Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T07:40:18.963Z Has data issue: false hasContentIssue false
  • English
  • Français

Onset of Appearance and Potential Significance of Telocytes in the Developing Fetal Lung

Published online by Cambridge University Press:  16 September 2019

Mahmoud Awad ,
Wafaa Gaber  and
Dalia Ibrahim
Mahmoud Awad
Affiliation:
Department of Histology, Faculty of Veterinary Medicine, South Valley University, Qena 83523, Egypt
Wafaa Gaber
Affiliation:
Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, Assuit University, Assuit, Egypt
Dalia Ibrahim*
Affiliation:
Department of Histology, Faculty of Veterinary Medicine, South Valley University, Qena 83523, Egypt
*
*Author for correspondence: D. Ibrahim, E-mail: dalia.mohamadain@vet.svu.edu.eg; daliamahmoud.histology@gmail.com
Get access

Abstract

CD34, vimentin, and vascular endothelial growth factor immunohistochemical analysis and electron microscopic tools were employed to record the initial appearance of telocytes (TCs) and stage-by-stage variations in TC localizations in the developing rabbit lung. TCs could not be identified in the primitive embryonic lung until day 18 of gestation. In the pseudoglandular lung, CD34+ TCs had been recorded under the cartilage of the main bronchus, in the wall of large-sized pulmonary vessels and large epithelial tubes. In the canalicular phase, TCs could be demonstrated in the smooth muscle layer of the bronchioles including the terminal ones. The strength of CD34 immunoreactive signals had been amplified by age until the day of parturition. Ultrastructurally, TCs consisted of a tiny body and exceptionally long telopodes (Tps). The Tp consisted of alternating thin segments (podomers) and dilated ones (podoms). The Tp sometimes branched with a dichotomous pattern. TCs interconnected in a network either by homocellular junctions with neighboring TCs or by heterocellular junctions with smooth muscle cells and alveolar cells. Collectively, early detection of TCs in pulmonary vessels suggests a potential role for TCs in their angiogenesis. For the lung tissue, TCs seem to be involved in the regulation of lung histogenesis.

Keywords

CD34lung developmenttelocyteTEM
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 25 , Issue 5 , October 2019 , pp. 1246 - 1256
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.)

References

Abd-Elhafeez, HH & Soliman, SA (2017). New description of telocyte sheaths in the bovine uterine tube: An immunohistochemical and scanning microscopic study. Cells Tissues Organs 203(5), 295–315.Google Scholar
Bani, D, Formigli, L, Gherghiceanu, M & Faussone-Pellegrini, MS (2010). Telocytes as supporting cells for myocardial tissue organization in developing and adult heart. J Cell Mol Med 14(10), 2531–2538.Google Scholar
Cantarero, CL, Luesma Bartolome, MJ & Junquera Escribano, C (2011). Identification of telocytes in the lamina propria of rat duodenum: Transmission electron microscopy. J Cell Mol Med 15(1), 26–30.Google Scholar
Chang, Y, Li, C, Lu, Z, Li, H & Guo, Z (2015). Multiple immunophenotypes of cardiac telocytes. Exp Cell Res 338(2), 239–244.Google Scholar
Chen, X, Zheng, Y, Manole, CG, Wang, X & Wang, Q (2013). Telocytes in human oesophagus. J Cell Mol Med 17(11), 1506–1512.Google Scholar
Chinoy, MR (2003). Lung growth and development. Front Biosci 8, d392–d415.Google Scholar
Deng, W (2010). Mesenchymal stem cells express c-kit. Circ Res 107(10), e17, Author reply e18.Google Scholar
Eidenschink, L, DiZerega, G, Rodgers, K, Barlet, M, Wells, D & Loken, M (2012). Basal levels of CD34 positive cells in peripheral blood differ between individuals and are stable for 18 months. Cytometry B Clin Cytom 82, 18–25.Google Scholar
Faussone-Pellegrini, MS & Gherghiceanu, M (2016). Telocyte's contacts. Semin Cell Dev Biol 55, 3–8.Google Scholar
Faussone Pellegrini, MS & Popescu, LM (2011). Telocytes. Biomol Concepts 2(6), 481–489.Google Scholar
Gherghiceanu, M, Hinescu, ME, Andrei, F, Mandache, E, Macarie, CE, Faussone-Pellegrini, MS & Popescu, LM (2008). Interstitial Cajal-like cells (ICLC) in myocardial sleeves of human pulmonary veins. J Cell Mol Med 12(5A), 1777–1781.Google Scholar
Gherghiceanu, M & Popescu, LM (2011). Heterocellular communication in the heart: Electron tomography of telocyte-myocyte junctions. J Cell Mol Med 15(4), 1005–1011.Google Scholar
Hinescu, ME, Gherghiceanu, M, Suciu, L & Popescu, LM (2011). Telocytes in pleura: Two- and three-dimensional imaging by transmission electron microscopy. Cell Tissue Res 343(2), 389–397.Google Scholar
Hinescu, ME, Popescu, LM, Gherghiceanu, M & Faussone-Pellegrini, MS (2008). Interstitial Cajal-like cells in rat mesentery: An ultrastructural and immunohistochemical approach. J Cell Mol Med 12(1), 260–270.Google Scholar
Hussein, MW & Mokhtar, DM (2018). The roles of telocytes in lung development and angiogenesis: An immunohistochemical, ultrastructural, scanning electron microscopy and morphometrical study. Developmental Biology 15, 443(2), 137–152.Google Scholar
Ingber, DE (2006). Cellular mechanotransduction: Putting all the pieces together again. FASEB J 20(7), 811–827.Google Scholar
Karnak, I, Muftuoglu, S, Cakar, N & Tanyel, FC (1999). Organ growth and lung maturation in rabbit fetuses. Res Exp Med (Berl) 198(5), 277–287.Google Scholar
Kostin, S & Popescu, LM (2009). A distinct type of cell in myocardium: Interstitial Cajal-like cells (ICLCs). J Cell Mol Med 13(2), 295–308.Google Scholar
Mandache, E, Popescu, LM & Gherghiceanu, M (2007). Myocardial interstitial Cajal-like cells (ICLC) and their nanostructural relationships with intercalated discs: Shed vesicles as intermediates. J Cell Mol Med 11(5), 1175–1184.Google Scholar
Mihalcea, CE, Morosanu, AM, Murarasu, D, Puiu, L, Cinca, S, Voinea, SC & Mirancea, N (2015). Particular molecular and ultrastructural aspects in invasive mammary carcinoma. Rom J Morphol Embryol 56(4), 1371–1381.Google Scholar
Nicolescu, MI & Popescu, LM (2012). Telocytes in the interstitium of human exocrine pancreas: Ultrastructural evidence. Pancreas 41(6), 949–956.Google Scholar
Popescu, LM, Ciontea, SM & Cretoiu, D (2007). Interstitial Cajal-like cells in human uterus and fallopian tube. Ann N Y Acad Sci 1101, 139–165.Google Scholar
Popescu, LM & Faussone-Pellegrini, MS (2010). TELOCYTES - A case of serendipity: The winding way from interstitial cells of Cajal (ICC), via interstitial Cajal-like cells (ICLC) to TELOCYTES. J Cell Mol Med 14(4), 729–740.Google Scholar
Popescu, LM, Gherghiceanu, M, Mandache, E & Cretoiu, D (2006). Caveolae in smooth muscles: Nanocontacts. J Cell Mol Med 10(4), 960–990.Google Scholar
Popescu, LM, Gherghiceanu, M, Manole, CG & Faussone-Pellegrini, MS (2009). Cardiac renewing: Interstitial Cajal-like cells nurse cardiomyocyte progenitors in epicardial stem cell niches. J Cell Mol Med 13(5), 866–886.Google Scholar
Popescu, LM, Gherghiceanu, M, Suciu, LC, Manole, CG & Hinescu, ME (2011). Telocytes and putative stem cells in the lungs: Electron microscopy, electron tomography and laser scanning microscopy. Cell Tissue Res 345(3), 391–403.Google Scholar
Popescu, LM, Manole, CG, Gherghiceanu, M, Ardelean, A, Nicolescu, MI, Hinescu, ME & Kostin, S (2010). Telocytes in human epicardium. J Cell Mol Med 14(8), 2085–2093.Google Scholar
Radu, E, Regalia, T, Ceafalan, L, Andrei, F, Cretoiu, D & Popescu, LM (2005). Cajal-type cells from human mammary gland stroma: Phenotype characteristics in cell culture. J Cell Mol Med 9(3), 748–752.Google Scholar
Reynolds, ES (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Cell Biol 17, 208–212.Google Scholar
Satelli, A & Li, S (2011). Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 68(18), 3033–3046.Google Scholar
Shi, L, Dong, N, Chen, C & Wang, X (2016). Potential roles of telocytes in lung diseases. Semin Cell Dev Biol 55, 31–39.Google Scholar
Sidney, LE, Branch, MJ, Dunphy, SE, Dua, HS & Hopkinson, A (2014). Concise review: Evidence for CD34 as a common marker for diverse progenitors. Stem Cells 32(6), 1380–1389.Google Scholar
Song, D, Cretoiu, D, Cretoiu, SM & Wang, X (2016). Telocytes and lung disease. Histol Histopathol 31(12), 1303–1314.Google Scholar
Suciu, L, Popescu, LM, Gherghiceanu, M, Regalia, T, Nicolescu, MI, Hinescu, ME & Faussone-Pellegrini, MS (2010). Telocytes in human term placenta: Morphology and phenotype. Cells Tissues Organs 192(5), 325–339.Google Scholar
Urban, L, Miko, M, Kajanova, M, Bozikova, S, Mrazova, H & Varga, I (2016). Telocytes (interstitial Cajal-like cells) in human fallopian tubes. Bratisl Lek Listy 117(5), 263–267.Google Scholar
Wang, J, Jin, M, Ma, WH, Zhu, Z & Wang, X (2016). The history of telocyte discovery and understanding. Adv Exp Med Biol 913, 1–21.Google Scholar
Warburton, D, El-Hashash, A, Carraro, G, Tiozzo, C, Sala, F, Rogers, O, De Langhe, S, Kemp, PJ, Riccardi, D, Torday, Jet al. (2010). Lung organogenesis. Curr Top Dev Biol 90, 73–158.Google Scholar
Weaver, M, Batts, L & Hogan, BL (2003). Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 258(1), 169–184.Google Scholar
Zheng, Y, Bai, C & Wang, X (2012 a). Potential significance of telocytes in the pathogenesis of lung diseases. Expert Rev Respir Med 6(1), 45–49.Google Scholar
Zheng, Y, Bai, C & Wang, X (2012 b). Telocyte morphologies and potential roles in diseases. J Cell Physiol 227(6), 2311–2317.Google Scholar
Zheng, Y, Chen, X, Qian, M, Zhang, M, Zhang, D, Bai, C, Wang, Q & Wang, X (2014). Human lung telocytes could promote the proliferation and angiogenesis of human pulmonary microvascular endothelial cells in vitro. Mol Cell Ther 2, 3.Google Scholar
Zheng, Y, Li, H, Manole, CG, Sun, A, Ge, J & Wang, X (2011). Telocytes in trachea and lungs. J Cell Mol Med 15(10), 2262–2268.Google Scholar
Zheng, Y, Zhang, M, Qian, M, Wang, L, Cismasiu, VB, Bai, C, Popescu, LM & Wang, X (2013). Genetic comparison of mouse lung telocytes with mesenchymal stem cells and fibroblasts. J Cell Mol Med 17(4), 567–577.Google Scholar