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Chromatin Fractal Organization, Textural Patterns, and Circularity of Nuclear Envelope in Adrenal Zona Fasciculata Cells

Published online by Cambridge University Press:  08 November 2016

Igor Pantic Open the ORCID record for Igor Pantic [Opens in a new window] ,
Dejan Nesic ,
Milos Basailovic ,
Mila Cetkovic ,
Sanja Mazic ,
Jelena Suzic-Lazic  and
Martin Popevic
Igor Pantic*
Affiliation:
Laboratory for Cellular Physiology, School of Medicine, Institute of Medical physiology, University of Belgrade, Visegradska 26/II, RS-11129 Belgrade, Serbia
Dejan Nesic
Affiliation:
School of Medicine, Institute of Medical physiology, University of Belgrade, Visegradska 26/II, RS-11129 Belgrade, Serbia
Milos Basailovic
Affiliation:
School of Medicine, University of Belgrade, Visegradska 26/II, RS-11129 Belgrade, Serbia
Mila Cetkovic
Affiliation:
School of Medicine, Institute of Histology and Embryology, University of Belgrade, Visegradska 26/II, RS-11129 Belgrade, Serbia
Sanja Mazic
Affiliation:
School of Medicine, Institute of Medical physiology, University of Belgrade, Visegradska 26/II, RS-11129 Belgrade, Serbia
Jelena Suzic-Lazic
Affiliation:
School of Medicine, University Clinical Centre “Dr Dragiša Mišović - Dedinje”, University of Belgrade, Heroja Milana Tepica 1, 11000 Belgrade, Serbia
Martin Popevic
Affiliation:
School of Medicine, Serbian Institute for Occupational Health, University of Belgrade, Deligradska 29, 11000 Belgrade, Serbia
*
*Corresponding author. [email protected]
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Abstract

Despite previous research efforts in the fields of histology and cell physiology, the relationship between chromatin structural organization and nuclear shape remains unclear. The aim of this research was to test the existence and strength of correlations between mathematical parameters of chromatin microarchitecture and roundness of the nuclear envelope. On a sample of 240 nuclei of adrenal zona fasciculata cells stained using the DNA-specific Feulgen method, we quantified fractal parameters such as fractal dimension and lacunarity, as well as textural parameters such as angular second moment (ASM), entropy, inverse difference moment, contrast, and variance. Circularity of the nuclear envelope was determined from the nuclear area and perimeter. The results indicate that there is a statistically significant negative correlation between chromatin ASM and circularity. Moreover, there was a statistically significant positive correlation between chromatin fractal dimension and envelope circularity. This is the first study to demonstrate these relationships in adrenal tissue, and also one of the first studies to test the connection between circularity and fractal and gray-level co-occurrence matrix parameters in DNA-specific Feulgen stain. The results could be useful both as an addition to the current knowledge on chromatin/nuclear envelope interactions, and for design of future computer-assisted research software for evaluation of nuclear morphology.

Keywords

nucleusshapestructurechromatinmicroscopy
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 6 , December 2016 , pp. 1120 - 1127
Copyright
© Microscopy Society of America 2016 

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References

Bancaud, A., Lavelle, C., Huet, S. & Ellenberg, J. (2012). A fractal model for nuclear organization: Current evidence and biological implications. Nucleic Acids Res 40(18), 8783–8792.Google Scholar
Bedin, V., Adam, R.L., de Sa, B.C., Landman, G. & Metze, K. (2010). Fractal dimension of chromatin is an independent prognostic factor for survival in melanoma. BMC Cancer 10, 260.Google Scholar
Biesterfeld, S., Beckers, S., Del Carmen Villa Cadenas, M. & Schramm, M. (2011). Feulgen staining remains the gold standard for precise DNA image cytometry. Anticancer Res 31(1), 53–58.Google Scholar
Ferro, D.P., Falconi, M.A., Adam, R.L., Ortega, M.M., Lima, C.P., de Souza, C.A., Lorand-Metze, I. & Metze, K. (2011). Fractal characteristics of May-Grunwald-Giemsa stained chromatin are independent prognostic factors for survival in multiple myeloma. PLoS One 6(6), e20706.CrossRefGoogle ScholarPubMed
Fetit, A.E., Novak, J., Peet, A.C. & Arvanitis, T.N. (2014). 3D texture analysis of MR images to improve classification of paediatric brain tumours: A preliminary study. Stud Health Technol Inform 202, 213–216.Google Scholar
Haralick, R.S., Shanmugam, K. & Dinstein, I. (1973). Textural features for image classification. IEEE Trans Syst Man Cybern SMC-3, 610–621.Google Scholar
Joseph, G.B., Baum, T., Carballido-Gamio, J., Nardo, L., Virayavanich, W., Alizai, H., Lynch, J.A., McCulloch, C.E., Majumdar, S. & Link, T.M. (2011). Texture analysis of cartilage T2 maps: Individuals with risk factors for OA have higher and more heterogeneous knee cartilage MR T2 compared to normal controls—Data from the osteoarthritis initiative. Arthritis Res Ther 13(5), R153.CrossRefGoogle ScholarPubMed
Karperien, A. (1999–2014). FracLac for ImageJ. Available at http://rsb.info.nih.gov/ij/plugins/fraclac/FLHelp/Introduction.htm (retrieved May 22, 2016).Google Scholar
Kubben, N., Voncken, J.W. & Misteli, T. (2010). Mapping of protein- and chromatin-interactions at the nuclear lamina. Nucleus 1(6), 460–471.Google Scholar
Loizou, C.P., Petroudi, S., Seimenis, I., Pantziaris, M. & Pattichis, C.S. (2015). Quantitative texture analysis of brain white matter lesions derived from T2-weighted MR images in MS patients with clinically isolated syndrome. J Neuroradiol 42(2), 99–114.CrossRefGoogle ScholarPubMed
Lopes, R. & Betrouni, N. (2009). Fractal and multifractal analysis: A review. Med Image Anal 13(4), 634–649.Google Scholar
Losa, G.A. & Castelli, C. (2005). Nuclear patterns of human breast cancer cells during apoptosis: Characterisation by fractal dimension and co-occurrence matrix statistics. Cell Tissue Res 322(2), 257–267.Google Scholar
Maani, R., Kalra, S. & Yang, Y.H. (2014). Robust volumetric texture classification of magnetic resonance images of the brain using local frequency descriptor. IEEE Trans Image Process 23(10), 4625–4636.Google Scholar
Mandelbrot, B.B. (1977). The Fractal Geometry of Nature. NY: W.H. Freeman. 468 pp.Google Scholar
Mattout-Drubezki, A. & Gruenbaum, Y. (2003). Dynamic interactions of nuclear lamina proteins with chromatin and transcriptional machinery. Cell Mol Life Sci 60(10), 2053–2063.Google Scholar
McNally, J.G. & Mazza, D. (2010). Fractal geometry in the nucleus. EMBO J 29(1), 2–3.CrossRefGoogle ScholarPubMed
Metze, K. (2010). Fractal dimension of chromatin and cancer prognosis. Epigenomics 2(5), 601–604.CrossRefGoogle ScholarPubMed
Metze, K. (2013). Fractal dimension of chromatin: Potential molecular diagnostic applications for cancer prognosis. Expert Rev Mol Diagn 13(7), 719–735.Google Scholar
Mohanaiah, P., Sathyanarayana, P. & GuruKumar, L. (2003). Image texture feature extraction using GLCM approach. Int J Sci Res Publ 3(5), 1–5.Google Scholar
Nedelec, J.F., Yu, O., Chambron, J. & Macher, J.P. (2004). Texture analysis of the brain: From animal models to human applications. Dialogues Clin Neurosci 6(2), 227–233.Google Scholar
Nielsen, B., Albregtsen, F. & Danielsen, H.E. (2012). Automatic segmentation of cell nuclei in Feulgen-stained histological sections of prostate cancer and quantitative evaluation of segmentation results. Cytometry A 81(7), 588–601.CrossRefGoogle ScholarPubMed
Pantic, I., Basailovic, M., Paunovic, J. & Pantic, S. (2015). Relationship between chromatin complexity and nuclear envelope circularity in hippocampal pyramidal neurons. Chaos Solitons Fractals 76, 271–277.CrossRefGoogle Scholar
Pantic, I., Basta-Jovanovic, G., Starcevic, V., Paunovic, J., Suzic, S., Kojic, Z. & Pantic, S. (2013 a). Complexity reduction of chromatin architecture in macula densa cells during mouse postnatal development. Nephrology (Carlton) 18(2), 117–124.Google Scholar
Pantic, I., Harhaji-Trajkovic, L., Pantovic, A., Milosevic, N.T. & Trajkovic, V. (2012 a). Changes in fractal dimension and lacunarity as early markers of UV-induced apoptosis. J Theor Biol 303, 87–92.CrossRefGoogle ScholarPubMed
Pantic, I. & Pantic, S. (2012). Germinal center texture entropy as possible indicator of humoral immune response: Immunophysiology viewpoint. Mol Imaging Biol 14(5), 534–540.Google Scholar
Pantic, I., Pantic, S. & Basta-Jovanovic, G. (2012 b). Gray level co-occurrence matrix texture analysis of germinal center light zone lymphocyte nuclei: Physiology viewpoint with focus on apoptosis. Microsc Microanal 18(3), 470–475.CrossRefGoogle ScholarPubMed
Pantic, I., Pantic, S. & Paunovic, J. (2012 c). Aging increases nuclear chromatin entropy of erythroid precursor cells in mice spleen hematopoietic tissue. Microsc Microanal 18(5), 1054–1059.CrossRefGoogle ScholarPubMed
Pantic, I., Pantic, S., Paunovic, J. & Perovic, M. (2013 b). Nuclear entropy, angular second moment, variance and texture correlation of thymus cortical and medullar lymphocytes: Grey level co-occurrence matrix analysis. An Acad Bras Cienc 85(3), 1063–1072.CrossRefGoogle ScholarPubMed
Pantic, I., Paunovic, J., Perovic, M., Cattani, C., Pantic, S., Suzic, S., Nesic, D. & Basta-Jovanovic, G. (2013 c). Time-dependent reduction of structural complexity of the buccal epithelial cell nuclei after treatment with silver nanoparticles. J Microsc 252(3), 286–294.CrossRefGoogle ScholarPubMed
Schreiner, S.M., Koo, P.K., Zhao, Y., Mochrie, S.G. & King, M.C. (2015). The tethering of chromatin to the nuclear envelope supports nuclear mechanics. Nat Commun 6, 7159.Google Scholar
Song, C.I., Ryu, C.H., Choi, S.H., Roh, J.L., Nam, S.Y. & Kim, S.Y. (2013). Quantitative evaluation of vocal-fold mucosal irregularities using GLCM-based texture analysis. Laryngoscope 123(11), E45–E50.Google Scholar
Zullo, J.M., Demarco, I.A., Pique-Regi, R., Gaffney, D.J., Epstein, C.B., Spooner, C.J., Luperchio, T.R., Bernstein, B.E., Pritchard, J.K., Reddy, K.L. & Singh, H. (2012). DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149(7), 1474–1487.Google Scholar