. Mol Cancer. 2022;21(1):76. doi:10.1186/s12943-022-01558-0. Liu X, Hartman CL, Li L, et al. Reprogramming lipid metabolism prevents effector T cell senescence and enhances tumor immunotherapy. Sci Transl Med. 2021;13(587):eaaz6314. doi:10.1126/scitranslmed.aaz6314. Habanjar O, Bingula R, Decombat C, Diab‐Assaf M, Caldefie‐Chezet F, Delort L. Crosstalk of inflammatory cytokines within the breast tumor microenvironment. Int J Mol Sci. 2023;24(4):4002. doi:10.3390/ijms24044002. Carlino MS, Larkin J, Long GV. Immune checkpoint inhibitors in melanoma. Lancet. 2021;398(10304):1002‐1014. doi:10.1016/S0140-6736(21)01206-X. Mao X, Xu J, Wang W, et al. Crosstalk between cancer‐associated fibroblasts and immune cells in the tumor microenvironment: new findings and future perspectives. Mol Cancer. 2021;20(1):131. doi:10.1186/s12943-021-01428-1. Kumar J, Kaur G, Ren R, et al. KRAB domain of ZFP568 disrupts TRIM28‐mediated abnormal interactions in cancer cells. NAR Cancer. 2020;2(2):zcaa007. doi:10.1093/narcan/zcaa007. Yang Y, Tan S, Han Y, et al. The role of tripartite motif‐containing 28 in cancer progression and its therapeutic potentials. Front Oncol. 2023;13:1100134. doi:10.3389/fonc.2023.1100134. Kim YS, Potashnikova DM, Gisina AM, et al. TRIM28 is a novel regulator of CD133 expression associated with cancer stem cell phenotype. Int J Mol Sci. 2022;23(17):9874. doi:10.3390/ijms23179874. Czerwinska P, Jaworska AM, Wlodarczyk NA, Mackiewicz AA. Melanoma stem cell‐like phenotype and significant suppression of immune response within a tumor are regulated by TRIM28 protein. Cancers (Basel). 2020;12(10):2998. doi:10.3390/cancers12102998. Huang Z, Li X, Tang B, et al. SETDB1 modulates degradation of phosphorylated RB and anticancer efficacy of CDK4/6 inhibitors. Cancer Res. 2023;83(6):875‐889. doi:10.1158/0008-5472.CAN-22-0264. Park HH, Kim HR, Park SY, et al. RIPK3 activation induces TRIM28 derepression in cancer cells and enhances the anti‐tumor microenvironment. Mol Cancer. 2021;20(1):107. doi:10.1186/s12943-021-01399-3. Butler A, Hoffman P, Smibert P, Papalexi E, Satija R. Integrating single‐cell transcriptomic data across different conditions, technologies, and species. Nat Biotechnol. 2018;36(5):411‐420. doi:10.1038/nbt.4096. Trapnell C, Cacchiarelli D, Grimsby J, et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol. 2014;32(4):381‐386. doi:10.1038/nbt.2859. Li D, Zhou X, Xu W, et al. Prostate cancer cells synergistically defend against CD8+ T cells by secreting exosomal PD‐L1. Cancer Med. 2023;12(15):16405‐16415. doi:10.1002/cam4.6275. Bi R, Yang Y, Liao H, et al. Porphyromonas gingivalis induces an inflammatory response via the cGAS‐STING signaling pathway in a periodontitis mouse model. Front Microbiol. 2023;14:1183415. doi:10.3389/fmicb.2023.1183415. Fan D, Yang Y, Zhang W. A novel circ_MACF1/miR‐942‐5p/TGFBR2 axis regulates the functional behaviors and drug sensitivity in gefitinib‐resistant non‐small cell lung cancer cells. BMC Pulm Med. 2022;22(1):27. doi:10.1186/s12890-021-01731-z. Hong Z, Mei J, Li C, et al. STING inhibitors target the cyclic dinucleotide binding pocket. Proc Natl Acad Sci USA. 2021;118(24):e2105465118. doi:10.1073/pnas.2105465118. Daunke T, Beckinger S, Rahn S, et al. Expression and role of the immune checkpoint regulator PD‐L1 in the tumor‐stroma interplay of pancreatic ductal adenocarcinoma. Front Immunol. 2023;14:1157397. doi:10.3389/fimmu.2023.1157397. Niu R, Li D, Chen J, Zhao W. Circ_0014235 confers gefitinib resistance and malignant behaviors in non‐small cell lung cancer resistant to gefitinib by governing the miR‐146b‐5p/YAP/PD‐L1 pathway. Cell Cycle. 2022;21(1):86‐100. doi:10.1080/15384101.2021.2009986. He X, Chen H, Zhong X, et al. BST2 induced macrophage M2 polarization to promote the progression of colorectal cancer. Int J Biol Sci. 2023;19(1):331‐345. doi:10.7150/ijbs.72538. Liu J, Jiang J, Hui X, Wang W, Fang D, Ding L. Mir‐758‐5p suppresses glioblastoma proliferation, migration and invasion by targeting ZBTB20. Cell Physiol Biochem. 2018;48(5):2074‐2083. doi:10.1159/000492545. Fan L, Peng G, Hussain A, et al. The steroidogenic enzyme AKR1C3 regulates stability of the ubiquitin ligase Siah2 in prostate cancer cells. J Biol Chem. 2015;290(34):20865‐20879. doi:10.1074/jbc.M115.662155. Lin TH, Lee SO, Niu Y, et al. Differential androgen deprivation therapies with anti‐androgens casodex/bicalutamide or MDV3100/enzalutamide versus anti‐androgen receptor ASC‐J9(R) lead to promotion versus suppression of prostate cancer metastasis [published correction appears in J Biol Chem. 2020 Nov 13;295(46):15796]. J Biol Chem. 2013;288(27):19359‐19369. doi:10.1074/jbc.M113.477216. Shen Y, Ni S, Li S, Lv B. Role of stemness‐related genes TIMP1, PGF, and SNAI1 in the prognosis of colorectal cancer through single‐cell RNA‐seq. Cancer Med. 2023;12(10):11611‐11623. doi:10.1002/cam4.5833. Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16(5):284‐287. doi:10.1089/omi.2011.0118. Li CW, Lim SO, Xia W, et al. Glycosylation and stabilization of programmed death ligand‐1 suppresses T‐cell activity. Nat Commun. 2016;7:12632. doi:10.1038/ncomms12632. Zhou X, Zou L, Liao H, et al. Abrogation of HnRNP L enhances anti‐PD‐1 therapy efficacy via diminishing PD‐L1 and promoting CD8+ T cell‐mediated ferroptosis in castration‐resistant prostate cancer. Acta Pharm Sin B. 2022;12(2):692‐707. doi:10.1016/j.apsb.2021.07.016. Wang G, Zhao D, Spring DJ, DePinho RA. Genetics and biology of prostate cancer. Genes Dev. 2018;32(17–18):1105‐1140. doi:10.1101/gad.315739.118. Czerwińska P, Mazurek S, Wiznerowicz M. The complexity of TRIM28 contribution to cancer. J Biomed Sci. 2017;24(1):63. doi:10.1186/s12929-017-0374-4. Achard V, Putora PM, Omlin A, Zilli T, Fischer S. Metastatic prostate cancer: treatment options. Oncology. 2022;100(1):48‐59. doi:10.1159/000519861. Munari E, Mariotti FR, Quatrini L, et al. PD‐1/PD‐L1 in cancer: pathophysiological, diagnostic and therapeutic aspects. Int J Mol Sci. 2021;22(10):5123. doi:10.3390/ijms22105123. Ye Z, Bing A, Zhao S, Yi S, Zhan X. Comprehensive analysis of spliceosome genes and their mutants across 27 cancer types in 9070 patients: clinically relevant outcomes in the context of 3P medicine. EPMA J. 2022;13(2):335‐350. doi:10.1007/s13167-022-00279-0. Chen K, Wang Q, Li M, et al. Single‐cell RNA‐seq reveals dynamic change in tumor microenvironment during pancreatic ductal adenocarcinoma malignant progression. EBioMedicine. 2021;66:103315. doi:10.1016/j.ebiom.2021.103315. Shorning BY, Dass MS, Smalley MJ, Pearson HB. The PI3K‐AKT‐mTOR pathway and prostate cancer: at the crossroads of AR, MAPK, and WNT signaling. Int J Mol Sci. 2020;21(12):4507. doi:10.3390/ijms21124507. Chen S, Zhu G, Yang Y, et al. Single‐cell analysis reveals transcriptomic remodellings in distinct cell types that contribute to human prostate cancer progression. Nat Cell Biol. 2021;23(1):87‐98. doi:10.1038/s41556-020-00613-6. Geis FK, Goff SP. Silencing and transcriptional regulation of endogenous retroviruses: an overview. Viruses. 2020;12(8):884. doi:10.3390/v12080884. Lin J, Guo D, Liu H, et al. The SETDB1‐TRIM28 complex suppresses antitumor immunity. Cancer Immunol Res. 2021;9(12):1413‐1424. doi:10.1158/2326-6066.CIR-21-0754. Cao J, Su B, Peng R, et al. Bioinformatics analysis of immune infiltrates and tripartite motif (TRIM) family genes in hepatocellular carcinoma. J Gastrointest Oncol. 2022;13(4):1942‐1958. doi:10.21037/jgo-22-619. Lu HP, Lin CJ, Chen WC, et al. TRIM28 regulates Dlk1 expression in adipogenesis. Int J Mol Sci. 2020;21(19):7245. doi:10.3390/ijms21197245. Herrington CS, Poulsom R, Koeppen H, Coates PJ. Recent advances in pathology: the 2021 annual review issue of the journal of pathology. J Pathol. 2021;254(4):303‐306. doi:10.1002/path.5687. Decout A, Katz JD, Venkatraman S, Ablasser A. The cGAS‐STING pathway as a therapeutic target in inflammatory diseases. Nat Rev Immunol. 2021;21(9):548‐569. doi:10.1038/s41577-021-00524-z. Tai F, Wang C, Deng X, et al. Treadmill exercise ameliorates chronic REM sleep deprivation‐induced anxiety‐like behavior and cognitive impairment in C57BL/6J mice. Brain Res Bull. 2020;164:198‐207. doi:10.1016/j.brainresbull.2020.08.025. |
| فهرسة مساهمة: | Keywords: TRIM28; anti‐tumor immunity; cGAS‐STING pathway; castration‐resistant prostate cancer; immune checkpoint; single‐cell transcriptome sequencing |
| المشرفين على المادة: | EC 2.7.7.- (cGAS protein, human) 0 (Membrane Proteins) EC 2.7.7.- (Nucleotidyltransferases) EC 2.3.2.27 (TRIM28 protein, human) EC 2.3.2.27 (Trim28 protein, mouse) EC 2.3.2.27 (Tripartite Motif-Containing Protein 28) |
| تواريخ الأحداث: | Date Created: 20240703 Date Completed: 20240703 Latest Revision: 20240729 |
| رمز التحديث: | 20240729 |
| DOI: | 10.1096/fj.202400061RR |
| PMID: | 38958986 |
| قاعدة البيانات: | MEDLINE |
| تدمد: | 1530-6860 |
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| DOI: | 10.1096/fj.202400061RR |