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Effects of Iron Oxide Nanoparticles on Structural Organization of Hepatocyte Chromatin: Gray Level Co-occurrence Matrix Analysis

Published online by Cambridge University Press:  27 May 2021

Jovana Paunovic
Affiliation:
Faculty of Medicine, Institute of Pathological Physiology, University of Belgrade, Dr Subotica 9, RS-11129, Belgrade, Serbia
Danijela Vucevic
Affiliation:
Faculty of Medicine, Institute of Pathological Physiology, University of Belgrade, Dr Subotica 9, RS-11129, Belgrade, Serbia
Tatjana Radosavljevic
Affiliation:
Faculty of Medicine, Institute of Pathological Physiology, University of Belgrade, Dr Subotica 9, RS-11129, Belgrade, Serbia
Biserka Vukomanovic Djurdjevic
Affiliation:
Faculty of Medicine, Military Medical Academy, Institute for Pathology, Crnotravska 17, RS-11000, Belgrade, Serbia
Sanja Stankovic
Affiliation:
Centre of Medical Biochemistry, Clinical Centre of Serbia, Visegradska 26, RS-11129, Belgrade, Serbia
Igor Pantic*
Affiliation:
Faculty of Medicine, Institute of Medical Physiology, University of Belgrade, Visegradska 26/II, RS-11129, Belgrade, Serbia University of Haifa, 199 Abba Hushi Blvd. Mount Carmel, HaifaIL-3498838, Israel
*
*Author for correspondence: Igor Pantic, E-mail: [email protected], [email protected]
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Abstract

Gray level co-occurrence matrix (GLCM) analysis is a contemporary and innovative computer-based algorithm that can be used for the quantification of subtle changes in a cellular structure. In this work, we use this method for the detection of discrete alterations in hepatocyte chromatin distribution after in vivo exposure to iron oxide nanoparticles (IONPs). The study was performed on 40 male, healthy C57BL/6 mice divided into four groups: three experimental groups that received different doses of IONPs and 1 control group. We describe the dose-dependent reduction of chromatin textural uniformity measured as GLCM angular second moment. Similar changes were detected for chromatin textural uniformity expressed as the value of inverse difference moment. To the best of our knowledge, this is the first study to investigate the impact of iron-based nanomaterials on hepatocyte GLCM parameters. Also, this is the first study to apply discrete wavelet transform analysis, as a supplementary method to GLCM, for the assessment of hepatocyte chromatin structure in these conditions. The results may present the useful basis for future research on the application of GLCM and DWT methods in pathology and other medical research areas.

Type
Biological Applications
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Abakumov, MA, Semkina, AS, Skorikov, AS, Vishnevskiy, DA, Ivanova, AV, Mironova, E, Davydova, GA, Majouga, AG & Chekhonin, VP (2018). Toxicity of iron oxide nanoparticles: Size and coating effects. J Biochem Mol Toxicol 32(12), e22225.CrossRefGoogle ScholarPubMed
Alcantara, D, Lopez, S, Garcia-Martin, ML & Pozo, D (2016). Iron oxide nanoparticles as magnetic relaxation switching (MRSw) sensors: Current applications in nanomedicine. Nanomedicine 12(5), 12531262.CrossRefGoogle ScholarPubMed
AlKubeyyer, A, Ben Ismail, MM, Bchir, O & Alkubeyyer, M (2020). Automatic detection of the meningioma tumor firmness in MRI images. J Xray Sci Technol 28(4), 659682.Google ScholarPubMed
Arias, LS, Pessan, JP, Vieira, APM, Lima, TMT, Delbem, ACB & Monteiro, DR (2018). Iron oxide nanoparticles for biomedical applications: A perspective on synthesis, drugs, antimicrobial activity, and toxicity. Antibiotics (Basel) 7(2), 46.CrossRefGoogle ScholarPubMed
Avci, D, Leblebicioglu, MK, Poyraz, M & Dogantekin, E (2014). A new method based on adaptive discrete wavelet entropy energy and neural network classifier (ADWEENN) for recognition of urine cells from microscopic images independent of rotation and scaling. J Med Syst 38(2), 7.CrossRefGoogle Scholar
Beletti, ME & Mello, ML (2004). Comparison between the toluidine blue stain and the feulgen reaction for evaluation of rabbit sperm chromatin condensation and their relationship with sperm morphology. Theriogenology 62(3–4), 398402.CrossRefGoogle ScholarPubMed
Cao, W, Li, J, Yang, K & Cao, D (2021). An overview of autophagy: Mechanism, regulation and research progress. Bull Cancer 108(3), 304322.CrossRefGoogle ScholarPubMed
Chen, X, Comish, PB, Tang, D & Kang, R (2021). Characteristics and biomarkers of ferroptosis. Front Cell Dev Biol 9, 637162.CrossRefGoogle ScholarPubMed
Chen, X, Wei, X, Zhang, Z, Yang, R, Zhu, Y & Jiang, X (2015). Differentiation of true-progression from pseudoprogression in glioblastoma treated with radiation therapy and concomitant temozolomide by GLCM texture analysis of conventional MRI. Clin Imaging 39(5), 775780.CrossRefGoogle ScholarPubMed
Comanescu, MV, Mocanu, MA, Anghelache, L, Marinescu, B, Dumitrache, F, Badoi, AD & Manda, G (2015). Toxicity of L-DOPA coated iron oxide nanoparticles in intraperitoneal delivery setting - Preliminary preclinical study. Rom J Morphol Embryol 56(2 Suppl), 691696.Google ScholarPubMed
de Toledo, LAS, Rosseto, HC & Bruschi, ML (2018). Iron oxide magnetic nanoparticles as antimicrobials for therapeutics. Pharm Dev Technol 23(4), 316323.CrossRefGoogle ScholarPubMed
Dhruv, B, Mittal, N & Modi, M (2019). Study of Haralick's and GLCM texture analysis on 3D medical images. Int J Neurosci 129(4), 350362.CrossRefGoogle ScholarPubMed
Dinali, R, Ebrahiminezhad, A, Manley-Harris, M, Ghasemi, Y & Berenjian, A (2017). Iron oxide nanoparticles in modern microbiology and biotechnology. Crit Rev Microbiol 43(4), 493507.CrossRefGoogle ScholarPubMed
Dincic, M, Todorovic, J, Nesovic Ostojic, J, Kovacevic, S, Dunderovic, D, Lopicic, S, Spasic, S, Radojevic-Skodric, S, Stanisavljevic, D & Ilic, AZ (2020). The fractal and GLCM textural parameters of chromatin may be potential biomarkers of papillary thyroid carcinoma in Hashimoto's thyroiditis specimens. Microsc Microanal 26(4), 717730.CrossRefGoogle ScholarPubMed
Easo, SL & Mohanan, PV (2016). Hepatotoxicity evaluation of dextran stabilized iron oxide nanoparticles in wistar rats. Int J Pharm 509(1–2), 2834.CrossRefGoogle ScholarPubMed
Elmore, S (2007). Apoptosis: A review of programmed cell death. Toxicol Pathol 35(4), 495516.CrossRefGoogle ScholarPubMed
Gonzalez-Moragas, L, Yu, SM, Benseny-Cases, N, Sturzenbaum, S, Roig, A & Laromaine, A (2017). Toxicogenomics of iron oxide nanoparticles in the nematode C. elegans. Nanotoxicology 11(5), 647657.CrossRefGoogle ScholarPubMed
Hopkins, LE, Laing, EA, Peake, JL, Uyeminami, D, Mack, SM, Li, X, Smiley-Jewell, S & Pinkerton, KE (2018). Repeated iron-soot exposure and nose-to-brain transport of inhaled ultrafine particles. Toxicol Pathol 46(1), 7584.CrossRefGoogle ScholarPubMed
Huang, X, Li, S & Gao, S (2018). Applying a modified wavelet shrinkage filter to improve cryo-electron microscopy imaging. J Comput Biol 25(9), 10501058.CrossRefGoogle ScholarPubMed
Jiao, K, Li, QJ, Sun, W & Wang, ZJ (2005). Voltammetric detection of the DNA interaction with toluidine blue. Electroanalysis 17(11), 9971002.CrossRefGoogle Scholar
Kanai, R, Ohshima, K, Ishii, K, Sonohara, M, Ishikawa, M, Yamaguchi, M, Ohtani, Y, Kobayashi, Y, Ota, H & Kimura, F (2020). Discriminant analysis and interpretation of nuclear chromatin distribution and coarseness using gray-level co-occurrence matrix features for lobular endocervical glandular hyperplasia. Diagn Cytopathol 48(8), 724735.CrossRefGoogle ScholarPubMed
Kazemipour, N, Nazifi, S, Poor, MHH, Esmailnezhad, Z, Najafabadi, RE & Esmaeili, A (2018). Hepatotoxicity and nephrotoxicity of quercetin, iron oxide nanoparticles, and quercetin conjugated with nanoparticles in rats. Comp Clin Pathol 27(6), 16211628.CrossRefGoogle Scholar
Kociołek, M, Materka, A, Strzelecki, M & Szczypinski, P (2001). Discrete wavelet transform-derived features for digital image texture analysis. In Proc. of International Conference on Signals and Electronic Systems, 18–21 September 2001, pp. 163–168.Google Scholar
Kouroumalis, E, Voumvouraki, A, Augoustaki, A & Samonakis, DN (2021). Autophagy in liver diseases. World J Hepatol 13(1), 665.CrossRefGoogle ScholarPubMed
Lee, HK, Kim, CH, Bhattacharjee, S, Park, HG, Prakash, D & Choi, HK (2020). A paradigm shift in nuclear chromatin interpretation: From qualitative intuitive recognition to quantitative texture analysis of breast cancer cell nuclei. Cytometry A.Google ScholarPubMed
Li, X, Guindani, M, Ng, CS & Hobbs, BP (2018). Spatial Bayesian modeling of GLCM with application to malignant lesion characterization. J Appl Stat 46(2), 230246.CrossRefGoogle ScholarPubMed
Mapayi, T, Viriri, S & Tapamo, JR (2015). Adaptive thresholding technique for retinal vessel segmentation based on GLCM-energy information. Comput Math Methods Med 2015, 597475.Google ScholarPubMed
Martinez Banderas, AI, Aires, A, Quintanilla, M, Holguin-Lerma, JA, Lozano-Pedraza, C, Teran, FJ, Moreno, J, Perez, JE, Ooi, BS, Ravasi, T, Merzaban, JS, Cortajarena, AL & Kosel, J (2019). Iron-based core-shell nanowires for combinatorial drug delivery, photothermal and magnetic therapy. ACS Appl Mater Interfaces 11(47), 4397643988.CrossRefGoogle ScholarPubMed
Nikolovski, D, Cumic, J & Pantic, I (2019). Application of gray level co-occurrence matrix algorithm for detection of discrete structural changes in cell nuclei after exposure to iron oxide nanoparticles and 6-hydroxydopamine. Microsc Microanal 25(4), 982988.CrossRefGoogle ScholarPubMed
Ou, X, Pan, W & Xiao, P (2014). In vivo skin capacitive imaging analysis by using grey level co-occurrence matrix (GLCM). Int J Pharm 460(1–2), 2832.CrossRefGoogle Scholar
Pantic, I, Dimitrijevic, D, Nesic, D & Petrovic, D (2016 a). Gray level co-occurrence matrix algorithm as pattern recognition biosensor for oxidopamine-induced changes in lymphocyte chromatin architecture. J Theor Biol 406, 124128.CrossRefGoogle ScholarPubMed
Pantic, I, Jeremic, R, Dacic, S, Pekovic, S, Pantic, S, Djelic, M, Vitic, Z, Brkic, P & Brodski, C (2020). Gray-level co-occurrence matrix analysis of granule neurons of the hippocampal dentate gyrus following cortical injury. Microsc Microanal 26(1), 166172.CrossRefGoogle ScholarPubMed
Pantic, I, Paunovic, J, Basta-Jovanovic, G, Perovic, M, Pantic, S & Milosevic, NT (2013). Age-related reduction of structural complexity in spleen hematopoietic tissue architecture in mice. Exp Gerontol 48(9), 926932.CrossRefGoogle ScholarPubMed
Pantic, I, Paunovic, J, Vucevic, D, Radosavljevic, T, Dugalic, S, Petkovic, A, Radojevic-Skodric, S & Pantic, S (2017). Postnatal developmental changes in fractal complexity of Giemsa-stained chromatin in mice spleen follicular cells. Microsc Microanal 23(5), 10241029.CrossRefGoogle ScholarPubMed
Pantic, I, Petrovic, D, Paunovic, J, Vucevic, D, Radosavljevic, T & Pantic, S (2016 b). Age-related reduction of chromatin fractal dimension in toluidine blue-stained hepatocytes. Mech Ageing Dev 157, 3034.CrossRefGoogle ScholarPubMed
Parivar, K, Malekvand Fard, F, Bayat, M, Alavian, SM & Motavaf, M (2016). Evaluation of iron oxide nanoparticles toxicity on liver cells of BALB/c rats. Iran Red Crescent Med J 18(1), e28939.CrossRefGoogle ScholarPubMed
Paunovic, J, Vucevic, D, Radosavljevic, T, Mandic-Rajcevic, S & Pantic, I (2020). Iron-based nanoparticles and their potential toxicity: Focus on oxidative stress and apoptosis. Chem Biol Interact 316, 108935.CrossRefGoogle ScholarPubMed
Paunovic, J, Vucevic, D, Radosavljevic, T, Pantic, S, Nikolovski, D & Pantic, I (2017). Effects of metallic nanoparticles on physiological liver functions. Rev Adv Mater Sci 49, 123128.Google Scholar
Paunovic, J, Vucevic, D, Radosavljevic, T, Pantic, S, Veskovic, M & Pantic, I (2019). Gray-level co-occurrence matrix analysis of chromatin architecture in periportal and perivenous hepatocytes. Histochem Cell Biol 151(1), 7583.CrossRefGoogle ScholarPubMed
Strzelecki, M, Szczypinski, P, Materka, A & Klepaczko, A (2013). A software tool for automatic classification and segmentation of 2D/3D medical images. Nucl Instrum Methods Phys Res A 702, 137140.CrossRefGoogle Scholar
Szczypinski, P, Strzelecki, M & Materka, A (2007). MaZda - A software for texture analysis. In Proc. of ISITC 2007, November 23–23, 2007, Republic of Korea. pp. 245–249.CrossRefGoogle Scholar
Szczypinski, P, Strzelecki, M, Materka, A & Klepaczko, A (2009). MaZda - A software package for image texture analysis. Comput Meth Prog Bio 94(1), 6676.CrossRefGoogle ScholarPubMed
Tan, J, Gao, Y, Liang, Z, Cao, W, Pomeroy, MJ, Huo, Y, Li, L, Barish, MA, Abbasi, AF & Pickhardt, PJ (2020). 3D-GLCM CNN: A 3-dimensional gray-level Co-occurrence matrix-based CNN model for polyp classification via CT colonography. IEEE Trans Med Imaging 39(6), 20132024.CrossRefGoogle ScholarPubMed
Tan, TC, Ritter, LJ, Whitty, A, Fernandez, RC, Moran, LJ, Robertson, SA, Thompson, JG & Brown, HM (2016). Gray level co-occurrence matrices (GLCM) to assess microstructural and textural changes in pre-implantation embryos. Mol Reprod Dev 83(8), 701713.CrossRefGoogle ScholarPubMed
Tang, D, Kang, R, Berghe, TV, Vandenabeele, P & Kroemer, G (2019). The molecular machinery of regulated cell death. Cell Res 29(5), 347364.CrossRefGoogle ScholarPubMed
Vidya, KS, Ng, EY, Acharya, UR, Chou, SM, Tan, RS & Ghista, DN (2015). Computer-aided diagnosis of myocardial infarction using ultrasound images with DWT, GLCM and HOS methods: A comparative study. Comput Biol Med 62, 8693.CrossRefGoogle ScholarPubMed
Yun, JW, Yoon, JH, Kang, BC, Cho, NH, Seok, SH, Min, SK, Min, JH, Che, JH & Kim, YK (2015). The toxicity and distribution of iron oxide-zinc oxide core-shell nanoparticles in C57BL/6 mice after repeated subcutaneous administration. J Appl Toxicol 35(6), 593602.CrossRefGoogle ScholarPubMed
Zheng, H, Jiang, J, Xu, S, Liu, W, Xie, Q, Cai, X, Zhang, J, Liu, S & Li, R (2021). Nanoparticle-induced ferroptosis: Detection methods, mechanisms and applications. Nanoscale 13(4), 22662285.CrossRefGoogle ScholarPubMed
Zhu, MT, Wang, Y, Feng, WY, Wang, B, Wang, M, Ouyang, H & Chai, ZF (2010). Oxidative stress and apoptosis induced by iron oxide nanoparticles in cultured human umbilical endothelial cells. J Nanosci Nanotechnol 10(12), 85848590.CrossRefGoogle ScholarPubMed