Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-22T20:16:03.588Z Has data issue: false hasContentIssue false
  • English
  • Français

New Insight into the Development of the Respiratory Acini in Rabbits: Morphological, Electron Microscopic Studies, and TUNEL Assay

Published online by Cambridge University Press:  14 February 2019

Doaa M. Mokhtar Open the ORCID record for Doaa M. Mokhtar [Opens in a new window] ,
Manal T. Hussein ,
Marwa M. Hussein ,
Enas A. Abd-Elhafez  and
Gamal Kamel
Doaa M. Mokhtar*
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Assiut, Egypt
Manal T. Hussein
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Assiut, Egypt
Marwa M. Hussein
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Assiut, Egypt
Enas A. Abd-Elhafez
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Assiut, Egypt
Gamal Kamel
Affiliation:
Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526, Assiut, Egypt
*
*Author for correspondence: Doaa M. Mokhtar, E-mail: [email protected]
Get access

Abstract

This study investigated the histomorphological features of developing rabbit respiratory acini during the postnatal period. On the 1st day of postnatal life, the epithelium of terminal bronchiole consisted of clear cells which intercalated between few ciliated and abundant non-ciliated (Clara) cells. At this age, the rabbit lung was in the alveolar stage. The terminal bronchioles branched into several alveolar ducts, which opened into atria that communicated to alveolar sacs. All primary and secondary inter-alveolar septa were thick and showed a double-capillary network (immature septa). The primitive alveoli were lined largely by type-I pneumocytes and mature type-II pneumocytes. The type-I pneumocytes displayed an intimate contact with the endothelial cells of the blood capillaries forming the blood–air barrier (0.90 ± 0.03 µm in thickness). On the 3rd day, we observed intense septation and massive formation of new secondary septa giving the alveolar sac a crenate appearance. The mean thickness of the air–blood barrier decreased to reach 0.78 ± 0.14 µm. On the 7th day, the terminal bronchiole epithelium consisted of ciliated and non-ciliated cells. The non-ciliated cells could be identified as Clara cells and serous cells. New secondary septa were formed, meanwhile the inter-alveolar septa become much thinner and the air–blood barrier thickness was 0.66 ± 0.03 µm. On the 14th day, the terminal bronchiole expanded markedly and the pulmonary alveoli were thin-walled. Inter-alveolar septa become much thinner and single capillary layers were observed. In the 1st month, the secondary septa increased in length forming mature cup-shaped alveoli. In the 2nd month, the lung tissue grew massively to involve the terminal respiratory unit. In the 3rd month, the pulmonary parenchyma appeared morphologically mature. All inter-alveolar septa showed a single-capillary layer, and primordia of new septa were also observed. The thickness of the air–blood barrier was much thinner; 0.56 ± 0.16 µm. TUNEL assay after birth revealed that the apoptotic cells were abundant and distributed in the epithelium lining of the pulmonary alveoli and the interstitium of the thick interalveolar septa. On the 7th day, and onward, the incidence of apoptotic cells decreased markedly. This study concluded that the lung development included two phases: the first phase (from birth to the 14th days) corresponds to the period of bulk alveolarization and microvascular maturation. The second phase (from the 14th days to the full maturity) corresponds to the lung growth and late alveolarization.

Keywords

air–blood barrieralveolarizationalveolielectron microscopypneumocytes
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 25 , Issue 3 , June 2019 , pp. 769 - 785
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

Amy, RWM, Bowes, D, Burri, PH, Haines, J & Thurlbeck, WM (1977). Postnatal growth of the mouse lung. J Anat 124, 131–151.Google Scholar
Blanco, LN & Frank, L (1993). The formation of alveoli in rat lung during the third and fourth postnatal weeks: Effect of hyperoxia, dexamethasone, and deferoxamine. Pediatr Res 34, 334–340.Google Scholar
Bruce, MC, Honaker, CE & Cross, RJ (1999). Lung fibroblasts undergoes apoptosis following alveolarization. Am J Respir Cell Mol Biol 20, 228–236.Google Scholar
Burri, PH (2006). Structural aspects of postnatal lung development: Alveolar formation and growth. Biol Neonate 89, 313–322.Google Scholar
Burri, PH, Dbaly, J & Weibel, ER (1974). The postnatal growth of the rat lung. I. Morphometry. Anat Rec 178, 711–730.Google Scholar
Carson, F (1990). Histotechnolog: A Self-Instructional Text, 1st ed, pp. 161–162. Chicago: ASCP Press.Google Scholar
Crossmon, G (1937). A modification of mallory's connective tissue stain with discussion of the principle involved. Anat Rec 69, 33–38.Google Scholar
Elhafez, EA, Mohamed, GK & Hussein, MM (2012). Development of the respiratory acinus in the rabbit lung. Recent Res Med Med Chem 1, 14–17.Google Scholar
Emery, JL & Mithal, A (1960). The number of alveoli in the terminal respiratory unit of man during late intrauterine life and childhood. Arch Dis Child 35, 544–547.Google Scholar
Gomori, G (1937). Silver impregnation of reticulum in paraffin sections. Am J Pathol 23, 993.Google Scholar
Gupta, AN & Jain, RK (2007). Histomicrometry of respiratory airways during postnatal lung development in goat (Capra hircus). Indian J Anim Res 41(1), 65–67.Google Scholar
Harris, HF (1900). On rapid conversion of haematoxylin into haematin in staining reactions. J Appl Microsc Lab Methods 3, 777. Cited by Bancroft, J.D. and Steven, A. (1996).Google Scholar
Herringes, M & Morrisey, EE (2014). Lung development: Orchestrating the generation and regeneration of a complex organ. Development 141, 502–513.Google Scholar
Joshi, S & Kotecha, S (2007). Lung growth and development. Early Hum Dev 83, 789–794.Google Scholar
Kovar, J, Sly, PD & Willet, KE (2002). Postnatal alveolar development of the rabbit. J Appl Physiol 93, 629–635.Google Scholar
Martiz, G & Van Wyk, G (1997). Influence of maternal nicotine exposure on neonatal rat lung structure: Protective effect of ascorbic acid. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 117, 159–165.Google Scholar
Massaro, GD & Massaro, D (1996). Formation of pulmonary alveoli and gas-exchange surface area: Quantitation and regulation. Annu Rev Physiol 58, 73–92.Google Scholar
McGowan, T (2007). The pulmonary lipofibroblasts and its contributions to alveolar development. Annu Rev Physiol 59, 43–62.Google Scholar
Mclaughlin, CA & Chiasson, RB (1990). Laboratory Anatomy of the Rabbit, 3rd ed. Dubuque, lowa, USA: Brown Publishers.Google Scholar
Mund, SI, Stampanoni, M & Schittny, JC (2004). Developmental alveolarization of the mouse lung. Dev Dyn 75, 125–151.Google Scholar
Nishino, H, Nemoto, N & Sakurai, I (1999). Significance of apoptosis in morphogenesis of human lung development: Light microscopic observation using in situ DNA end-labeling and ultrastructural study. Med Electron Microsc 32, 57–61.Google Scholar
Reynolds, EG (1963). The use of lead citrate at high pH as electron-opaque stain in electron microscopy. J Cell Biol 17, 208–212.Google Scholar
Riccio, VD, Tuyl, MV & Post, M (2004). Apoptosis in lung development and neonatal lung injury. Pediatr Res 55, 183–189.Google Scholar
Roth-Kleiner, M & Post, M (2005). Similarities and dissimilarities of branching and septation during lung development. Pediatr Pulmonol 40, 113–134.Google Scholar
Rucker, RB & Dubick, MA (1984). Elastin metabolism and chemistry: Potential roles in lung development and structure. Environ Health Perspect 55, 179–191.Google Scholar
Runciman, SIC, Baudinette, RV & Gannon, BJ (1996). Postnatal development of the lung parenchyma in a marsupial: The tammar wallaby. Anat Record 244, 93–206.Google Scholar
Schittny, JC (2017). Development of the lung. Cell Tissue Res 367, 427–444.Google Scholar
Schittny, JC & Burri, PH (2007). Development and growth of the lung. Development 139, 111–124.Google Scholar
Schittny, JC, Mund, SI & Stampanoni, M (2007). Evidence and structural mechanism for late lung alveolarization. Am J Physiol Lung Cell Mol Physiol 294, L246–L254.Google Scholar
Spurr (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26, 31–43.Google Scholar
Starcher, BC (2000). Lung elastin and matrix. Chest 117, 229S–234S.Google Scholar
Thurmon, JC, Tranquilli, WJ & Benson, GJ (1996). Lumb & Jones Veterinary Anesthesia, 3rd ed. London: Lea & Febiger.Google Scholar
Van Gieson, I (1889). Laboratory notes of technical methods for the nervous system. New York Med J 50, 57–60.Google Scholar
Weigert, C (1898). Übereine methode zur färbung elastischer fasern. Zentrablat fuer Allgemeine pathologie und pathologische Anatomie 9, 289–292. Cited by Bancroft, J.D. and Steven, A. (1996). Theory and practice of histological techniques. 4th ed., Churchill Livingstone. New York. Edinburg. London. Madrid. Melbourne. San Francisco. Tokyo.Google Scholar
Wickman, G, Julian, L & Olson, MF (2012). How apoptoticc cells aid in the removal of their own cold dead bodies. Cell Death Differ 19, 735–742.Google Scholar
Williams, GT (1991). Programed cell death: Apoptosis and oncogenesis. Cell 65, 1097–1098.Google Scholar
Zhenxing, F, Heldt, GP & West, JB (2003). Thickness of the blood-gas barrier in premature and 1-day-old newborn rabbit lungs. Am J Physiol Lung Cell Mol Physiol 285, L130–L136.Google Scholar