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| Coordinated AR and microRNA regulation in prostate cancer |
Ieva Eringyte,Joanna N. Zamarbide Losada,Sue M. Powell,Charlotte L. Bevan,Claire E. Fletcher( )
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| Imperial Centre for Translational and Experimental Medicine, Department of Surgery and Cancer, Imperial College London, Hammersmith Hospital, London, United Kingdom |
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Abstract The androgen receptor (AR) remains a key driver of prostate cancer (PCa) progression, even in the advanced castrate-resistant stage, where testicular androgens are absent. It is therefore of critical importance to understand the molecular mechanisms governing its activity and regulation during prostate tumourigenesis. MicroRNAs (miRs) are small ~22 nt non-coding RNAs that regulate target gene, often through association with 3′ untranslated regions (3′UTRs) of transcripts. They display dysregulation during cancer progression, can function as oncogenes or tumour suppressors, and are increasingly recognised as targets or regulators of hormonal action. Thus, understanding factors which modulate miRs synthesis is essential. There is increasing evidence for complex and dynamic bi-directional cross-talk between the multi-step miR biogenesis cascade and the AR signalling axis in PCa. This review summarises the wealth of mechanisms by which miRs are regulated by AR, and conversely, how miRs impact AR's transcriptional activity, including that of AR splice variants. In addition, we assess the implications of the convergence of these pathways on the clinical employment of miRs as PCa biomarkers and therapeutic targets.
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Received: 11 August 2019
Available online: 20 July 2020
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Corresponding Authors:
Claire E. Fletcher
E-mail: Claire.fletcher07@imperial.ac.uk
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Direct and indirect mechanisms of microRNA (miR)-regulation of androgen receptor (AR) activity. (A) AR transcription—miRs modulate expression of AR by targeting AR transcription factors and regulatory proteins. Let-7c indirectly represses AR activity by targeting c-Myc, which acts as a transcription factor for the AR gene [65,66]; (B) AR mRNA—miRs target AR directly through binding to microRNA response elements in its transcript. Most microRNAs target the 3′UTR [4,24,31,[38], [39], [40], [41], [42], [43],45,46], but interactions with the coding region and 5′UTR have also been reported [4,56]; (C) AR-mediated transcription of target genes—miRs modulate AR indirectly by targeting cofactors, regulators or effectors of AR activity [19,63,64]; (D) AR competitive endogenous RNAs (ceRNAs) —AR is regulated by ceRNAs containing microRNA response elements (MREs) for AR-targeting miRs. For example, PlncRNA-1 protects AR from miR-mediated repression. A direct transcriptional target of AR, this lncRNA contains some of the same miR binding sites as AR, allowing it to sequester two AR-targeting miRs: miR-34c and miR-297. These in turn directly suppress PlncRNA-1, creating a feedback loop of AR regulation [87].
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| Target | miR | Binding location | Identifying experiments | Effects on AR | References | | AR-V7 | 181c-5p | 3′UTR | Expression of AR mRNA & protein/AR-V7 3′UTR
luciferase reporter assay | miR-181c-5p overexpression represses AR-V7 activity, transcript & protein expression. | [23] | | AR-V7/WT AR | 101-3p | 3′UTR | Expression of AR protein/3′UTR luciferase reporter assay (WT AR only) | miR-101-3p overexpression represses AR-V7 protein expression. | [24] | | ARV4,V7/WT AR | 124-3p | 3′UTR | Expression of AR protein/3′UTR luciferase reporter assay | miR-124-3p overexpression represses AR-V7 activity, transcript & protein expression. | [22,100] | | AR-V7/WT AR | 135b | 3′UTR | Expression of AR protein/3′UTR luciferase reporter assay | miR-135b overexpression represses AR-V7 protein expression. | [38] | | AR-V7/WT AR | 488 | 3′UTR | Expression of AR mRNA & protein/3′UTR luciferase reporter assay | miR-488 overexpression represses AR-V7 transcript & protein expression. | [24,38] | | AR-V7, V567es/WT AR | 346 | 3′UTR | Expression of AR protein/proliferation assays | miR-346 inhibition reduces AR expression and PCa proliferation. | [40] | | AR-V7, V567es/WT AR | 361-3p | 3′UTR | Expression of AR protein/proliferation assays | miR-361-3p inhibition reduces AR expression and PCa proliferation. | [40] | | AR-V7/WT AR | 193a-3p | CDS | Expression of AR protein/PSE-PBN luciferase reporter assay | miR-193a-3p overexpression represses AR-V7/WT AR activity & protein expression. | [24] | | AR-V7/WT AR | 371-3p | CDS | Expression of AR protein/PSE-PBN luciferase reporter assay | miR-371-3p overexpression represses AR-V7/WT AR activity & protein expression. | [24] | | AR-V7/WT AR | 646 | CDS | Expression of AR protein/PSE-PBN luciferase reporter assay | miR-646 overexpression represses AR-V7/WT AR activity & protein expression. | [24] |
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Reported miRs targeting variant AR in prostate cancer.
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Androgen receptor (AR) regulates microRNA (miR) biogenesis at different stages. 1) AR binds to androgen receptor elements (ARE) at promotor regions of miR genes or miR host genes to increase miR expression (e.g. miR-21, miR-29a, miR-29b, miR-22 or miR-14), or to repress it (e.g. miR-17a, miR-20a, miR-222/-221 and miR-31) [56,[103], [104], [105]]. 2) AR associates with lysine-specific demethylase 1 (KDM1A) to remove repressive methyl marks from AR-target miR genes to enhance transcription of miR-27a, miR-133b and miR-19a through post-translational modifications mediated by KDM1A at miR gene promotors [114]. 3) AR has been linked to altered methylation of miR-22 and miR-29a through an unknown mechanism [102]. 4) AR increases Drosha-mediated pri-miR processing of the miR-23a27a24-2 cluster to promote miR maturation [36]. 5) AR upregulates protein levels of the Drosha accessory factor, DGCR8 [35]. 6) Dicer, the enzyme responsible for generation of miR:miR? duplexes from pre-miRs, is transcriptionally-upregulated by androgen signaling [35].
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