{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,2]],"date-time":"2026-05-02T15:06:14Z","timestamp":1777734374827,"version":"3.51.4"},"reference-count":48,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2022,1,7]],"date-time":"2022-01-07T00:00:00Z","timestamp":1641513600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100002243","name":"National Ataxia Foundation","doi-asserted-by":"publisher","award":["E81I18000370005"],"award-info":[{"award-number":["E81I18000370005"]}],"id":[{"id":"10.13039\/100002243","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009647","name":"Ministry of Health","doi-asserted-by":"publisher","award":["RF-2019-12368918"],"award-info":[{"award-number":["RF-2019-12368918"]}],"id":[{"id":"10.13039\/100009647","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,6,22]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Frataxin (FXN) deficiency is responsible for Friedreich\u2019s ataxia (FRDA) in which, besides the characteristic features of spinocerebellar ataxia, two thirds of patients develop hypertrophic cardiomyopathy that often progresses to heart failure and premature death. Different mechanisms might underlie FRDA pathogenesis. Among them, the role of miRNAs deserves investigations. We carried out an miRNA PCR-array analysis of plasma samples of early-, intermediate- and late-onset FRDA groups, defining a set of 30 differentially expressed miRNAs. Hsa-miR223-3p is the only miRNA shared between the three patient groups and appears upregulated in all of them. The up-regulation of hsa-miR223-3p was further validated in all enrolled patients (n\u2009=\u200937, Fc\u2009=\u2009+2.3; P\u2009&amp;lt;\u20090.0001). Using a receiver operating characteristic curve analysis, we quantified the predictive value of circulating hsa-miR223-3p for FRDA, obtaining an area under the ROC curve value of 0.835 (P\u2009&amp;lt;\u20090.0001) for all patients. Interestingly, we found a significant positive correlation between hsa-miR223-3p expression and cardiac parameters in typical FRDA patients (onset &amp;lt;\u200925\u00a0years). Moreover, a significant negative correlation between hsa-miR223-3p expression and HAX-1 (HCLS1-associated protein X-1) at mRNA and protein level was observed in all FRDA patients. In silico analyses suggested HAX-1 as a target gene of hsa-miR223-3p. Accordingly, we report that HAX-1 is negatively regulated by hsa-miR223-3p in cardiomyocytes (AC16) and neurons (SH-SY5Y), which are critically affected cell types in FRDA. This study describes for the first time the association between hsa-miR223-3p and HAX-1 expression in FRDA, thus supporting a potential role of this microRNA as non-invasive epigenetic biomarker for FRDA.<\/jats:p>","DOI":"10.1093\/hmg\/ddac005","type":"journal-article","created":{"date-parts":[[2022,1,5]],"date-time":"2022-01-05T12:23:20Z","timestamp":1641385400000},"page":"2010-2022","source":"Crossref","is-referenced-by-count":6,"title":["Hsa-miR223-3p circulating level is upregulated in Friedreich\u2019s ataxia and inversely associated with HCLS1 associated protein X-1, HAX-1"],"prefix":"10.1093","volume":"31","author":[{"given":"Andrea","family":"Quatrana","sequence":"first","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elena","family":"Morini","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Section of Medical Genetics, University of Rome Tor Vergata, Rome 00133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Francesca","family":"Tiano","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"},{"name":"Unit of Oncogenomics and Epigenetics , IRCCS Regina Elena National Cancer Institute, Rome 00144, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chiara","family":"Vancheri","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Section of Medical Genetics, University of Rome Tor Vergata, Rome 00133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Luca","family":"Panarello","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Silvia","family":"Romano","sequence":"additional","affiliation":[{"name":"Neurosciences , Mental Health and Sensory Organs (NESMOS) Department, Faculty of Medicine and Psychology, Sapienza University, Rome 00189 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christian","family":"Marcotulli","sequence":"additional","affiliation":[{"name":"UOC Neurology , Provincial General Hospital of Macerata, Macerata 62100 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carlo","family":"Casali","sequence":"additional","affiliation":[{"name":"Department of Medical Surgical Sciences and Biotechnologies , Polo Pontino-Sapienza University of Rome, Latina 04100 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Caterina","family":"Mariotti","sequence":"additional","affiliation":[{"name":"Unit of Medical Genetics and Neurogenetics , Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan 20133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alessia","family":"Mongelli","sequence":"additional","affiliation":[{"name":"Unit of Medical Genetics and Neurogenetics , Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan 20133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mario","family":"Fichera","sequence":"additional","affiliation":[{"name":"Unit of Medical Genetics and Neurogenetics , Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan 20133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alessandra","family":"Rufini","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"},{"name":"Fratagene Therapeutics Srl , Rome 00144 , Italy"},{"name":"Saint Camillus International University of Health and Medical Sciences , Rome 00131, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5421-4846","authenticated-orcid":false,"given":"Ivano","family":"Cond\u00f2","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giuseppe","family":"Novelli","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Section of Medical Genetics, University of Rome Tor Vergata, Rome 00133 , Italy"},{"name":"Neuromed Institute , IRCCS, Pozzilli 86077, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberto","family":"Testi","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"},{"name":"Fratagene Therapeutics Srl , Rome 00144 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2209-2156","authenticated-orcid":false,"given":"Francesca","family":"Amati","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Section of Medical Genetics, University of Rome Tor Vergata, Rome 00133 , Italy"},{"name":"Department for the Promotion of Human Science and Quality of Life , University San Raffaele, Rome 00166 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0213-9407","authenticated-orcid":false,"given":"Florence","family":"Malisan","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Prevention , Laboratory of Signal Transduction, University of Rome Tor Vergata, Rome 00133 , Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2022,1,7]]},"reference":[{"key":"2022062822114041900_ref1","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1089\/ars.2009.3015","article-title":"Friedreich ataxia: molecular mechanisms, redox considerations, and therapeutic opportunities","volume":"13","author":"Santos","year":"2010","journal-title":"Antioxid. Redox Signal."},{"key":"2022062822114041900_ref2","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1177\/0883073812448535","article-title":"Cardiomyopathy in Friedreich ataxia: clinical findings and research","volume":"27","author":"Payne","year":"2012","journal-title":"J. Child Neurol."},{"key":"2022062822114041900_ref3","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1086\/513887","article-title":"Phenotype correlation and intergenerational dynamics of the Friedreich ataxia GAA trinucleotide repeat","volume":"61","author":"Monr\u00f3s","year":"1997","journal-title":"Am. J. Hum. Genet."},{"key":"2022062822114041900_ref4","first-page":"8587203","article-title":"Friedreich\u2019s ataxia: clinical presentation of a compound heterozygote child with a rare nonsense mutation and comparison with previously published cases","volume":"2018","author":"Rao","year":"2018","journal-title":"Case Rep. Neurol. Med."},{"key":"2022062822114041900_ref5","article-title":"Epigenetics in Friedreich\u2019s ataxia: challenges and opportunities for therapy","volume":"2013","author":"Sandi","year":"2013","journal-title":"Genet. Res. Int."},{"key":"2022062822114041900_ref6","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1002\/mds.26382","article-title":"Delayed-onset Friedreich\u2019s ataxia revisited","volume":"31","author":"Lecocq","year":"2016","journal-title":"Mov. Disord. Off. J. Mov. Disord. Soc."},{"key":"2022062822114041900_ref7","doi-asserted-by":"crossref","first-page":"1717","DOI":"10.1212\/01.wnl.0000219042.60538.92","article-title":"Scale for the assessment and rating of ataxia: development of a new clinical scale","volume":"66","author":"Schmitz-H\u00fcbsch","year":"2006","journal-title":"Neurology"},{"key":"2022062822114041900_ref8","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1212\/NXG.0000000000000371","article-title":"Psychometric properties of the Friedreich ataxia rating scale","volume":"5","author":"Rummey","year":"2019","journal-title":"Neurol. Genet."},{"key":"2022062822114041900_ref9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4330\/wjc.v11.i1.1","article-title":"Heart disease in Friedreich\u2019s ataxia","volume":"11","author":"Hanson","year":"2019","journal-title":"World J. Cardiol."},{"key":"2022062822114041900_ref10","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.ijcard.2015.05.074","article-title":"The cardiomyopathy in Friedreich\u2019s ataxia \u2014 new biomarker for staging cardiac involvement","volume":"194","author":"Weidemann","year":"2015","journal-title":"Int. J. Cardiol."},{"key":"2022062822114041900_ref11","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1093\/hmg\/ddz306","article-title":"Frataxin deficiency in Friedreich\u2019s ataxia is associated with reduced levels of HAX-1, a regulator of cardiomyocyte death and survival","volume":"29","author":"Tiano","year":"2020","journal-title":"Hum. Mol. 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Data"},{"key":"2022062822114041900_ref21","doi-asserted-by":"crossref","first-page":"5237","DOI":"10.1038\/s41598-017-04996-9","article-title":"Circulating miR-323-3p is a biomarker for cardiomyopathy and an indicator of phenotypic variability in Friedreich\u2019s ataxia patients","volume":"7","author":"Seco-Cervera","year":"2017","journal-title":"Sci. Rep."},{"key":"2022062822114041900_ref22","doi-asserted-by":"crossref","first-page":"2639","DOI":"10.1007\/s12035-020-01899-1","article-title":"A comprehensive transcriptome analysis identifies FXN and BDNF as novel targets of miRNAs in Friedreich\u2019s ataxia patients","volume":"57","author":"Misiorek","year":"2020","journal-title":"Mol. Neurobiol."},{"key":"2022062822114041900_ref23","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.freeradbiomed.2020.07.019","article-title":"Antioxidant defense mechanisms and its dysfunctional regulation in the mitochondrial disease, Friedreich\u2019s ataxia","volume":"159","author":"Chiang","year":"2020","journal-title":"Free Radic. Biol. Med."},{"key":"2022062822114041900_ref24","first-page":"25","article-title":"Beyond loss of frataxin: the complex molecular pathology of Friedreich ataxia","volume":"17","author":"Evans-Galea","year":"2014","journal-title":"Discov. Med."},{"key":"2022062822114041900_ref25","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1007\/s00246-015-1325-z","article-title":"MiRNA-145 regulates the development of congenital heart disease through targeting FXN","volume":"37","author":"Wang","year":"2016","journal-title":"Pediatr. 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Sin."},{"key":"2022062822114041900_ref37","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/S1474-4422(14)70321-7","article-title":"Biological and clinical characteristics of the European Friedreich\u2019s Ataxia Consortium for Translational Studies (EFACTS) cohort: a cross-sectional analysis of baseline data","volume":"14","author":"Reetz","year":"2015","journal-title":"Lancet Neurol."},{"key":"2022062822114041900_ref38","article-title":"MIR223 microRNA 223 [Homo sapiens (human)] - Gene \u2013 NCBI"},{"key":"2022062822114041900_ref39","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.4161\/rna.21998","article-title":"Dose-dependent differential mRNA target selection and regulation by let-7a-7f and miR-17-92 cluster microRNAs","volume":"9","author":"Shu","year":"2012","journal-title":"RNA Biol."},{"key":"2022062822114041900_ref40","first-page":"1849","article-title":"MicroRNA-125a-5p regulates liver cancer cell growth, migration and invasion and EMT by targeting HAX1","volume":"46","author":"Zha","year":"2020","journal-title":"Int. J. Mol. Med."},{"key":"2022062822114041900_ref41","first-page":"1","article-title":"Mesenchymal stem cell-derived exosomal miR-223 regulates neuronal cell apoptosis","volume":"11","author":"Wei","year":"2020","journal-title":"Cell Death Dis."},{"key":"2022062822114041900_ref42","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.4103\/1673-5374.280307","article-title":"MicroRNAs as disease progression biomarkers and therapeutic targets in experimental autoimmune encephalomyelitis model of multiple sclerosis","volume":"15","author":"Martinez","year":"2020","journal-title":"Neural Regen. 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Cardiol."},{"key":"2022062822114041900_ref46","doi-asserted-by":"crossref","first-page":"1439","DOI":"10.1159\/000489185","article-title":"MicroRNA-223 regulates cardiac fibrosis after myocardial infarction by targeting RASA1","volume":"46","author":"Liu","year":"2018","journal-title":"Cell. Physiol. Biochem."},{"key":"2022062822114041900_ref47","doi-asserted-by":"crossref","first-page":"13721","DOI":"10.1038\/srep13721","article-title":"Exosomal miR-223 contributes to mesenchymal stem cell-elicited cardioprotection in polymicrobial sepsis","volume":"5","author":"Wang","year":"2015","journal-title":"Sci. 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