Abstract—
This work was aimed at studying the structural organization of nucleolus and constitutive heterochromatin in different types of tanycytes during postnatal development and aging of rats. The distribution of nucleolus argentophilic proteins (nucleolin and nucleophosmin) and heterochromatin aggregates in tanycytes at various stages of postnatal development have been described for the first time using immunohistochemical methods and confocal laser microscopy. The heterogeneity of the size and number of nucleoli was demonstrated both in different tanycytes subpopulations and at different ages of an animal. This may indicate different levels of the tanycyte synthetic activity and the ability to proliferate during early postnatal development and aging. During aging, the distribution of heterochromatin aggregates varies among tanycyte subpopulations: α-tanycytes undergo intense heterochromatization, while β-tanycytes are characterized by a stable organization of the studied compartments of the cell nucleus. The data obtained significantly supplement the modern understanding of organization of the structure of the cell nucleus of tanycytes during normal development and aging. This can subsequently serve as a basis for establishing the role of these subnuclear structures in pathological processes.
Similar content being viewed by others
REFERENCES
Prevot V., Dehouck B., Sharif A., Ciofi P., Giacobini P., Clasadonte J. 2018. The versatile tanycyte: A hypothalamic integrator of reproduction and energy metabolism. Endocr. Rev. 39 (3), 333–368.
Rodríguez E., Guerra M., Peruzzo B., Blázquez J.L. 2019. Tanycytes: A rich morphological history to underpin future molecular and physiological investigations. J. Neuroendocrinol. 31 (3), e12690.
Parlato R., Kreiner G. 2013. Nucleolar activity in neurodegenerative diseases: A missing piece of the puzzle? J. Mol. Med (Berl.). 91 (5), 541–547.
Parlato R., Bierhoff H. 2015. Role of nucleolar dysfunction in neurodegenerative disorders: A game of genes? AIMS Mol. Sci. 2 (3), 211–224.
Yang K., Yang J., Yi J. 2018. Nucleolar stress: Hallmarks, sensing mechanism and diseases. Cell Stress. 2 (6), 125–140.
Kourmouli N., Jeppesen P., Mahadevhaiah S., Burgoyne P., Wu R., Gilbert D.M., Bongiorni S., Prantera G., Fanti L., Pimpinelli S., Shi W, Fundele R., Singh P.B. 2004. Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J. Cell. Sci. 117 (Pt 12), 2491–501.
Wang Z., Zang C., Rosenfeld J.A., Schones D.E., Barski A., Cuddapah S., Cui K., Roh T.Y., Peng W., Zhang M.Q., Zhao K. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40 (7), 897–903.
Schotta G., Lachner M., Sarma K., Ebert A., Sengupta R., Reuter G., Reinberg D., Jenuwein T. 2004. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18 (11), 1251–1262.
Fraga M.F., Ballestar E., Villar-Garea A., Boix-Chornet M., Espada J., Schotta G., Bonaldi T., Haydon C., Ropero S., Petrie K., Iyer N.G., Pérez-Rosado A., Calvo E., Lopez J.A., Cano A., Calasanz M.J., Colomer D., Piris M.A., Ahn N., Imhof A., Caldas C., Jenuwein T., Esteller M.2005. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 37, 391–400.
Korzhevskii D.E., Sukhorukova E.G., Kirik O.V., Grigorev I.P. 2015. Immunohistochemical demonstration of specific antigens in the human brain fixed in zinc-ethanol-formaldehyde. Eur. J. Histochem. 59 (3), 2530.
Paxinos G., Watson C. 2007. The rat brain in stereotaxic coordinates. 6th edition. New York: Elsevier/Academic Press.
Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. 2012. Fiji: An open-source platform for biological-image analysis. Nat. Meth. 9 (7), 676–682.
Berciano M.T., Villagrá N.T., Pena E., Navascués J., Casafont I., Lafarga M. 2002. Structural and functional compartmentalization of the cell nucleus in supraoptic neurons. Microsc. Res. Tech. 56 (2), 132–142.
Pleshakova I., Gusel’nikova V., Sufieva D., Korzhevskii D. 2018. The distribution of the nucleophosmin (B23) and histone H4K20me3 in the granule cells of the rat cerebellar cortex. Tsitologiya (Rus.). 60, 632–638.
Cohen S., Greenberg M.E. 2008. Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev. Cell Dev. Biol. 24, 183–209.
Sufieva D.A., Kirik O.V., Korzhevskii D.E. 2018. Nucleolin and nucleoli in ependymocytes and tanycytes of the third ventricle of the rat brain. Cell Tiss. Biol. 12, 167–173.
Pena E., Berciano M.T., Fernandez R., Ojeda J.L., Lafarga M. 2001. Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J. Comp. Neurol. 430 (2), 250–263.
Zharskaya O.O., Zatsepina O.V. 2007. Dynamics and mechanisms of reorganization of the nucleolus in mitosis. Tsitologiya (Rus.). 49 (5), 355–369.
Watanabe-Susaki K., Takada H., Enomoto K., Miwata K., Ishimine H., Intoh A., Ohtaka M., Nakanishi M., Sugino H., Asashima M., Kurisaki A. 2014. Biosynthesis of ribosomal RNA in nucleoli regulates pluripotency and differentiation ability of pluripotent stem cells. Stem Cells. 32 (12), 3099–3111.
Tajrishi M.M., Tuteja R., Tuteja N. 2011. Nucleolin: The most abundant multifunctional phosphoprotein of nucleolus. Commun. Integr. Biol. 4 (3), 267–275.
Feric M., Vaidya N., Harmon T.S., Mitrea D.M., Zhu L., Richardson T.M., Kriwacki R.W., Pappu R.V., Brangwynne C.P. 2016. Coexisting liquid phases underlie nucleolar subcompartments. Cell. 165 (7), 1686–1697.
Ginisty H., Sicard H., Roger B., Bouvet P. 1999. Structure and functions of nucleolin. J. Cell. Sci. 112 (Pt. 6), 761–772.
Lindström M.S. 2011. NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem. Res. Int. 2011, 195209.
Colombo E., Alcalay M., Pelicci P. 2011. Nucleophosmin and its complex network: A possible therapeutic target in hematological diseases. Oncogene. 30, 2595–2609.
Guselnikova V.V., Sufieva D.A., Korzhevsky D.E. 2020. Nucleophosmin, coilin, and argentophilic (AgNOR) proteins in the neurons of human substantia nigra. Cell Tiss. Biol. 14, 380–387.
Jia W., Yao Z., Zhao J., Guan Q., Gao L. 2017. New perspectives of physiological and pathological functions of nucleolin (NCL). Life Sci. 186, 1–10.
Ugrinova I., Petrova M., Chalabi-Dchar M., Bouvet P. 2018. Multifaceted nucleolin protein and its molecular partners in oncogenesis. Adv. Protein Chem. Struct. Biol. 111, 133–164.
Vladimirova N.M., Potapenko N.A., Surina E.A., Volpina O.M. 2014. Peculiarities of structural status of protein B23/nucleophosmin in brain cells. Biol. membrany (Rus.). 31 (1), 57–67.
Wang J., Jia S.T., Jia S. 2016. New insights into the regulation of heterochromatin. Trends Genet. 32 (5), 284–294.
Lee J.H., Kim E.W., Croteau D.L., Bohr V.A. 2020. Heterochromatin: An epigenetic point of view in aging. Exp. Mol. Med. 52, 1466–1474.
Lezhava T. 2001. Chromosome and aging: Genetic conception of aging. Biogerontology. 2 (4), 253–260.
Frehlick L.J., Eirín-López J.M., Ausió J. 2007. New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays. 29 (1), 49–59.
Lafarga M., Berciano M.T., Hervas J.P., Villegas J. 1989. Nucleolar organization in granule cell neurons of the rat cerebellum. J. Neurocytol. 18 (1), 19–26.
ACKNOWLEDGMENTS
The work was supported by the State Assignment for the Institute of Experimental Medicine. The images were obtained at the Human Microbiome Center for Collective Use of Scientific Equipment of the Institute of Experimental Medicine.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest.
All procedures were performed in accordance with the European Communities Council Directive (November 24, 1986; 86/609/EEC) and the Declaration on humane treatment of animals. The protocol of experiments was approved by the Commission on Bioethics of the Institute of Experimental Medicine.
Additional information
Translated by E. Makeeva
Rights and permissions
About this article
Cite this article
Sufieva, D.A., Pleshakova, I.M. & Korzhevskii, D.E. Structural Characteristic of Nucleolus and Heterochromatin Aggregates of Rat Brain Tanycytes. Biochem. Moscow Suppl. Ser. A 15, 319–328 (2021). https://doi.org/10.1134/S199074782105007X
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S199074782105007X