Hostname: page-component-6d856f89d9-8l2sj Total loading time: 0 Render date: 2024-07-16T06:57:52.151Z Has data issue: false hasContentIssue false
  • English
  • Français

Cellular Invasion and Matrix Degradation, a Different Type of Matrix-Degrading Cells in the Cartilage of Catfish (Clarias gariepinus) and Japanese Quail Embryos (Coturnix coturnix japonica)

Part of: Micrographia Collection

Published online by Cambridge University Press:  04 October 2019

Soha A. Soliman ,
Basma Mohamed Kamal  and
Hanan H. Abd-Elhafeez Open the ORCID record for Hanan H. Abd-Elhafeez [Opens in a new window]
Soha A. Soliman
Affiliation:
Department of Histology, Faculty of Veterinary Medicine, South Valley University, Qena, Egypt
Basma Mohamed Kamal
Affiliation:
Anatomy and Embryology Department, Faculty of Veterinary Medicine, Sadat-City University, Sadat City, Egypt
Hanan H. Abd-Elhafeez*
Affiliation:
Department of Anatomy, Embryology and Histology, Assiut University, Assiut, 71526, Egypt
*
*Author for correspondence: Hanan H. Abd-Elhafeez, E-mail: hhmmzz91@gmail.com
Get access

Abstract

We previously studied the phenomena of the mesenchymal cell-dependent mode of cartilage growth in quail and catfish. Thus, we selected the two cartilage models in which mesenchymal cells participate in their growth. In such models, cartilage degradation occurred to facilitate cellular invasion. The studies do not explain the nature of the cartilage degrading cells. The current study aims to explore the nature of the cartilage-degrading cells using transmission electron microscopy (TEM) and immunohistochemistry. Samples of cartilage have been isolated from the air-breathing organ of catfish and the cartilage of the prospective occipital bone of quail embryos. Samples have been processed for TEM and immunohistochemistry. We found that two different cell types are involved in cartilage degradation; the macrophage in the cartilage of catfish and mesenchymal cells in the cartilage of the quail. Areas of cellular invasion in both catfish cartilage and quail embryo cartilage had an immunological affinity for MMP-9. In catfish, cartilage-degrading cells had identical morphological features of macrophages, whereas in quail embryos, cartilage-degrading cells were mesenchymal-like cells which had cell processes rich in vesicles and expressed CD117. Further study should consider the role of macrophage and mesenchymal cells during cartilage degradation. This could be valuable to be applied to remove the defective cartilage matrix formed in osteoarthritic patients to improve cartilage repair strategies.

Keywords

c-kitcartilage degrading cellsmacrophagemesenchymal-like cellsMMP-9
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 25 , Issue 5 , October 2019 , pp. 1283 - 1292
Copyright
Copyright © Microscopy Society of America 2019 

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.)

Footnotes

The work is equally distributed between authors.

References

Abd-Elhafeez, HH & Soliman, SA (2016 a). New description of telocyte sheaths in the bovine uterine tube: An immunohistochemical and scanning microscopic study. Cells Tissues Organs 203(5), 295–315. doi: 10.1159/000452243.Google Scholar
Abd-Elhafeez, HH & Soliman, SA (2016 b). Origin of rodlet cells and mapping their distribution in ruby-red-fin shark (rainbow shark) Epalzeorhynchos frenatum (Teleostei: Cyprinidae): Light, immunohistochemistry and ultrastructure study. J Cytol Histol 7. doi: 10.4172/2157-7099.1000345.Google Scholar
Abdel-Maksoud, FM, Abd-Elhafeez, HH & Soliman, SA (2019). Morphological changes of telocytes in camel efferent ductules in response to seasonal variations during the reproductive cycle. Sci Rep 9(1), 4507.Google Scholar
Ahmed, YA, Soliman, SA & Kamel, G (2013). Histomorphological and morphometrical studies on endochondral ossification in the Japanese quail, PhD Thesis. Germany: LAP LAMBERT Academic Publishing; 284 pages.Google Scholar
Akkiraju, H & Nohe, A (2015). Role of chondrocytes in cartilage formation, progression of osteoarthritis and cartilage regeneration. J Dev Biol 3(4), 177–192.Google Scholar
An, YH & Martin, KL (2003). Handbook of Histology Methods for Bone and Cartilage. Charleston, USA: Springer Science & Business Media. Medical University of South Carolina.Google Scholar
Bijata, M, Labus, J, Guseva, D, Stawarski, M, Butzlaff, M, Dzwonek, J, Schneeberg, J, Bohm, K, Michaluk, P, Rusakov, DA, Dityatev, A, Wilczynski, G, Wlodarczyk, J & Ponimaskin, E (2017). Synaptic remodeling depends on signaling between serotonin receptors and the extracellular matrix. Cell Rep 19(9), 1767–1782.Google Scholar
Cawston, TE & Young, DA (2010). Proteinases involved in matrix turnover during cartilage and bone breakdown. Cell Tissue Res 339(1), 221–235.Google Scholar
Cole, AA & Cole, MB (1989). Are perivascular cells in cartilage canals chondrocytes? J Anat 165, 1–8.Google Scholar
Cox, TR & Erler, JT (2011). Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 4(2), 165–178.Google Scholar
Fatma El-Zahraa, AM & Abd-Elhafez, EA (2018). A histological, histochemical and ultrastructural characterization of uterine vessels at early stages of pregnancy. J Histol Histopathol Res 2(2), 41–47.Google Scholar
Ferrer-Ferrer, M & Dityatev, A (2018). Shaping synapses by the neural extracellular matrix. Front Neuroanat 12, 40.Google Scholar
Frevert, CW & Sannes, PL (2005). Matrix proteoglycans as effector molecules for epithelial cell function. Eur Respir Rev 14(97), 137–144.Google Scholar
Harris, HF (1900). On the rapid conversion of haematoxylin into haematein in staining reactions. J Appl Microsc Lab Methods 3(3), 777–780.Google Scholar
Hayami, T, Zhuo, Y, Wesolowski, GA, Pickarski, M & Duong, LT (2012). Inhibition of cathepsin K reduces cartilage degeneration in the anterior cruciate ligament transection rabbit and murine models of osteoarthritis. Bone 50(6), 1250–1259.Google Scholar
Hoff, RG, Newman, DE & Staneck, JL (1985). Bacteriuria screening by use of acridine orange-stained smears. J Clin Microbiol 21(4), 513–516.Google Scholar
Hohenester, E & Yurchenco, PD (2013). Laminins in basement membrane assembly. Cell Adh Migr 7(1), 56–63.Google Scholar
Hsiao, CT, Cheng, HW, Huang, CM, Li, HR, Ou, MH, Huang, JR, Khoo, KH, Yu, HW, Chen, YQ, Wang, YK, Chiou, A & Kuo, JC (2017). Fibronectin in cell adhesion and migration via N-glycosylation. Oncotarget 8(41), 70653–70668.Google Scholar
Hsu, SM, Raine, L & Fanger, H (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29, 577–580.Google Scholar
Janusz, MJ & Hare, M (1993). Cartilage degradation by cocultures of transformed macrophage and fibroblast cell lines. A model of metalloproteinase-mediated connective tissue degradation. J Immunol 150(5), 1922–1931.Google Scholar
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27, 137A–138A.Google Scholar
Kelwick, R, Desanlis, I, Wheeler, GN & Edwards, DR (2015). The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family. Genome Biol 16, 113.Google Scholar
Klaas, M, Kangur, T, Viil, J, Maemets-Allas, K, Minajeva, A, Vadi, K, Antsov, M, Lapidus, N, Jarvekulg, M & Jaks, V (2016). The alterations in the extracellular matrix composition guide the repair of damaged liver tissue. Sci Rep 6, 27398.Google Scholar
Loffek, S, Schilling, O & Franzke, CW (2011). Series “matrix metalloproteinases in lung health and disease”: Biological role of matrix metalloproteinases: A critical balance. Eur Respir J 38(1), 191–208.Google Scholar
Lu, P, Takai, K, Weaver, VM & Werb, Z (2011). Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 3, 12.Google Scholar
Maeda, N (2015). Proteoglycans and neuronal migration in the cerebral cortex during development and disease. Front Neurosci 9, 98.Google Scholar
Mandelin, J, Hukkanen, M, Li, TF, Korhonen, M, Liljestrom, M, Sillat, T, Hanemaaijer, R, Salo, J, Santavirta, S & Konttinen, YT (2006). Human osteoblasts produce cathepsin K. Bone 38(6), 769–777.Google Scholar
Melton, JT, Clarke, NM & Roach, HI (2006). Matrix metalloproteinase-9 induces the formation of cartilage canals in the chondroepiphysis of the neonatal rabbit. J Bone Joint Surg Am 88(Suppl 3), 155–161.Google Scholar
Miosge, N, Holzhausen, S, Zelent, C, Sprysch, P & Herken, R (2001). Nidogen-1 and nidogen-2 are found in basement membranes during human embryonic development. Histochem J 33(9–10), 523–530.Google Scholar
Mira, E, Lacalle, RA, Buesa, JM, de Buitrago, GG, Jimenez-Baranda, S, Gomez-Mouton, C, Martinez, AC & Manes, S (2004). Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J Cell Sci 117(Pt 9), 1847–1857.Google Scholar
Mizuguchi, S, Uyama, T, Kitagawa, H, Nomura, KH, Dejima, K, Gengyo-Ando, K, Mitani, S, Sugahara, K & Nomura, K (2003). Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 423, 443.Google Scholar
Otani, S, Kakinuma, S, Kamiya, A, Goto, F, Kaneko, S, Miyoshi, M, Tsunoda, T, Asano, Y, Kawai-Kitahata, F, Nitta, S, Nakata, T, Okamoto, R, Itsui, Y, Nakagawa, M, Azuma, S, Asahina, Y, Yamaguchi, T, Koshikawa, N, Seiki, M, Nakauchi, H & Watanabe, M (2016). Matrix metalloproteinase-14 mediates formation of bile ducts and hepatic maturation of fetal hepatic progenitor cells. Biochem Biophys Res Commun 469(4), 1062–1068.Google Scholar
Petrey, AC, Flanagan-Steet, H, Johnson, S, Fan, X, De la Rosa, M, Haskins, ME, Nairn, AV, Moremen, KW & Steet, R (2012). Excessive activity of cathepsin K is associated with cartilage defects in a zebrafish model of mucolipidosis II. Dis Model Mech 5(2), 177–190.Google Scholar
Reynolds, EG (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208–212.Google Scholar
Roughley, PJ (2006). The structure and function of cartilage proteoglycans, November 30th. doi: 10.22203 /eCM. v012a11.Google Scholar
Ruoslahti, E & Yamaguchi, Y (1991). Proteoglycans as modulators of growth factor activities. Cell 64(5), 867–869.Google Scholar
Sanchez, C, Bay-Jensen, AC, Pap, T, Dvir-Ginzberg, M, Quasnichka, H, Barrett-Jolley, R, Mobasheri, A & Henrotin, Y (2017). Chondrocyte secretome: A source of novel insights and exploratory biomarkers of osteoarthritis. Osteoarthr Cartilage 25(8), 1199–1209.Google Scholar
Seibel, MJ, Robins, SP & Bilezikian, JP (2006). Dynamics of Bone and Cartilage Metabolism: Principles and Clinical Applications, 2nd. USA: Academic Press, pp. 1–920.Google Scholar
Skouteris, GG & Nicolson, GL (1999). Intermolecular Cross-Talk in Tumor Metastasis, vol. 311 of NATO Science series: Life Science. Washington: IOS Press, 310 pp.Google Scholar
Soliman, AS & Abd-Elhafeez, HH (2018 a). Mesenchymal Cells in Cartilage Growth II, 2nd. Germany: Scholars' Press, Book.Google Scholar
Soliman, AS & Abd-Elhafeez, HH (2018 b). Organization and pattering of mesenchymal cells in quail embryonic cartilage. SciFed J Stem Cells 1, 1.Google Scholar
Soliman, AS, Ahmed, YA, Alghadrifi, S & Kamel, G (2017 b). An unusual step during endochondral bone formation: Mesenchymal stem-dependent cartilage growth at the onset of ossification. SciFed J Stem Cells 1, 1.Google Scholar
Soliman, S (2014). New aspect in cartilage growth “the invasive interstitial type”. J Aquaculture Res Dev 5, 253.Google Scholar
Soliman, S (2017). Potential role of telocytes in differentiation of embryonic skeletal progenitor cells. SciFed J Stem Cell 1(1) doi: 1000001.Google Scholar
Soliman, SA & Abd-Elhafeez, HH (2014). Mesenchymal Cells in Cartilage Growth, 1–49, First Edition. LAP LAMBERT Academic Publishing. ISBN: 978-3-65964843-4.Google Scholar
Soliman, SA & Abd-Elhafeez, HH (2016 a). Are C-KIT, MMP-9 and Type II collagen positive undifferentiated cells involved in cartilage growth? A description of unusual interstitial type of cartilage growth. J Cytol Histol 7, 440.Google Scholar
Soliman, SA & Abd-Elhafeez, HH (2016 b). Mesenchymal cells in cartilage growth and regeneration “an Immunohistochemical and electron microscopic study”. J Cytol Histol 7, 437. doi: 10. 4172/2157-7099.1000437.Google Scholar
Soliman, SA, Abd-Elhafeez, HH & Enas, A (2017a). A new mechanism of cartilage growth in mammals “Involvement of CD117 positive undifferentiated cells in interstitial growth”. Math J Cyto Histol 1(1), 001.Google Scholar
Soliman, SA, Ahmed, YA & Abdelsabour-Khalaf, M (2016). Histogenesis of the stomach of the pre-hatching quail: A light microscopic study. Anat Sci Int 91(4), 407–418.Google Scholar
Soliman, SA, Madkour, FA & Abdelhakeim, F (2017 c). Mesenchymal dependent mode of cartilage growth in post-hatching birds. J Histol Histopathol Res 1(1), 10–14.Google Scholar
Sottile, J (2004). Regulation of angiogenesis by extracellular matrix. Biochim Biophys Acta 1654(1), 13–22.Google Scholar
Suvarna, K, Layton, C & Bancroft, J (2013). Bancroft's Theory and Practice of Histological Techniques, 7th ed. Churchill Livingstone: Elsevier. eBook. ISBN: 9780702050329.Google Scholar
Troen, BR (2004). The role of cathepsin K in normal bone resorption. Drug News Perspect 17(1), 19–28.Google Scholar
van der Laan, WH, Quax, PH, Seemayer, CA, Huisman, LG, Pieterman, EJ, Grimbergen, JM, Verheijen, JH, Breedveld, FC, Gay, RE, Gay, S, Huizinga, TW & Pap, T (2003). Cartilage degradation and invasion by rheumatoid synovial fibroblasts is inhibited by gene transfer of TIMP-1 and TIMP-3. Gene Ther 10(3), 234–242.Google Scholar
van Donkelaar, CC & Wilson, W (2012). Mechanics of chondrocyte hypertrophy. Biomech Model Mechanobiol 11(5), 655–664.Google Scholar
Wilson, SR, Peters, C, Saftig, P & Bromme, D (2009). Cathepsin K activity-dependent regulation of osteoclast actin ring formation and bone resorption. J Biol Chem 284(4), 2584–2592.Google Scholar
Yang, L (2008). Mechanical properties of collagen fibrils and elastic fibers explored by AFM. phD Thesis, University of Twente.Google Scholar
Yousef, MS, Abd-Elhafeez, HH, Talukder, AK & Miyamoto, A (2019). Ovulatory follicular fluid induces sperm phagocytosis by neutrophils, but oviductal fluid around oestrus suppresses its inflammatory effect in the buffalo oviduct in vitro. Mol Reprod Dev 86(7), 835–846. doi: 10.1002 mrd 23164.Google Scholar