Neural Differentiation in HDAC1-Depleted Cells Is Accompanied by Coilin Downregulation and the Accumulation of Cajal Bodies in Nucleoli

. 2017 ; 2017 () : 1021240. [epub] 20170227

Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28337219

Cajal bodies (CBs) are important compartments containing accumulated proteins that preferentially regulate RNA-related nuclear events, including splicing. Here, we studied the nuclear distribution pattern of CBs in neurogenesis. In adult brains, coilin was present at a high density, but CB formation was absent in the nuclei of the choroid plexus of the lateral ventricles. Cells of the adult hippocampus were characterized by a crescent-like morphology of coilin protein. We additionally observed a 70 kDa splice variant of coilin in adult mouse brains, which was different to embryonic brains and mouse pluripotent embryonic stem cells (mESCs), characterized by the 80 kDa standard variant of coilin. Here, we also showed that depletion of coilin is induced during neural differentiation and HDAC1 deficiency in mESCs caused coilin accumulation inside the fibrillarin-positive region of the nucleoli. A similar distribution pattern was observed in adult brain hippocampi, characterized by lower levels of both coilin and HDAC1. In summary, we observed that neural differentiation and HDAC1 deficiency lead to coilin depletion and coilin accumulation in body-like structures inside the nucleoli.

Zobrazit více v PubMed

Cajal S. R. Un sencillo metodo de coloracion selectiva del reticulo protoplasmico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrados. Trabajos del Laboratorio de Investigaciones Biológicas de la Universidad de Madrid. 1903;2:129–221.

Lafarga M., Casafont I., Bengoechea R., Tapia O., Berciano M. T. Cajal's contribution to the knowledge of the neuronal cell nucleus. Chromosoma. 2009;118(4):437–443. doi: 10.1007/s00412-009-0212-x. PubMed DOI

Baltanás F. C., Casafont I., Weruaga E., Alonso J. R., Berciano M. T., Lafarga M. Nucleolar disruption and cajal body disassembly are nuclear hallmarks of DNA damage-induced neurodegeneration in Purkinje cells. Brain Pathology. 2011;21(4):374–388. doi: 10.1111/j.1750-3639.2010.00461.x. PubMed DOI PMC

Ogg S. C., Lamond A. I. Cajal bodies and coilin—moving towards function. Journal of Cell Biology. 2002;159(1):17–21. doi: 10.1083/jcb.200206111. PubMed DOI PMC

Tapia O., Bengoechea R., Berciano M. T., Lafarga M. Nucleolar targeting of coilin is regulated by its hypomethylation state. Chromosoma. 2010;119(5):527–540. doi: 10.1007/s00412-010-0276-7. PubMed DOI

Nizami Z., Deryusheva S., Gall J. G. The Cajal body and histone locus body. Cold Spring Harbor perspectives in biology. 2010;2(7):p. a000653. doi: 10.1101/cshperspect.a000653. PubMed DOI PMC

Gall J. G. Cajal bodies: the first 100 years. Annual Review of Cell and Developmental Biology. 2000;16:273–300. doi: 10.1146/annurev.cellbio.16.1.273. PubMed DOI

Gall J. G. A role for Cajal bodies in assembly of the nuclear transcription machinery. Tsitologiia. 2003;45(10):971–975. PubMed

Lafontaine J. G. A light and electron microscope study of small, spherical nuclear bodies in meristematic cells of Allium cepa, Vicia faba, and Raphanus sativus. Journal of Cell Biology. 1965;26(1):1–17. doi: 10.1083/jcb.26.1.1. PubMed DOI PMC

Bártová E., Foltánková V., Legartová S., et al. Coilin is rapidly recruited to UVA-induced DNA lesions and γ-radiation affects localized movement of Cajal bodies. Nucleus. 2014;5(3):460–468. doi: 10.4161/nucl.29229. PubMed DOI PMC

Carmo-Fonseca M., Ferreira J., Lamond A. I. Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis—evidence that the coiled body is a kinetic nuclear structure. Journal of Cell Biology. 1993;120(4):841–852. doi: 10.1083/jcb.120.4.841. PubMed DOI PMC

Raška I., Andrade L. E. C., Ochs R. L., et al. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Experimental Cell Research. 1991;195(1):27–37. doi: 10.1016/0014-4827(91)90496-H. PubMed DOI

Tucker K. E., Berciano M. T., Jacobs E. Y., et al. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. Journal of Cell Biology. 2001;154(2):293–307. doi: 10.1083/jcb.200104083. PubMed DOI PMC

Wang Q., Sawyer I. A., Sung M.-H., et al. Cajal bodies are linked to genome conformation. Nature Communications. 2016;7 doi: 10.1038/ncomms10966.10966 PubMed DOI PMC

Sawyer I. A., Dundr M. Nuclear bodies: built to boost. Journal of Cell Biology. 2016;213(5):509–511. doi: 10.1083/jcb.201605049. PubMed DOI PMC

Dundr M. Nuclear bodies: multifunctional companions of the genome. Current Opinion in Cell Biology. 2012;24(3):415–422. doi: 10.1016/j.ceb.2012.03.010. PubMed DOI PMC

Dundr M., Hebert M. D., Karpova T. S., et al. In vivo kinetics of Cajal body components. Journal of Cell Biology. 2004;164(6):831–842. doi: 10.1083/jcb.200311121. PubMed DOI PMC

Platani M., Goldberg I., Lamond A. I., Swedlow J. R. Cajal body dynamics and association with chromatin are ATP-dependent. Nature Cell Biology. 2002;4(7):502–508. doi: 10.1038/ncb809. PubMed DOI

Platani M., Goldberg I., Swedlow J. R., Lamond A. I. In vivo analysis of Cajal body movement, separation, and joining in live human cells. Journal of Cell Biology. 2000;151(7):1561–1574. doi: 10.1083/jcb.151.7.1561. PubMed DOI PMC

Moore H. M., Bai B., Boisvert F.-M., et al. Quantitative proteomics and dynamic imaging of the nucleolus reveal distinct responses to UV and ionizing radiation. Molecular & Cellular Proteomics. 2011;10(10) doi: 10.1074/mcp.m111.009241. PubMed DOI PMC

Stixová L., Sehnalová P., Legartová S., et al. HP1β-dependent recruitment of UBF1 to irradiated chromatin occurs simultaneously with CPDs. Epigenetics & Chromatin. 2014;7(1, article 39) doi: 10.1186/1756-8935-7-39. PubMed DOI PMC

Boulon S., Westman B. J., Hutten S., Boisvert F.-M., Lamond A. I. The nucleolus under stress. Molecular Cell. 2010;40(2):216–227. doi: 10.1016/j.molcel.2010.09.024. PubMed DOI PMC

Kruhlak M., Crouch E. E., Orlov M., et al. The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature. 2007;447(7145):730–734. doi: 10.1038/nature05842. PubMed DOI

Rubbi C. P., Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO Journal. 2003;22(22):6068–6077. doi: 10.1093/emboj/cdg579. PubMed DOI PMC

Cajal S. R. Nota sobre la retina de los múscidos. Boletín de la Real Sociedad Española de Historia Natural. 1910;10:92–95.

MacDonald J. L., Roskams A. J. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Developmental Dynamics. 2008;237(8):2256–2267. doi: 10.1002/dvdy.21626. PubMed DOI

Volmar C.-H., Wahlestedt C. Histone deacetylases (HDACs) and brain function. Neuroepigenetics. 2015;1:20–27.

Jiang Y., Hsieh J. HDAC3 controls gap 2/mitosis progression in adult neural stem/progenitor cells by regulating CDK1 levels. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(37):13541–13546. doi: 10.1073/pnas.1411939111. PubMed DOI PMC

Bártová E., Pacherník J., Harničarová A., et al. Nuclear levels and patterns of histone H3 modification and HP1 proteins after inhibition of histone deacetylases. Journal of Cell Science. 2005;118(21):5035–5046. doi: 10.1242/jcs.02621. PubMed DOI

Görisch S. M., Lichter P., Rippe K. Mobility of multi-subunit complexes in the nucleus: accessibility and dynamics of chromatin subcompartments. Histochemistry and Cell Biology. 2005;123(3):217–228. doi: 10.1007/s00418-005-0752-y. PubMed DOI

Mouse brain atlas. http://mouse.brain-map.org/experiment/thumbnails/100048576?image_ type=atlas.

Lagger G., O'Carroll D., Rembold M., et al. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO Journal. 2002;21(11):2672–2681. doi: 10.1093/emboj/21.11.2672. PubMed DOI PMC

Zhu Y., Tomlinson R. L., Lukowiak A. A., Terns R. M., Terns M. P. Telomerase RNA accumulates in Cajal bodies in human cancer cells. Molecular Biology of the Cell. 2004;15(1):81–90. doi: 10.1091/mbc.e03-07-0525. PubMed DOI PMC

Andrade L. E. C., Chan E. K. L., Raska I., Peebles C. L., Roos G., Tan E. M. Human autoantibody to a novel protein of the nuclear coiled body: Immunological characterization and cDNA cloning of p80-coilin. Journal of Experimental Medicine. 1991;173(6):1407–1419. doi: 10.1084/jem.173.6.1407. PubMed DOI PMC

Matera A. G. Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends in Cell Biology. 1999;9(8):302–309. doi: 10.1016/s0962-8924(99)01606-2. PubMed DOI

Rosowski K. A., Mertz A. F., Norcross S., Dufresne E. R., Horsley V. Edges of human embryonic stem cell colonies display distinct mechanical properties and differentiation potential. Scientific Reports. 2015;5 doi: 10.1038/srep14218.14218 PubMed DOI PMC

Butler J. T., Hall L. L., Smith K. P., Lawrence J. B. Changing nuclear landscape and unique PML structures during early epigenetic transitions of human embryonic stem cells. Journal of Cellular Biochemistry. 2009;107(4):609–614. doi: 10.1002/jcb.22183. PubMed DOI PMC

Bernardi R., Pandolfi P. P. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nature Reviews Molecular Cell Biology. 2007;8(12):1006–1016. doi: 10.1038/nrm2277. PubMed DOI

Dundr M., Misteli T. Biogenesis of nuclear bodies. Cold Spring Harbor perspectives in biology. 2010;2(12):p. a000711. PubMed PMC

Handwerger K. E., Gall J. G. Subnuclear organelles: new insights into form and function. Trends in Cell Biology. 2006;16(1):19–26. doi: 10.1016/j.tcb.2005.11.005. PubMed DOI

Lamond A. I., Spector D. L. Nuclear speckles: a model for nuclear organelles. Nature Reviews Molecular Cell Biology. 2003;4(8):605–612. doi: 10.1038/nrm1172. PubMed DOI

Misteli T. The concept of self-organization in cellular architecture. Journal of Cell Biology. 2001;155(2):181–185. doi: 10.1083/jcb.200108110. PubMed DOI PMC

Misteli T. Beyond the sequence: cellular organization of genome function. Cell. 2007;128(4):787–800. doi: 10.1016/j.cell.2007.01.028. PubMed DOI

Pederson T., Tsai R. Y. L. In search of nonribosomal nucleolar protein function and regulation. Journal of Cell Biology. 2009;184(6):771–776. doi: 10.1083/jcb.200812014. PubMed DOI PMC

Zupkovitz G., Grausenburger R., Brunmeir R., et al. The cyclin-dependent kinase inhibitor p21 is a crucial target for histone deacetylase 1 as a regulator of cellular proliferation. Molecular and Cellular Biology. 2010;30(5):1171–1181. doi: 10.1128/MCB.01500-09. PubMed DOI PMC

Franek M., Legartová S., Suchánková J., et al. CARM1 modulators affect epigenome of stem cells and change morphology of nucleoli. Physiological Research. 2015;64(5):769–782. PubMed

Pacherník J., Ešner M., Bryja V., Dvořák P., Hampl A. Neural differentiation of mouse embryonic stem cells grown in monolayer. Reproduction Nutrition Development. 2002;42(4):317–326. doi: 10.1051/rnd:2002028. PubMed DOI

Suchánková J., Kozubek S., Legartová S., Sehnalová P., Küntziger T., Bártová E. Distinct kinetics of DNA repair protein accumulation at DNA lesions and cell cycle-dependent formation of γH2AX- and NBS1-positive repair foci. Biology of the Cell. 2015;107(12):440–454. doi: 10.1111/boc.201500050. PubMed DOI

Bártová E., Večeřa J., Krejčí J., Legartová S., Pacherník J., Kozubek S. The level and distribution pattern of HP1β in the embryonic brain correspond to those of H3K9me1/me2 but not of H3K9me3. Histochemistry and Cell Biology. 2016;145(4):447–461. doi: 10.1007/s00418-015-1402-7. PubMed DOI

Krejčí J., Harničarová A., Kůrová J., et al. Nuclear organization of PML bodies in leukaemic and multiple myeloma cells. Leukemia Research. 2008;32(12):1866–1877. doi: 10.1016/j.leukres.2008.04.021. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...