Dynamic changes in LINC00458/HBL1 lncRNA expression during hiPSC differentiation to cardiomyocytes.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
02 Jan 2024
Historique:
received: 18 10 2023
accepted: 12 12 2023
medline: 4 1 2024
pubmed: 4 1 2024
entrez: 3 1 2024
Statut: epublish

Résumé

Long non-coding RNAs (lncRNAs) constitute the largest and most diverse class of non-coding RNAs. They localize to the nucleus, cytoplasm, or both compartments, and regulate gene expression through various mechanisms at multiple levels. LncRNAs tend to evolve faster and present higher tissue- and developmental stage-specific expression than protein-coding genes. Initially considered byproducts of erroneous transcription without biological function, lncRNAs are now recognized for their involvement in numerous biological processes, such as immune response, apoptosis, pluripotency, reprogramming, and differentiation. In this study, we focused on Heart Brake lncRNA 1 (HBL1), a lncRNA recently reported to modulate the process of pluripotent stem cell differentiation toward cardiomyocytes. We employed RT-qPCR and high-resolution RNA FISH to monitor the expression and localization of HBL1 during the differentiation progression. Our findings indicate a significant increase in HBL1 expression during mesodermal and cardiac mesodermal stages, preceding an anticipated decrease in differentiated cells. We detected the RNA in discrete foci in both the nucleus and in the cytoplasm. In the latter compartment, we observed colocalization of HBL1 with Y-box binding protein 1 (YB-1), which likely results from an interaction between the RNA and the protein, as the two were found to be coimmunoprecipitated in RNP-IP experiments. Finally, we provide evidence that HBL1, initially reported as an independent lncRNA gene, is part of the LINC00458 (also known as lncRNA-ES3 or ES3) gene, forming the last exon of some LINC00458 splice isoforms.

Identifiants

pubmed: 38167488
doi: 10.1038/s41598-023-49753-3
pii: 10.1038/s41598-023-49753-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

109

Subventions

Organisme : Narodowe Centrum Nauki
ID : 2019/33/B/NZ3/02837
Organisme : Narodowe Centrum Nauki
ID : UMO2018/30/E/NZ1/00874
Organisme : Narodowe Centrum Nauki
ID : UMO-2022/45/B/NZ3/03890

Informations de copyright

© 2024. The Author(s).

Références

Charles Richard, J. L. & Eichhorn, P. J. A. Platforms for investigating LncRNA functions. SLAS Technol. 23, 493–506. https://doi.org/10.1177/2472630318780639 (2018).
doi: 10.1177/2472630318780639 pubmed: 29945466 pmcid: 6249642
Cabili, M. et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25, 1915–1927 (2011).
doi: 10.1101/gad.17446611 pubmed: 21890647 pmcid: 3185964
Gong, C., Popp, M. W. L. & Maquat, L. E. Biochemical analysis of long non-coding RNA-containing ribonucleoprotein complexes. Methods 58, 88–93 (2012).
doi: 10.1016/j.ymeth.2012.06.020 pubmed: 22789663 pmcid: 3523100
Flynn, R. A. & Chang, H. Y. Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell 14, 752–761. https://doi.org/10.1016/j.stem.2014.05.014 (2014).
doi: 10.1016/j.stem.2014.05.014 pubmed: 24905165 pmcid: 4120821
Robinson, E. K., Covarrubias, S. & Carpenter, S. The how and why of lncRNA function: An innate immune perspective. Biochim. et Biophys. Acta Gene Regul. Mech. 1863, 194419. https://doi.org/10.1016/j.bbagrm.2019.194419 (2020).
doi: 10.1016/j.bbagrm.2019.194419
Fico, A., Fiorenzano, A., Pascale, E., Patriarca, E. J. & Minchiotti, G. Long non-coding RNA in stem cell pluripotency and lineage commitment: Functions and evolutionary conservation. Cell. Mol. Life Sci. 76, 1459–1471. https://doi.org/10.1007/s00018-018-3000-z (2019).
doi: 10.1007/s00018-018-3000-z pubmed: 30607432 pmcid: 6439142
Wang, K. C. & Chang, H. Y. Molecular mechanisms of long noncoding RNAs. Mol. Cell 43, 904–914. https://doi.org/10.1016/j.molcel.2011.08.018 (2011).
doi: 10.1016/j.molcel.2011.08.018 pubmed: 21925379 pmcid: 3199020
Chujo, T. & Hirose, T. Nuclear bodies built on architectural long noncoding RNAs: Unifying principles of their construction and function. Mol. Cells 40, 889–896. https://doi.org/10.14348/molcells.2017.0263 (2017).
doi: 10.14348/molcells.2017.0263 pubmed: 29276943 pmcid: 5750707
Lekka, E. & Hall, J. Noncoding RNAs in disease. FEBS Lett. 592, 2884–2900. https://doi.org/10.1002/1873-3468.13182 (2018).
doi: 10.1002/1873-3468.13182 pubmed: 29972883 pmcid: 6174949
Kimbrel, E. A. & Lanza, R. Pluripotent stem cells: The last 10 years. Regen. Med. 11, 831–847. https://doi.org/10.2217/rme-2016-0117 (2016).
doi: 10.2217/rme-2016-0117 pubmed: 27908220
Liu, J., Li, Y., Lin, B., Sheng, Y. & Yang, L. HBL1 is a human long noncoding RNA that modulates cardiomyocyte development from pluripotent stem cells by counteracting MIR1. Dev. Cell 42, 333-348.e5 (2017).
doi: 10.1016/j.devcel.2017.07.023 pubmed: 28829943 pmcid: 5567988
Liu, J. et al. LncRNA HBL1 is Required for Genome-Wide PRC2 Occupancy and Function in Cardiogenesis from Human Pluripotent Stem Cells. (2021).
Burridge, P. W. et al. Chemically defined generation of human cardiomyocytes. Nat. Methods 11, 855–860 (2014).
doi: 10.1038/nmeth.2999 pubmed: 24930130 pmcid: 4169698
Ng, S. Y., Johnson, R. & Stanton, L. W. Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J. 31, 522–533 (2012).
doi: 10.1038/emboj.2011.459 pubmed: 22193719
Shin, Y. & Brangwynne, C. P. Liquid phase condensation in cell physiology and disease. Science 357, 6357. https://doi.org/10.1126/science.aaf4382 (2017).
doi: 10.1126/science.aaf4382
Cabili, M. N. et al. Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. Genome Biol. https://doi.org/10.1186/s13059-015-0586-4 (2015).
doi: 10.1186/s13059-015-0586-4 pubmed: 25630241 pmcid: 4369099
Grosch, M., Ittermann, S., Shaposhnikov, D. & Drukker, M. Chromatin-associated membraneless organelles in regulation of cellular differentiation. Stem Cell Rep. 15, 1220–1232. https://doi.org/10.1016/j.stemcr.2020.10.011 (2020).
doi: 10.1016/j.stemcr.2020.10.011
Grosch, M. et al. Nucleus size and DNA accessibility are linked to the regulation of paraspeckle formation in cellular differentiation. BMC Biol. https://doi.org/10.1186/s12915-020-00770-y (2020).
doi: 10.1186/s12915-020-00770-y pubmed: 32321486 pmcid: 7178590
Kohno, K., Izumi, H., Uchiumi, T., Ashizuka, M. & Kuwano, M. The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 25, 691–698 (2003).
doi: 10.1002/bies.10300 pubmed: 12815724
Eliseeva, I. A., Kim, E. R., Guryanov, S. G., Ovchinnikov, L. P. & Lyabin, D. N. Y-box-binding protein 1 (YB-1) and its functions. Biochemistry (Moscow) 76, 1402–1433. https://doi.org/10.1134/S0006297911130049 (2011).
doi: 10.1134/S0006297911130049 pubmed: 22339596
Mateu-Regué, À. et al. Single mRNP analysis reveals that small cytoplasmic mRNP granules represent mRNA singletons. Cell Rep. 29, 736-748.e4 (2019).
doi: 10.1016/j.celrep.2019.09.018 pubmed: 31618640
Kedersha, N. & Anderson, P. Mammalian stress granules and processing bodies. Methods Enzymol. 431, 61–81. https://doi.org/10.1016/S0076-6879(07)31005-7 (2007).
doi: 10.1016/S0076-6879(07)31005-7 pubmed: 17923231
Somasekharan, S. P. et al. YB-1 regulates stress granule formation and tumor progression by translationally activating G3BP1. J. Cell Biol. 208, 913–929 (2015).
doi: 10.1083/jcb.201411047 pubmed: 25800057 pmcid: 4384734
Suresh, P. S., Tsutsumi, R. & Venkatesh, T. YBX1 at the crossroads of non-coding transcriptome, exosomal, and cytoplasmic granular signaling. Eur. J. Cell Biol. 97, 163–167. https://doi.org/10.1016/j.ejcb.2018.02.003 (2018).
doi: 10.1016/j.ejcb.2018.02.003 pubmed: 29478751
Li, S. et al. Long noncoding RNA HOTAIR interacts with Y-Box Protein-1 (YBX1) to regulate cell proliferation. Life Sci. Alliance 4, e202101139 (2021).
doi: 10.26508/lsa.202101139 pubmed: 34266873 pmcid: 8321693
Song, S. et al. A novel long noncoding RNA, TMEM92-AS1, promotes gastric cancer progression by binding to YBX1 to mediate CCL5. Mol. Oncol. 15, 1256–1273 (2021).
doi: 10.1002/1878-0261.12863 pubmed: 33247987 pmcid: 8024739
Li, Y. L. et al. LncRNA BASP1-AS1 interacts with YBX1 to regulate Notch transcription and drives the malignancy of melanoma. Cancer Sci. 112, 4526–4542 (2021).
doi: 10.1111/cas.15140 pubmed: 34533860 pmcid: 8586662
Zhang, E. et al. A novel long noncoding RNA HOXC-AS3 mediates tumorigenesis of gastric cancer by binding to YBX1. Genome Biol. https://doi.org/10.1186/s13059-018-1523-0 (2018).
doi: 10.1186/s13059-018-1523-0 pubmed: 30537986 pmcid: 6290540
Stickeler, E. et al. The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J. 20, 3821–3830 (2001).
doi: 10.1093/emboj/20.14.3821 pubmed: 11447123 pmcid: 125550
Skabkina, O. V., Lyabin, D. N., Skabkin, M. A. & Ovchinnikov, L. P. YB-1 Autoregulates translation of its own mRNA at or prior to the step of 40S ribosomal subunit joining. Mol. Cell. Biol. 25, 3317–3323 (2005).
doi: 10.1128/MCB.25.8.3317-3323.2005 pubmed: 15798215 pmcid: 1069629
Goodarzi, H. et al. Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell 161, 790–802 (2015).
doi: 10.1016/j.cell.2015.02.053 pubmed: 25957686 pmcid: 4457382
Ray, D. et al. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat. Biotechnol. 27, 667–670 (2009).
doi: 10.1038/nbt.1550 pubmed: 19561594
Mattick, J. S. & Makunin, I. V. Non-coding RNA. Hum. Mol. Genet. https://doi.org/10.1093/hmg/ddl046 (2006).
doi: 10.1093/hmg/ddl046 pubmed: 16651366
Guttman, M. & Rinn, J. L. Modular regulatory principles of large non-coding RNAs. Nature 482, 339–346. https://doi.org/10.1038/nature10887 (2012).
doi: 10.1038/nature10887 pubmed: 22337053 pmcid: 4197003
Chen, Y.-F. et al. Control of matrix stiffness promotes endodermal lineage specification by regulating SMAD2/3 via lncRNA LINC00458. Sci. Adv. vol. 6. http://advances.sciencemag.org/ (2020).
Kula-Pacurar, A. et al. Visualization of SARS-CoV-2 using immuno RNA-fluorescence in situ hybridization. J. Visual. Exp. https://doi.org/10.3791/62067 (2020).
doi: 10.3791/62067

Auteurs

Patrycja Maciak (P)

Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland.

Agnieszka Suder (A)

Virogenetics Laboratory of Virology, Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland.
Doctoral School of Exact and Natural Sciences, Jagiellonian University, Łojasiewicza 11, 30-348, Cracow, Poland.

Jakub Wadas (J)

Virogenetics Laboratory of Virology, Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland.
Doctoral School of Exact and Natural Sciences, Jagiellonian University, Łojasiewicza 11, 30-348, Cracow, Poland.

Faith Aronimo (F)

Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland.

Paolo Maiuri (P)

Department of Molecular Medicine and Medical Biotechnology, University of Naples Federico II, Naples, Italy.

Michał Bochenek (M)

Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland.

Krzysztof Pyrc (K)

Virogenetics Laboratory of Virology, Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland.

Anna Kula-Pacurar (A)

Virogenetics Laboratory of Virology, Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland. anna.kula-pacurar@uj.edu.pl.

Marta Pabis (M)

Małopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7A, 30-387, Cracow, Poland. marta.pabis@uj.edu.pl.

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