Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-24T06:19:19.907Z Has data issue: false hasContentIssue false
  • English
  • Français

Aging Increases Nuclear Chromatin Entropy of Erythroid Precursor Cells in Mice Spleen Hematopoietic Tissue

Published online by Cambridge University Press:  12 October 2012

Igor Pantic ,
Senka Pantic  and
Jovana Paunovic
Igor Pantic*
Affiliation:
Institute of Medical Physiology, Faculty of Medicine, University of Belgrade, Visegradska 26/II, 11000 Belgrade, Serbia
Senka Pantic
Affiliation:
Institute of Histology and Embryology, Faculty of Medicine, University of Belgrade, Visegradska 26/II, 11000 Belgrade, Serbia
Jovana Paunovic
Affiliation:
Institute of Histology and Embryology, Faculty of Medicine, University of Belgrade, Visegradska 26/II, 11000 Belgrade, Serbia
*
*Corresponding author. E-mail: [email protected], [email protected]
Get access

Abstract

Despite recent advances in hematopoietic tissue research, effects of aging on hematopoietic erythroid precursor (EP) cells are unclear. In this article we present results suggesting that chromatin textural entropy of EP cells in mouse spleen increases with age, while chromatin homogeneity decreases. The experiment was conducted on a total of 32 male Swiss white mice. Spleen tissue was acquired from four age groups: 10 days, 1 month, 4 months, and 7 months old mice. A total of 640 randomly selected, nonoverlapping EP cell nuclei (20 per animal) were analyzed using the gray level co-occurrence matrix method. There was statistically highly significant difference between the age groups, both in chromatin entropy (ANOVA, F = 12.99, p < 0.0001) and in homogeneity (ANOVA, F = 7.05, p < 0.001). When the individual groups were compared (ANOVA post hoc test), statistical difference was detected in all group pairs, except between the animals 4 months and 7 months old, either in chromatin entropy or homogeneity. The detected increase of chromatin disorder in mouse juvenile period/early adulthood suggests that cell intrinsic factors such as epigenetic dysregulation and DNA damage accumulation may have an important role in EP cell aging.

Keywords

gray level co-occurrence matrix (GLCM)chromatinheterogeneityinverse difference momentintrinsicheterochromatin
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 18 , Issue 5 , October 2012 , pp. 1054 - 1059
Copyright
Copyright © Microscopy Society of America 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bancaud, A., Huet, S., Daigle, N., Mozziconacci, J., Beaudouin, J. & Ellenberg, J. (2009). Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J 28, 3785–3798.Google Scholar
Boggs, D.R. & Patrene, K.D. (1985). Hematopoiesis and aging III: Anemia and a blunted erythropoietic response to hemorrhage in aged mice. Am J Hematol 19, 327–338.Google Scholar
Cesta, M.F. (2006). Normal structure, function, and histology of the spleen. Toxicol Pathol 34, 455–465.Google Scholar
Chambers, S.M., Shaw, C.A., Gatza, C., Fisk, C.J., Donehower, L.A. & Goodell, M.A. (2007). Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol 5, e201. Google Scholar
Crooks, G.E. (2007). Beyond Boltzmann-Gibbs statistics: Maximum entropy hyperensembles out of equilibrium. Phys Rev E 75, 041119. Google Scholar
De Haan, G. & Gerrits, A. (2007). Epigenetic control of hematopoietic stem cell aging the case of Ezh2. Ann NY Acad Sci 1106, 233–239.Google Scholar
Ergen, A.V. & Goodell, M.A. (2010). Mechanisms of hematopoietic stem cell aging. Exp Gerontol 45, 286–290.Google Scholar
Fox, J.G. (2007). The Mouse in Biomedical Research, pp. 162–163. London: Academic Press.Google Scholar
Gorban, A.N., Karlin, I.V. & Ottinger, H.C. (2003). Additive generalization of the Boltzmann entropy. Phys Rev E 67, 067104. Google Scholar
Guo, Y., Lübbert, M. & Engelhardt, M. (2003). CD34-hematopoietic stem cells: Current concepts and controversies. Stem Cells 21, 15–20.CrossRefGoogle Scholar
Haralick, R., Shanmugam, K. & Dinstein, I. (1973). Textural features for image classification. IEEE Trans Syst Man Cybern SMC-3, 610–621.Google Scholar
Kohler, A., Schmithorst, V., Filippi, M.D., Ryan, M.A., Daria, D., Gunzer, M. & Geiger, H. (2009). Altered cellular dynamics and endosteal location of aged early hematopoietic progenitor cells revealed by time-lapse intravital imaging in long bones. Blood 114, 290–298.Google Scholar
Lebedev, D.V., Filatov, M.V., Kuklin, A.I., Islamov, A.Kh., Kentzinger, E., Pantina, R., Toperverg, B.P. & Isaev-Ivanov, V.V. (2005). Fractal nature of chromatin organization in interphase chicken erythrocyte nuclei: DNA structure exhibits biphasic fractal properties. FEBS Lett 579, 1465–1468.CrossRefGoogle ScholarPubMed
Metze, K. (2010). Fractal dimension of chromatin and cancer prognosis. Epigenomics 2, 601–604.CrossRefGoogle ScholarPubMed
Muller-Sieburg, C.E., Cho, R.H., Thoman, M., Adkins, B. & Sieburg, H.B. (2002). Deterministic regulation of haematopoietic stem cell self-renewal and differentiation. Blood 100, 1302–1309.Google Scholar
NIH. (1985). Guide for the Care and Use of Laboratory Animals. NIH Publication No. 85-23. Bethesda MD: U.S. National Institutes of Health. Google Scholar
Pantic, I. & Pantic, S. (2011). Germinal center texture entropy as possible indicator of humoral immune response: Immunophysiology viewpoint. Mol Imaging Biol doi: 10.1007/s11307-011-0531-1.Google Scholar
Pantic, I., Pantic, S. & Basta-Jovanovic, G. (2012). Gray level co-occurrence matrix (GLCM) texture analysis of germinal center light zone lymphocyte nuclei: Physiology viewpoint with focus on apoptosis. Microsc Microanal 18(3), 470–475.Google Scholar
Rossi, D.J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J. & Weissman, I.L. (2007). Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447, 725–729.Google Scholar
Rossi, D.J., Bryder, D., Zahn, J.M., Ahlenius, H., Sonu, R., Wagers, A.J. & Weissman, I.L. (2005). Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 102, 9194–9199.Google Scholar
Rube, C.E., Fricke, A., Widmann, T.A., Furst, T., Madry, H., Pfreundschuh, M. & Rube, C. (2011). Accumulation of DNA damage in hematopoietic stem and progenitor cells during human aging. PLoS 6, e17487. Google Scholar
Saitoh, T., Morimoto, K., Kumagai, T., Tsuboi, I., Aikawa, S. & Horie, T. (1999). Comparison of erythropoietic response to androgen in young and old senescence accelerated mice. Mech Ageing Dev 109, 125–139.Google Scholar
Suttie, A.W. (2006). Histopathology of the spleen. Toxicol Pathol 34, 466–503.Google Scholar
Tsuboi, I., Morimoto, K., Horie, T. & Mori, K.J. (1991). Age-related changes in various hemopoietic progenitor cells in senescence accelerated (SAM-P) mice. Exp Hematol 19, 874–877.Google ScholarPubMed
University of Belgrade (n.d.). Guidelines for the Work with Experimental Animals. University of Belgrade, Faculty of Medicine. Available at wwwold.med.bg.ac.rs/?sid=820 (accessed February 22, 2012).Google Scholar
Wagner, W., Horn, P., Bork, S. & Ho, A.D. (2008). Aging of hematopoietic stem cells is regulated by the stem cell niche. Exp Gerontol 43, 974–980.Google Scholar
Wilson, A., Laurenti, E. & Trumpp, A. (2009). Balancing dormant and self-renewing hematopoietic stem cells. Curr Opin Genet Dev 19, 461–468.Google Scholar
Woolthuis, C.M., de Haan, G. & Huls, G. (2011). Aging of hematopoietic stem cells: Intrinsic changes or micro-environmental effects? Curr Opin Immunol 23, 512–517.Google Scholar
Xing, Z., Ryan, M.A., Daria, D., Nattamai, K.J., Van Zant, G., Wang, L., Zheng, Y. & Geiger, H. (2006). Increased hematopoietic stem cell mobilization in aged mice. Blood 108, 2190–2197.Google Scholar