{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,27]],"date-time":"2026-06-27T05:45:25Z","timestamp":1782539125229,"version":"3.54.5"},"reference-count":48,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T00:00:00Z","timestamp":1782172800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>Background\/Objectives: Long non-coding RNAs (lncRNAs) have been identified as potential biomarkers for cancer diagnosis and prognosis. In the present study, we proposed the analysis of four lncRNAs as a diagnostic support candidate for the follow-up of leukemia patients. The aim of this study was to characterize the expression of BALR6, LINC-PINT, MEG3, and ZEB1-AS1 in patients with B-cell acute lymphoblastic leukemia (B-ALL) at diagnosis and at the end of remission induction therapy. Methods: B-ALL diagnosis and MRD assessment were performed by flow cytometry, while lncRNA expression levels were quantified using TaqMan probe-based assays. Results: Fifteen pediatric patients with B-ALL were followed longitudinally. MRD evaluation identified seven refractory and eight remitted patients. Significant expression changes were observed for MEG3 in remitted patients and for BALR6 and LINC-PINT in refractory patients. No statistically significant differences were detected for ZEB1-AS1. Conclusions: Changes in MEG3, LINC-PINT, and BALR6 lncRNA expression are associated with treatment response and MRD status in pediatric B-ALL, supporting their potential role as complementary biomarkers to conventional MRD monitoring.<\/jats:p>","DOI":"10.3390\/life16071042","type":"journal-article","created":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T08:19:52Z","timestamp":1782202792000},"page":"1042","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Long Non-Coding RNA Expression in B-Cell Precursor Acute Lymphoblastic Leukemia: Analysis of LINC-PINT, MEG3, BALR6, and ZEB1-AS1"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0009-0002-7619-860X","authenticated-orcid":false,"given":"Gabriel","family":"Mata Moreno","sequence":"first","affiliation":[{"name":"Medical Genomics Section, Research Center in Health Sciences and Biomedicine, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"},{"name":"Molecular and Translational Medicine Section, Research Center for Health Sciences and Biomedicine, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9028-442X","authenticated-orcid":false,"given":"Edgar A.","family":"Turrubiartes Mart\u00ednez","sequence":"additional","affiliation":[{"name":"Medical Genomics Section, Research Center in Health Sciences and Biomedicine, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"},{"name":"Hematology Laboratory, Faculty of Chemical Sciences, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9756-7713","authenticated-orcid":false,"given":"Lourdes Cecilia Correa","family":"Gonz\u00e1lez","sequence":"additional","affiliation":[{"name":"Hospital Regional de Alta Especialidad \u201cDr. Ignacio Morones Prieto\u201d, San Luis Potosi 78290, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-0593-9649","authenticated-orcid":false,"given":"Eduardo Roberto Caballero","family":"Lugo","sequence":"additional","affiliation":[{"name":"Hospital Regional de Alta Especialidad \u201cDr. Ignacio Morones Prieto\u201d, San Luis Potosi 78290, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u00d3scar","family":"P\u00e9rez Ram\u00edrez","sequence":"additional","affiliation":[{"name":"Hospital Regional de Alta Especialidad \u201cDr. Ignacio Morones Prieto\u201d, San Luis Potosi 78290, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7335-7156","authenticated-orcid":false,"given":"Perla Ni\u00f1o","family":"Moreno","sequence":"additional","affiliation":[{"name":"Medical Genomics Section, Research Center in Health Sciences and Biomedicine, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"},{"name":"Faculty of Chemical Sciences, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2824-5486","authenticated-orcid":false,"given":"Esther","family":"Layseca Espinosa","sequence":"additional","affiliation":[{"name":"Molecular and Translational Medicine Section, Research Center for Health Sciences and Biomedicine, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"},{"name":"Department of Immunology, Faculty of Medicine, Universidad Aut\u00f3noma de San Luis Potos\u00ed, San Luis Potosi 78210, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,6,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.1007\/s12672-025-03683-w","article-title":"The global, regional, and national burden of acute lymphoblastic leukemia, 1990 to 2021: A cross-sectional analysis from the 2021 global burden of disease study","volume":"16","author":"Yuan","year":"2025","journal-title":"Discov. Oncol."},{"key":"ref_2","unstructured":"Centro Nacional para la Salud de la Infancia y la Adolescencia (CeNSIA) (2026, June 15). Comportamiento Epidemiol\u00f3gico del C\u00e1ncer en Menores de 18 A\u00f1os. Available online: https:\/\/www.gob.mx\/salud\/censia\/documentos\/epidemiologia-del-cancer-en-menores-de-18-anos-mexico-2015."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Juarez-Ocana, S., Gonzalez-Miranda, G., Mejia-Arangure, J.M., Rendon-Macias, M.E., Martinez-Garcia Mdel, C., and Fajardo-Gutierrez, A. (2004). Frequency of cancer in children residing in Mexico City and treated in the hospitals of the Instituto Mexicano del Seguro Social (1996\u20132001). BMC Cancer, 4.","DOI":"10.1186\/1471-2407-4-50"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"N\u00fa\u00f1ez-Enr\u00edquez, J.C., Romo-Rodr\u00edguez, R., Gaspar-Mendoza, P., Zamora-Herrera, G., Torres-Pineda, L., Amador-Cardoso, J., L\u00f3pez-Blanco, J.A., Alfaro-Hern\u00e1ndez, L., L\u00f3pez-Garc\u00eda, L., and Rosas-Cruz, A. (2024). Implementation of a roadmap for the comprehensive diagnosis, follow-up, and research of childhood leukemias in vulnerable regions of Mexico: Results from the PRONAII Strategy. Front. Oncol., 14.","DOI":"10.3389\/fonc.2024.1304690"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2807","DOI":"10.1182\/blood-2012-02-265884","article-title":"How I treat relapsed childhood acute lymphoblastic leukemia","volume":"120","author":"Locatelli","year":"2012","journal-title":"Blood"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"5178","DOI":"10.1002\/cncr.30899","article-title":"Survival among children diagnosed with acute lymphoblastic leukemia in the United States, by race and age, 2001 to 2009: Findings from the CONCORD-2 study","volume":"123","author":"Tai","year":"2017","journal-title":"Cancer"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3996","DOI":"10.1182\/blood-2015-03-580027","article-title":"Minimal residual disease diagnostics in acute lymphoblastic leukemia: Need for sensitive, fast, and standardized technologies","volume":"125","author":"Orfao","year":"2015","journal-title":"Blood"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2318","DOI":"10.1038\/sj.leu.2403135","article-title":"Standardization and quality control studies of \u2018real-time\u2019quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia\u2013a Europe Against Cancer program","volume":"17","author":"Gabert","year":"2003","journal-title":"Leukemia"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Qian, Y., Shi, L., and Luo, Z. (2020). Long non-coding RNAs in cancer: Implications for diagnosis, prognosis, and therapy. Front. Med., 7.","DOI":"10.3389\/fmed.2020.612393"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"10976","DOI":"10.18632\/oncotarget.2770","article-title":"A pathophysiological view of the long non-coding RNA world","volume":"5","author":"Capaccioli","year":"2014","journal-title":"Oncotarget"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Dahl, M., Kristensen, L.S., and Gr\u00f8nb\u00e6k, K. (2018). Long non-coding RNAs guide the fine-tuning of gene regulation in B-cell development and malignancy. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19092475"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Cruz-Miranda, G.M., Hidalgo-Miranda, A., B\u00e1rcenas-L\u00f3pez, D.A., N\u00fa\u00f1ez-Enr\u00edquez, J.C., Ram\u00edrez-Bello, J., Mej\u00eda-Arangur\u00e9, J.M., and Jim\u00e9nez-Morales, S. (2019). Long non-coding RNA and acute leukemia. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20030735"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3892\/ijo.2022.5348","article-title":"lncRNA deregulation in childhood acute lymphoblastic leukemia: A systematic review","volume":"60","author":"Illarregi","year":"2022","journal-title":"Int. J. Oncol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Gasic, V., Karan-Djurasevic, T., Pavlovic, D., Zukic, B., Pavlovic, S., and Tosic, N. (2022). Diagnostic and Therapeutic Implications of Long Non-Coding RNAs in Leukemia. Life, 12.","DOI":"10.3390\/life12111770"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Baghdadi, H., Heidari, R., Zavvar, M., Ahmadi, N., Shakouri Khomartash, M., Vahidi, M., Mohammadimehr, M., Bashash, D., and Ghorbani, M. (2023). Long non-coding RNA signatures in lymphopoiesis and lymphoid malignancies. Noncoding RNA, 9.","DOI":"10.3390\/ncrna9040044"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Xu, J., Wang, X., Zhu, C., and Wang, K. (2022). A review of current evidence about lncRNA MEG3: A tumor suppressor in multiple cancers. Front. Cell. Dev. Biol., 10.","DOI":"10.3389\/fcell.2022.997633"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1097\/FPC.0000000000000534","article-title":"MEG3 in hematologic malignancies: From the role of disease biomarker to therapeutic target","volume":"34","author":"Zhang","year":"2024","journal-title":"Pharmacogenet. Genom."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"112127","DOI":"10.1016\/j.biopha.2021.112127","article-title":"Long intragenic non-coding RNA p53-induced transcript (LINC-PINT) as a novel prognosis indicator and therapeutic target in cancer","volume":"143","author":"He","year":"2021","journal-title":"Biomed. Pharmacother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1038\/s41419-021-03728-2","article-title":"LINC-PINT impedes DNA repair and enhances radiotherapeutic response by targeting DNA-PKcs in nasopharyngeal cancer","volume":"12","author":"Wang","year":"2021","journal-title":"Cell Death Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1186\/s12943-015-0485-z","article-title":"BALR-6 regulates cell growth and cell survival in B-lymphoblastic leukemia","volume":"14","author":"Fernando","year":"2015","journal-title":"Mol. Cancer"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"584","DOI":"10.21037\/tcr-2024-2276","article-title":"LncRNA ZEB1-AS1 promotes the proliferation and migration of non-small cell lung cancer by activating epithelial-mesenchymal transition with STAT3","volume":"14","author":"Chen","year":"2025","journal-title":"Transl. Cancer Res."},{"key":"ref_22","first-page":"2624","article-title":"Long non-coding RNA ZEB1-AS1 is associated with poor prognosis in gastric cancer and promotes cancer cell metastasis","volume":"22","author":"Liu","year":"2018","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1111\/ijlh.12795","article-title":"Role of CD81 and CD58 in minimal residual disease detection in pediatric B lymphoblastic leukemia","volume":"40","author":"Tsitsikov","year":"2018","journal-title":"Int. J. Lab. Hematol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Li, W. (2022). Measurable residual disease testing in acute leukemia: Technology and clinical significance. Leukemia, Exon Publications.","DOI":"10.36255\/exon-publications-leukemia-measurable-residual-disease"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1016\/j.ccell.2016.03.010","article-title":"Long noncoding RNAs in cancer pathways","volume":"29","author":"Schmitt","year":"2016","journal-title":"Cancer Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1038\/s41580-022-00566-8","article-title":"Long non-coding RNAs: Definitions, functions, challenges and recommendations","volume":"24","author":"Mattick","year":"2023","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1080\/00365513.2021.1881998","article-title":"Long non-coding RNA MEG3 as a candidate prognostic factor for induction therapy response and survival profile in childhood acute lymphoblastic leukemia patients","volume":"81","author":"Gao","year":"2021","journal-title":"Scand. J. Clin. Lab. Investig."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"7483","DOI":"10.1038\/s41598-024-57836-y","article-title":"Long non-coding RNA LINC-PINT as a novel prognostic biomarker in human cancer: A meta-analysis and machine learning","volume":"14","author":"Lin","year":"2024","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"12842","DOI":"10.18632\/oncotarget.24401","article-title":"Deregulation of LINC-PINT in acute lymphoblastic leukemia is implicated in abnormal proliferation of leukemic cells","volume":"9","author":"Ezponda","year":"2018","journal-title":"Oncotarget"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.jfma.2016.12.002","article-title":"Concordance of two approaches in monitoring of minimal residual disease in B-precursor acute lymphoblastic leukemia: Fusion transcripts and leukemia-associated immunophenotypes","volume":"116","author":"Huang","year":"2017","journal-title":"J. Formos. Med. Assoc."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1801","DOI":"10.1007\/s10529-017-2421-3","article-title":"LncRNA ZEB1-AS1 contributes to STAT3 activation by associating with IL-11 in B-lymphoblastic leukemia","volume":"39","author":"Wang","year":"2017","journal-title":"Biotechnol. Lett."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1586","DOI":"10.1182\/blood.V81.6.1586.1586","article-title":"Effects of interleukin-11 on the proliferation and cell cycle status of myeloid leukemic cells","volume":"81","author":"Hu","year":"1993","journal-title":"Blood"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1186\/s12967-022-03456-x","article-title":"Tumor-suppressive MEG3 induces microRNA-493-5p expression to reduce arabinocytosine chemoresistance of acute myeloid leukemia cells by downregulating the METTL3\/MYC axis","volume":"20","author":"Wang","year":"2022","journal-title":"J. Transl. Med."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"100280","DOI":"10.1016\/j.jlb.2024.100280","article-title":"Liquid biopsy in gallbladder carcinoma: Current evidence and future prospective","volume":"6","author":"Mishra","year":"2024","journal-title":"J. Liq. Biopsy"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.1634\/theoncologist.2015-0156","article-title":"Comprehensive genomic profiling of advanced esophageal squamous cell carcinomas and esophageal adenocarcinomas reveals similarities and differences","volume":"20","author":"Wang","year":"2015","journal-title":"Oncologist"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1159\/000452529","article-title":"Three Circulating LncRNA Predict Early Progress of Esophageal Squamous Cell Carcinoma","volume":"40","author":"Hu","year":"2016","journal-title":"Cell. Physiol. Biochem."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"4348","DOI":"10.1016\/j.cell.2021.07.016","article-title":"A proteogenomic portrait of lung squamous cell carcinoma","volume":"184","author":"Satpathy","year":"2021","journal-title":"Cell"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"7539","DOI":"10.1002\/jcb.28028","article-title":"The discovery of a novel eight-mRNA-lncRNA signature predicting survival of hepatocellular carcinoma patients","volume":"120","author":"Shi","year":"2019","journal-title":"J. Cell. Biochem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"6902","DOI":"10.3748\/wjg.v25.i48.6902","article-title":"Diagnostic and prognostic value of lncRNA cancer susceptibility candidate 9 in hepatocellular carcinoma","volume":"25","author":"Zeng","year":"2019","journal-title":"World J. Gastroenterol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2150","DOI":"10.1002\/ijc.31573","article-title":"Identification of a five-lncRNA signature for predicting the risk of tumor recurrence in patients with breast cancer","volume":"143","author":"Li","year":"2018","journal-title":"Int. J. Cancer"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Shaath, H., Elango, R., and Alajez, N.M. (2021). Molecular classification of breast cancer utilizing long non-coding RNA (lncRNA) transcriptomes identifies novel diagnostic lncRNA panel for triple-negative breast cancer. Cancers, 13.","DOI":"10.3390\/cancers13215350"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1097\/MEG.0b013e328306a3a2","article-title":"Highly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis","volume":"21","author":"Matouk","year":"2009","journal-title":"Eur. J. Gastroenterol. Hepatol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e192","DOI":"10.1038\/oncsis.2015.48","article-title":"A serum-circulating long noncoding RNA signature can discriminate between patients with clear cell renal cell carcinoma and healthy controls","volume":"5","author":"Wu","year":"2016","journal-title":"Oncogenesis"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1186\/s12967-019-2032-y","article-title":"Prognosis of clear cell renal cell carcinoma (ccRCC) based on a six-lncRNA-based risk score: An investigation based on RNA-sequencing data","volume":"17","author":"Zeng","year":"2019","journal-title":"J. Transl. Med."},{"key":"ref_45","first-page":"3304","article-title":"Prognostic 4-lncRNA-based risk model predicts survival time of patients with head and neck squamous cell carcinoma","volume":"18","author":"Xing","year":"2019","journal-title":"Oncol. Lett."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"10049","DOI":"10.1080\/21655979.2021.1995577","article-title":"Identification and in vitro validation of prognostic lncRNA signature in head and neck squamous cell carcinoma","volume":"12","author":"Wang","year":"2021","journal-title":"Bioengineered"},{"key":"ref_47","first-page":"1473","article-title":"A three-lncRNA signature for prognosis prediction of acute myeloid leukemia in patients","volume":"18","author":"Wang","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"ref_48","first-page":"2203","article-title":"lncRNA-CCDC26, as a novel biomarker, predicts prognosis in acute myeloid leukemia","volume":"18","author":"Chen","year":"2019","journal-title":"Oncol. Lett."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/16\/7\/1042\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,27]],"date-time":"2026-06-27T04:47:57Z","timestamp":1782535677000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/16\/7\/1042"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,23]]},"references-count":48,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["life16071042"],"URL":"https:\/\/doi.org\/10.3390\/life16071042","relation":{},"ISSN":["2075-1729"],"issn-type":[{"value":"2075-1729","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,23]]}}}