The molecular conversations of sarcomas: exosomal non-coding RNAs in tumor’s biology and their translational prospects

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Abstract

Exosomes mediate cell-to-cell crosstalk involving a variety of biomolecules through an intricate signaling network. In recent years, the pivotal role of exosomes and their non-coding RNAs cargo in the development and progression of several cancer types clearly emerged. In particular, tumor bulk and its microenvironment co-evolve through cellular communications where these nanosized extracellular vesicles are among the most relevant actors. Knowledge about the cellular, and molecular mechanisms involved in these communications will pave the way for novel exosome-based delivery of therapeutic RNAs as well as innovative prognostic/diagnostic tools. Despite the valuable therapeutic potential and clinical relevance of exosomes, their role on sarcoma has been vaguely reported because the rarity and high heterogeneity of this type of cancer. Here, we dissected the scientific literature to unravel the multifaceted role of exosomal non-coding RNAs as mediator of cell-to-cell communications in the sarcoma subtypes.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12943-024-02083-y.

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Extracellular vesicles: Exosomes, microvesicles, and friends

Graça Raposo, Willem Stoorvogel (2013)

Cells release into the extracellular environment diverse types of membrane vesicles of endosomal and plasma membrane origin called exosomes and microvesicles, respectively. These extracellular vesicles (EVs) represent an important mode of intercellular communication by serving as vehicles for transfer between cells of membrane and cytosolic proteins, lipids, and RNA. Deficiencies in our knowledge of the molecular mechanisms for EV formation and lack of methods to interfere with the packaging of cargo or with vesicle release, however, still hamper identification of their physiological relevance in vivo. In this review, we focus on the characterization of EVs and on currently proposed mechanisms for their formation, targeting, and function.

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The biogenesis, biology and characterization of circular RNAs

Lasse S. Kristensen, Maria Andersen, Lotte V. W. Stagsted … (2019)

Circular RNAs (circRNAs) are covalently closed, endogenous biomolecules in eukaryotes with tissue-specific and cell-specific expression patterns, whose biogenesis is regulated by specific cis-acting elements and trans-acting factors. Some circRNAs are abundant and evolutionarily conserved, and many circRNAs exert important biological functions by acting as microRNA or protein inhibitors ('sponges'), by regulating protein function or by being translated themselves. Furthermore, circRNAs have been implicated in diseases such as diabetes mellitus, neurological disorders, cardiovascular diseases and cancer. Although the circular nature of these transcripts makes their detection, quantification and functional characterization challenging, recent advances in high-throughput RNA sequencing and circRNA-specific computational tools have driven the development of state-of-the-art approaches for their identification, and novel approaches to functional characterization are emerging.

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Circular RNAs are abundant, conserved, and associated with ALU repeats.

W. R. Jeck, J A Sorrentino, K. Wang … (2013)

Circular RNAs composed of exonic sequence have been described in a small number of genes. Thought to result from splicing errors, circular RNA species possess no known function. To delineate the universe of endogenous circular RNAs, we performed high-throughput sequencing (RNA-seq) of libraries prepared from ribosome-depleted RNA with or without digestion with the RNA exonuclease, RNase R. We identified >25,000 distinct RNA species in human fibroblasts that contained non-colinear exons (a "backsplice") and were reproducibly enriched by exonuclease degradation of linear RNA. These RNAs were validated as circular RNA (ecircRNA), rather than linear RNA, and were more stable than associated linear mRNAs in vivo. In some cases, the abundance of circular molecules exceeded that of associated linear mRNA by >10-fold. By conservative estimate, we identified ecircRNAs from 14.4% of actively transcribed genes in human fibroblasts. Application of this method to murine testis RNA identified 69 ecircRNAs in precisely orthologous locations to human circular RNAs. Of note, paralogous kinases HIPK2 and HIPK3 produce abundant ecircRNA from their second exon in both humans and mice. Though HIPK3 circular RNAs contain an AUG translation start, it and other ecircRNAs were not bound to ribosomes. Circular RNAs could be degraded by siRNAs and, therefore, may act as competing endogenous RNAs. Bioinformatic analysis revealed shared features of circularized exons, including long bordering introns that contained complementary ALU repeats. These data show that ecircRNAs are abundant, stable, conserved and nonrandom products of RNA splicing that could be involved in control of gene expression.

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Author and article information

Contributors

Sabino Russi: sabino.russi@crob.it

Journal

Journal ID (nlm-ta): Mol Cancer

Journal ID (iso-abbrev): Mol Cancer

Title: Molecular Cancer

Publisher: BioMed Central (London )

ISSN (Electronic): 1476-4598

Publication date (Electronic): 22 August 2024

Publication date PMC-release: 22 August 2024

Publication date Collection: 2024

Volume: 23

Electronic Location Identifier: 172

Affiliations

[1 ]Laboratory of Preclinical and Translational Research, IRCCS CROB Centro di Riferimento Oncologico della Basilicata, ( https://ror.org/00n6jcj93) Rionero in Vulture (PZ), 85028 Italy

[2 ]Experimental Oncology Unit, IRCCS CROB Centro di Riferimento Oncologico della Basilicata, ( https://ror.org/00n6jcj93) Rionero in Vulture (PZ), 85028 Italy

[3 ]Department of Biology, University of Naples Federico II, ( https://ror.org/05290cv24) Naples, 80126 Italy

[4 ]AORN San Giuseppe Moscati, Avellino (AV), 83100 Italy

Article

Publisher ID: 2083

DOI: 10.1186/s12943-024-02083-y

PMC ID: 11340101

PubMed ID: 39174949

SO-VID: 53792d0d-f620-4f4b-a3d1-8a41d8898897

License:

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

History

Date received : 4 July 2024

Date accepted : 13 August 2024

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003196, Ministero della Salute;

Award ID: Ricerca Corrente 2024

Custom metadata

ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: sarcomas,exosomes,non-coding rnas,tumor microenvironment,micrornas,circrna,lncrnas

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: sarcomas, exosomes, non-coding rnas, tumor microenvironment, micrornas, circrna, lncrnas

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The molecular conversations of sarcomas: exosomal non-coding RNAs in tumor’s biology and their translational prospects

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Supplementary Information

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Journal of Circulating Biomarkers

Most cited references 157

Extracellular vesicles: Exosomes, microvesicles, and friends

The biogenesis, biology and characterization of circular RNAs

Circular RNAs are abundant, conserved, and associated with ALU repeats.

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