70
Views
26
CrossRef citations to date
0
Altmetric
Research Article

RBM4 Regulates Neuronal Differentiation of Mesenchymal Stem Cells by Modulating Alternative Splicing of Pyruvate Kinase M

, , &
Article: e00466-16 | Received 18 Aug 2016, Accepted 01 Nov 2016, Published online: 17 Mar 2023

REFERENCES

  • Tarn WY, Kuo HC, Yu HI, Liu SW, Tseng CT, Dhananjaya D, Hung KY, Tu CC, Chang SH, Huang GJ, Chiu IM. 2016. RBM4 promotes neuronal differentiation and neurite outgrowth via Numb isoform expression. Mol Biol Cell 27:1676–1683. https://doi.org/10.1091/mbc.E15-11-0798.
  • Wang Y, Chen D, Qian H, Tsai YS, Shao S, Liu Q, Dominguez D, Wang Z. 2014. The splicing factor RBM4 controls apoptosis, proliferation, and migration to suppress tumor progression. Cancer Cell 26:374–389. https://doi.org/10.1016/j.ccr.2014.07.010.
  • Lin JC, Tarn WY. 2011. RBM4 down-regulates PTB and antagonizes its activity in muscle cell-specific alternative splicing. J Cell Biol 193:509–520. https://doi.org/10.1083/jcb.201007131.
  • Lin JC, Yan YT, Hsieh WK, Peng PJ, Su CH, Tarn WY. 2013. RBM4 promotes pancreas cell differentiation and insulin expression. Mol Cell Biol 33:319–327. https://doi.org/10.1128/MCB.01266-12.
  • Lin JC, Lu YH, Liu YR, Lin YJ. 9February2016. RBM4a-regulated splicing cascade modulates the differentiation and metabolic activities of brown adipocytes. Sci Rep https://doi.org/10.1038/srep20665.
  • Joyce N, Annett G, Wirthlin L, Olson S, Bauer G, Nolta JA. 2010. Mesenchymal stem cells for the treatment of neurodegenerative disease. Regen Med 5:933–946. https://doi.org/10.2217/rme.10.72.
  • Shyh-Chang N, Daley GQ, Cantley LC. 2013. Stem cell metabolism in tissue development and aging. Development 140:2535–2547. https://doi.org/10.1242/dev.091777.
  • Folmes CDL, Dzeja PP, Nelson TJ, Terzic A. 2012. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11:596–606. https://doi.org/10.1016/j.stem.2012.10.002.
  • Rossi DJ, Jamieson CHM, Weissman IL. 2008. Stems cells and the pathways to aging and cancer. Cell 132:681–696. https://doi.org/10.1016/j.cell.2008.01.036.
  • Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St John JC. 2007. Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 120:4025–4034. https://doi.org/10.1242/jcs.016972.
  • Takubo K, Nagamatsu G, Kobayashi CI, Nakamura-Ishizu A, Kobayashi H, Ikeda E, Goda N, Rahimi Y, Johnson RS, Soga T, Hirao A, Suematsu M, Suda T. 2013. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12:49–61. https://doi.org/10.1016/j.stem.2012.10.011.
  • Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH. 2008. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26:960–968. https://doi.org/10.1634/stemcells.2007-0509.
  • Homem CCF, Steinmann V, Burkard TR, Jais A, Esterbauer H, Knoblich A. 2014. Ecdysone and Mediator change energy metabolism to terminate proliferation in Drosophila neural stem cells. Cell 158:874–888. https://doi.org/10.1016/j.cell.2014.06.024.
  • Lange C, Garcia MT, Decimo I, Bifari F, Eelen G, Quaegebeur A, Boon R, Zhao H, Boeckx B, Chang J, Wu C, Le Nobel F, Lambrechts D, Dewerhin M, Kuo CJ, Huttner WB, Carmeliet P. 2016. Relief of hypoxia by angiogenesis promotes neural stem cell differentiation by targeting glycolysis. EMBO J 35:924–941. https://doi.org/10.15252/embj.201592372.
  • Bartesaghi S, Graziano V, Galavotti S, Henriquez NV, Betts J, Saxena J, Deli A, Karlsson A, Martins LM, Capasso M, Nicotera P, Brandner S, De Laurenzi V, Salomoni P. 2015. Inhibition of oxidative metabolism leads to p53 genetic inactivation and transformation in neural stem cells. Proc Natl Acad Sci U S A 112:1059–1064. https://doi.org/10.1073/pnas.1413165112.
  • Bélanger M, Allaman I, Magistretti PJ. 2011. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14:724–738. https://doi.org/10.1016/j.cmet.2011.08.016.
  • Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O'Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, Deng S, Liddelow SA, Zhang C, Daneman R, Maniatis T, Barres BA, Wu JQ. 2014. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34:11929–11947. https://doi.org/10.1523/JNEUROSCI.1860-14.2014.
  • Alves-Filho JC, Påisson-McDermott EM. 21April2016. Pyruvate kinase M2: a potential target for regulating inflammation. Front Immunol https://doi.org/10.3389/immu.2016.00145.
  • Taniguchi K, Ito Y, Sugito N, Kumazaki M, Shinohara H, Yamada N, Nakagawa Y, Sugiyama T, Futamura M, Otsuki Y, Yoshida K, Uchiyama K, Akao Y. 2015. Organ-specific PTB1-asociated microRNAs determine expression of pyruvate kinase isoforms. Sci Rep 5:8647. https://doi.org/10.1038/srep08647.
  • David CJ, Chen M, Assanah M, Canoll P, Manley JL. 2010. hnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 463:364–368. https://doi.org/10.1038/nature08697.
  • Clower CV, Chatterjee D, Wang Z, Cantley LC, Vander Heiden MG, Krainer AR. 2010. The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism. Proc Natl Acad Sci U S A 107:1894–1899. https://doi.org/10.1073/pnas.0914845107.
  • Chen M, David CJ, Manley JL. 2012. Concentration-dependent control of pyruvate kinase M mutually exclusive splicing by hnRNP proteins. Nat Struct Mol Biol 19:346–354. https://doi.org/10.1038/nsmb.2219.
  • Lin JC, Tarn WY. 2005. Exon selection in alpha-tropomyosin mRNA is regulated by the antagonistic action of RBM4 and PTB. Mol Cell Biol 25:10111–10121. https://doi.org/10.1128/MCB.25.22.10111-10121.2005.
  • Tsai CC, Chen CL, Liu HC, Lee YT, Wang HW, Hou LT, Hung SC. 2010. Overexpression of hTERT increases stem-like properties and decreases spontaneous differentiation in human mesenchymal stem cell lines. J Biomed Sci 17:64. https://doi.org/10.1186/1423-0127-17-64.
  • Gueroussov S, Gonatopoulos-Pournatzis T, Irimia M, Raj B, Lin ZY, Gingras AC, Blencowe BJ. 2015. An alternative splicing event amplifies evolutionary differences between vertebrates. Science 349:868–873. https://doi.org/10.1126/science.aaa8381.
  • Nakashima K, Takizawa T, Ochiai W, Yanagisawa M, Hisatsune T, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T. 2001. BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci U S A 8:5868–5873.
  • Wang Y, Yang J, Li H, Wang X, Zhu L, Fan M, Wang X. 2013. Hypoxia promotes dopaminergic differentiation of mesenchymal stem cells and shows benefits for transplantation in a rat model of Parkinson's disease. PLoS One 8:e54296. https://doi.org/10.1371/journal.pone.0054296.
  • Jeon ES, Shin JH, Hwang SJ, Moon GJ, Bang OY, Kim HH. 2014. Cobalt chloride induces neuronal differentiation of human mesenchymal stem cells through upregulation of microRNA-124a. Biochem Biophys Res Commun 444:581–587. https://doi.org/10.1016/j.bbrc.2014.01.114.
  • Luo W, Hu H, Chang R, Zhong J, Knable M, O'Meally R, Cole RN, Pandey A, Semenza GL. 2011. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 145:732–744. https://doi.org/10.1016/j.cell.2011.03.054.
  • Agostini M, Romeo F, Inoue S, Niklisin-Chirou MV, Elia AJ, Dinsdale D, Morone N, Knight RA, Mak TW, Melino G. 8April2016. Metabolic reprogramming during neuronal differentiation. Cell Death Differ https://doi.org/10.1038/cdd.2016.36.
  • Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. 2010. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7:150–161. https://doi.org/10.1016/j.stem.2010.07.007.
  • Vieira HL, Alves PM, Vercelli A. 2011. Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog Neurobiol 93:444–455. https://doi.org/10.1016/j.pneurobio.2011.01.007.
  • Pacary E, Legros H, Valable S, Duchatelle P, Lecocq M, Petit E, Nicole O, Bernaudin M. 2006. Synergistic effect of CoCl(2) and ROCK inhibition on mesenchymal stem cell differentiation into neuron-like cells. J Cell Sci 199:2667–2678.
  • Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, Shiue L, Ares M, Jr, Black DL. 2007. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21:1636–1652. https://doi.org/10.1101/gad.1558107.
  • Makeyev EV, Zhang J, Carrasco MA, Maniatis T. 2007. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27:435–448. https://doi.org/10.1016/j.molcel.2007.07.015.
  • Lou CH, Shao A, Shum EY, Espinoza JL, Huang L, Katam R, Wilkinson MF. 2014. Posttranscriptional control of the stem cell and neurogenic programs by the nonsense-mediated RNA decay pathway. Cell Rep 6:748–764. https://doi.org/10.1016/j.celrep.2014.01.028.
  • Lai MC, Kuo HW, Chang WC, Tarn WY. 2003. A novel splicing regulator shares a nuclear import pathway with SR proteins. EMBO J 22:1359–1369. https://doi.org/10.1093/emboj/cdg126.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.