Evaluation of Exosomal Coding and Non-Coding RNA Signature in Obese Adolescents

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2023 Jan 8

PMID 36613584

Authors

Manuela Cabiati

Emioli Randazzo

Letizia Guiducci

Alessandra Falleni

Antonella Cecchettini

Valentina Casieri

Giovanni Federico

Silvia Del Ry

Affiliations

Soon will be listed here.

Abstract

Exosomes may contribute to the pathogenesis of obesity through their action as communication mediators. As we have previously demonstrated, in obese adolescents, some circulating miRNAs modified the C-type natriuretic peptide (CNP) expression and were associated with changes in metabolic functions. At present no data are available on miRNA transport by exosomes in this condition. To verify and compare the presence and the expression of CNP/NPR-B/NPR-C, and some miRNAs (miR-33a-3p/miR-223-5p/miR-142-5p/miRNA-4454/miRNA-181a-5p/miRNA-199-5p), in circulating exosomes obtained from the same cohort of obese (O, n = 22) and normal-weight adolescents (N, n = 22). For the first time, we observed that exosomes carried CNP and its specific receptors only randomly both in O and N, suggesting that exosomes are not important carriers for the CNP system. On the contrary, exosomal miRNAs resulted ubiquitously and differentially expressed in O and N. O showed a significant decrease (p < 0.01) in the expression of all miRNAs except for miR-4454 and miR-142-5p. We have found significant correlations among miRNAs themselves and with some inflammatory/metabolic factors of obesity. These relationships may help in finding new biomarkers, allowing us to recognize, at an early stage, obese children and adolescents at high risk to develop the disease complications in adult life.

Citing Articles

RNA Therapies in Cardio-Kidney-Metabolic Syndrome: Advancing Disease Management.

Mohammadi A, Karimian A, Shokri K, Mohammadi A, Hazhir-Karzar N, Bahar R J Cardiovasc Transl Res. 2025; .

PMID: 40080261 DOI: 10.1007/s12265-025-10603-4.

Modulation of MicroRNAs and Exosomal MicroRNAs after Dietary Interventions for Obesity and Insulin Resistance: A Narrative Review.

Hernandez-Gomez K, Avila-Nava A, Gonzalez-Salazar L, Noriega L, Serralde-Zuniga A, Guizar-Heredia R Metabolites. 2023; 13(12).

PMID: 38132872 PMC: 10745452. DOI: 10.3390/metabo13121190.

The Regulatory Role of MicroRNAs in Obesity and Obesity-Derived Ailments.

Benavides-Aguilar J, Torres-Copado A, Isidoro-Sanchez J, Pathak S, Duttaroy A, Banerjee A Genes (Basel). 2023; 14(11).

PMID: 38003013 PMC: 10671661. DOI: 10.3390/genes14112070.

Circulating and Exosomal microRNA-33 in Childhood Obesity.

Cabiati M, Guiducci L, Randazzo E, Casieri V, Federico G, Del Ry S Biomedicines. 2023; 11(8).

PMID: 37626791 PMC: 10452681. DOI: 10.3390/biomedicines11082295.

Editorial: The role of exosomes and organokines in metabolic and endocrine disease.

Wang Q, Liao Z, Lai J, Xiao X Front Endocrinol (Lausanne). 2023; 14:1198791.

PMID: 37152957 PMC: 10162493. DOI: 10.3389/fendo.2023.1198791.

References

Cole T, Green P . Smoothing reference centile curves: the LMS method and penalized likelihood. Stat Med. 1992; 11(10):1305-19. DOI: 10.1002/sim.4780111005. View

Oliveira-Rodriguez M, Serrano-Pertierra E, Costa Garcia A, Lopez-Martin S, Yanez-Mo M, Cernuda-Morollon E . Point-of-care detection of extracellular vesicles: Sensitivity optimization and multiple-target detection. Biosens Bioelectron. 2016; 87:38-45. DOI: 10.1016/j.bios.2016.08.001. View

DAnnunzio G, Vanelli M, Pistorio A, Minuto N, Bergamino L, Iafusco D . Insulin resistance and secretion indexes in healthy Italian children and adolescents: a multicentre study. Acta Biomed. 2009; 80(1):21-8. View

Doyle L, Wang M . Overview of Extracellular Vesicles, Their Origin, Composition, Purpose, and Methods for Exosome Isolation and Analysis. Cells. 2019; 8(7). PMC: 6678302. DOI: 10.3390/cells8070727. View

Bartel D . MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136(2):215-33. PMC: 3794896. DOI: 10.1016/j.cell.2009.01.002. View

Johnnidis J, Harris M, Wheeler R, Stehling-Sun S, Lam M, Kirak O . Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature. 2008; 451(7182):1125-9. DOI: 10.1038/nature06607. View

Vickers K, Landstreet S, Levin M, Shoucri B, Toth C, Taylor R . MicroRNA-223 coordinates cholesterol homeostasis. Proc Natl Acad Sci U S A. 2014; 111(40):14518-23. PMC: 4210029. DOI: 10.1073/pnas.1215767111. View

Maligianni I, Yapijakis C, Bacopoulou F, Chrousos G . The Potential Role of Exosomes in Child and Adolescent Obesity. Children (Basel). 2021; 8(3). PMC: 7999028. DOI: 10.3390/children8030196. View

Endzelins E, Berger A, Melne V, Bajo-Santos C, Sobolevska K, Abols A . Detection of circulating miRNAs: comparative analysis of extracellular vesicle-incorporated miRNAs and cell-free miRNAs in whole plasma of prostate cancer patients. BMC Cancer. 2017; 17(1):730. PMC: 5679326. DOI: 10.1186/s12885-017-3737-z. View

10.

Aswad H, Forterre A, Wiklander O, Vial G, Danty-Berger E, Jalabert A . Exosomes participate in the alteration of muscle homeostasis during lipid-induced insulin resistance in mice. Diabetologia. 2014; 57(10):2155-64. PMC: 4153976. DOI: 10.1007/s00125-014-3337-2. View

11.

Del Ry S, Cabiati M, Bianchi V, Randazzo E, Peroni D, Clerico A . C-type natriuretic peptide plasma levels and whole blood mRNA expression show different trends in adolescents with different degree of endothelial dysfunction. Peptides. 2019; 124:170218. DOI: 10.1016/j.peptides.2019.170218. View

12.

Raposo G, Stahl P . Extracellular vesicles: a new communication paradigm?. Nat Rev Mol Cell Biol. 2019; 20(9):509-510. DOI: 10.1038/s41580-019-0158-7. View

13.

Wentworth J, Naselli G, Brown W, Doyle L, Phipson B, Smyth G . Pro-inflammatory CD11c+CD206+ adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes. 2010; 59(7):1648-56. PMC: 2889764. DOI: 10.2337/db09-0287. View

14.

Cabiati M, Randazzo E, Salvadori C, Peroni D, Federico G, Del Ry S . Circulating microRNAs associated with C-type natriuretic peptide in childhood obesity. Peptides. 2020; 133:170387. DOI: 10.1016/j.peptides.2020.170387. View

15.

Zhuang G, Meng C, Guo X, Cheruku P, Shi L, Xu H . A novel regulator of macrophage activation: miR-223 in obesity-associated adipose tissue inflammation. Circulation. 2012; 125(23):2892-903. DOI: 10.1161/CIRCULATIONAHA.111.087817. View

16.

Holvoet P, Vanhaverbeke M, Bloch K, Baatsen P, Sinnaeve P, Janssens S . Low MT-CO1 in Monocytes and Microvesicles Is Associated With Outcome in Patients With Coronary Artery Disease. J Am Heart Assoc. 2016; 5(12). PMC: 5210432. DOI: 10.1161/JAHA.116.004207. View

17.

Bustin S, Benes V, Garson J, Hellemans J, Huggett J, Kubista M . The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55(4):611-22. DOI: 10.1373/clinchem.2008.112797. View

18.

Thomou T, Mori M, Dreyfuss J, Konishi M, Sakaguchi M, Wolfrum C . Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature. 2017; 542(7642):450-455. PMC: 5330251. DOI: 10.1038/nature21365. View

19.

Thaker V . GENETIC AND EPIGENETIC CAUSES OF OBESITY. Adolesc Med State Art Rev. 2018; 28(2):379-405. PMC: 6226269. View

20.

Nik Mohamed Kamal N, Shima Shahidan W . Non-Exosomal and Exosomal Circulatory MicroRNAs: Which Are More Valid as Biomarkers?. Front Pharmacol. 2020; 10:1500. PMC: 6984169. DOI: 10.3389/fphar.2019.01500. View