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Direct circMAN1A2(2,3,4,5)-CENPB mRNA interaction regulates cell proliferation and cancer progression

ABSTRACT: Alternative circularization (AC) results in multiple circular transcripts from a single gene locus. Here, we profile the landscape of AC across multiple cell lines and colorectal cancer (CRC) tissues, and identify alternatively-circularized circMAN1A2(2,3,4,5) as a universally and predominantly expressed circular RNA, playing a role in cell proliferation and CRC progression. Mechanistically, circMAN1A2(2,3,4,5) enhances IGF2BP2-mediated Centromere Protein B (CENPB) mRNA stability through a direct interaction with CENPB mRNA via its characteristic back-splicing junction site. Both shRNAs and locked nucleic acids specifically targeting circMAN1A2(2,3,4,5) inhibit CRC progression, suggesting a potential therapeutic target for CRC treatment.

ORGANISM(S): Homo Sapiens

SUBMITTER: Yang Li

PROVIDER: PXD057478 | iProX | Fri Nov 01 00:00:00 GMT 2024

REPOSITORIES: iProX

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Direct circMAN1A2(2,3,4,5)-CENPB mRNA interaction regulates cell proliferation and cancer progression

Project description:A large number of covalently closed circular RNAs (circRNAs), produced from back-splicing of eukaryotic exons, have been identified among different cell lines/tissues. Interestingly, multiple circRNAs could be produced from a single gene locus through alternative circularization (AC), expanding the complexity and diversity of circRNAs. However, functions of most AC circRNAs remains poorly understood. Here, we profiled the landscape of AC across multiple cell lines and colorectal cancer (CRC) tissues, identifying predominantly expressed circRNAs (pe-circRNA) in each AC gene loci. While the expression of top pe-circRNAs exhibits a cell-type-specific manner, circMAN1A2(2,3,4,5), a pe-circRNA that is universally expressed in examined cells and CRC samples, was shown to play an important role in cell proliferation and CRC progression. Mechanistically, circMAN1A2(2,3,4,5) directly interacted with the 3' untranslated region of Centromere Protein B (CENPB) mRNA via its characteristic back-splicing junction site, which enhanced IGF2BP2-mediated CENPB mRNA stability. Inhibition of circMAN1A2(2,3,4,5) expression with specific shRNAs and locked nucleic acids (LNAs) resulted in repressed cell proliferation and tumor progression in the subcutaneous mouse CRC model. These results together uncover the prevalence of AC and the regulatory role of a specific AC circRNA, circMAN1A2(2,3,4,5), in cell proliferation and tumor progression.

2025-07-27 | GSE274247 | GEO

circRNAs microarray analysis in colorectal caner tissues

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Resident Macrophages are Locally Programmed for Silent Clearance of Apoptotic Cells

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CircNCOR1 suppresses lymphatic metastasis in bladder cancer

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Next Generation Sequencing Quantitative Analysis of altered expression of genes in circNCOR1 overexpressing bladder cancer cells

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Project description:Circular RNAs (circRNAs) represent critical roles in the biology of various cancers. However, their expression patterns and biological functions in human colorectal cancer (CRC) remain largely unknown. The aim of this study was to explore circRNAs profiles in CRC and investigate key circRNAs involved in CRC tumourigenesis and progression.

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2018-03-23 | MSV000082206 | MassIVE

CircHIPK3 and FMRP compete for direct binding to BRCA1 mRNA controlling its protein levels and DNA damage response [miRNA_pulldown]

Project description:Circular RNAs (circRNAs) are covalently closed RNA molecules widely expressed in eukaryotes and regulated in several pathological processes, including cancer. Many studies point to their mechanism of action as miRNA and protein sponges; however, we propose a new functionality based on circRNA-mRNA interaction to regulate mRNA fate. We show that the widely expressed circHIPK3 directly interacts in vivo with the BRCA1 mRNA through the back-splicing region. This interaction favoured the translation of BRCA1 by competing for the binding of the FMRP1 RNA-binding protein, which acts as a repressor of BRCA1 translation. CircHIPK3 depletion or disruption of the CircRNA-mRNA interaction decreased BRCA1 levels and increased DNA damage, sensitizing several cancer cell lines to DNA-damage-inducing agents and rendering them susceptible to synthetic lethality. Additionally, mimicking circHIPK3 interaction with lock-nucleic acid (LNA) oligonucleotides restores BRCA1 levels in hereditary breast cancer model cells, underscoring circRNA-mRNA interaction’s importance in regulating cell homeostasis and drug response.

2024-09-13 | GSE246225 | GEO

CircHIPK3 and FMRP compete for direct binding to BRCA1 mRNA controlling its protein levels and DNA damage response [RNA_pulldown]

2024-09-13 | GSE246224 | GEO

Back-spliced RNA from Retrotransposon Binds to Centromere and Regulates Centromeric Chromatin Loops in Maize

Project description:In most plants, centromeric DNA contains highly repetitive sequences, including tandem repeats and retrotransposons; however, the roles of these sequences in the structure and function of the centromere are unclear. Here, we found that retrotransposon-derived back-spliced RNA can bind to the centromere through R-loops and regulate the formation of centromeric chromatin loops. Multiple RNA sequences from centromeric retrotransposons (CRMs) were enriched in maize (Zea mays) centromeres and back spliced RNA from CRM1 were detected. We identified three types of circular CRM1 RNAs with the same back-splicing site based on the back-spliced sequences. These circular RNAs bound to the centromere through R-loops. Two R-loop sites inside a single circular RNA promoted the formation of chromatin loops in CRM1 regions. When RNAi was used to target the back-spliced site of the circular CRM1 RNAs, the levels of R-loops and chromatin loops formed by these circular RNAs decreased, while the levels of R-loops produced by linear RNAs with similar binding sites increased. Linear RNAs with only one R-loop site could not promote chromatin loop formation. Higher levels of R-loops and lower levels of chromatin loops in the CRM1 regions of RNAi plants led to a reduced localization of the centromeric H3 variant (CENH3). Our work reveals that centromeric chromatin organization by circular CRM1 RNAs via R-loops and chromatin loops. R-loops are integral components of centromeric chromatin. Proper centromere structure is essential for CENH3 localization. CRM1 elements may have helped to build a suitable chromatin environment during centromere evolution.

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