Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction

Abstract Background The cellular mechanisms involved in the development of proximal tubules are not only associated with morphogenesis in fetal life, but also with restoration of damaged tubules in adulthood. Knowledge about morphological features of cell differentiation and proliferation along the...

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Main Authors: Jing Cong, Shi‐Jie Chang, Jesper Skovhus Thomsen, Arne Andreasen, Xue Chen, Jia Xing, Jie Zhang, Ling Gu, Xiao‐Yue Zhai
Format: Article
Language:English
Published: Wiley 2021-09-01
Series:Veterinary Medicine and Science
Subjects:
Online Access:https://doi.org/10.1002/vms3.558
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author Jing Cong
Shi‐Jie Chang
Jesper Skovhus Thomsen
Arne Andreasen
Xue Chen
Jia Xing
Jie Zhang
Ling Gu
Xiao‐Yue Zhai
author_facet Jing Cong
Shi‐Jie Chang
Jesper Skovhus Thomsen
Arne Andreasen
Xue Chen
Jia Xing
Jie Zhang
Ling Gu
Xiao‐Yue Zhai
author_sort Jing Cong
collection DOAJ
description Abstract Background The cellular mechanisms involved in the development of proximal tubules are not only associated with morphogenesis in fetal life, but also with restoration of damaged tubules in adulthood. Knowledge about morphological features of cell differentiation and proliferation along the developing tubule is insufficient, which hinders identification of the cellular origin. Objectives This study aimed to investigate ultrastructures of the proximal tubule at different stages of nephrogenesis. Methods Electron microscopy was used and guided by computer‐assisted tubular tracing to identify the cellular structures. Results Renal vesicles and S‐shaped bodies revealed more proliferative features, such as densely‐packed fusiform‐shaped cells with numerous protein‐producing organelles than membrane specializations typical for mature tubules. At the capillary‐loop stage the proximal tubules demonstrated all characteristics of the mature tubules, but not as developed, including shorter but densely packed microvilli, fewer lateral processes with cell‐cell contacts, lower basal membrane infoldings, and lower mitochondrial volume density. However, they exhibited an elaborated endocytic system above the nucleus, indicating a membrane transport is being established. Abundant free‐ and endoplasmic reticulum‐adhered ribosomes and Golgi complexes reflected active protein synthesis for cell growth and proliferation. Interestingly, electron dense cells were occasionally intermixed with electron lucent cells characterized by various organelles in less cytosol and a larger nucleus with abundant euchromatin, which is a feature of active proliferation. Conclusions These ultrastructures indicate that the morphogenesis of the developing proximal tubule corresponds to the gradually established physiological activities. The two different cellular electron densities may suggest distinctive differentiation of the cells along the tubule.
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spelling doaj.art-8d5cbfc58c0341f1825a236ea60a2a8c2022-12-21T22:31:36ZengWileyVeterinary Medicine and Science2053-10952021-09-01751989199810.1002/vms3.558Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstructionJing Cong0Shi‐Jie Chang1Jesper Skovhus Thomsen2Arne Andreasen3Xue Chen4Jia Xing5Jie Zhang6Ling Gu7Xiao‐Yue Zhai8Department of Histology and Embryology, Basic Medical College China Medical University Shenyang ChinaDepartment of Biomedical Engineering, College of Fundamental Science China Medical University Shenyang ChinaDepartment of Biomedicine–Anatomy Aarhus University Aarhus DenmarkDepartment of Biomedicine–Anatomy Aarhus University Aarhus DenmarkDepartment of Histology and Embryology, Basic Medical College China Medical University Shenyang ChinaDepartment of Histology and Embryology, Basic Medical College China Medical University Shenyang ChinaDepartment of Histology and Embryology, Basic Medical College China Medical University Shenyang ChinaDepartment of Histology and Embryology, Basic Medical College China Medical University Shenyang ChinaDepartment of Histology and Embryology, Basic Medical College China Medical University Shenyang ChinaAbstract Background The cellular mechanisms involved in the development of proximal tubules are not only associated with morphogenesis in fetal life, but also with restoration of damaged tubules in adulthood. Knowledge about morphological features of cell differentiation and proliferation along the developing tubule is insufficient, which hinders identification of the cellular origin. Objectives This study aimed to investigate ultrastructures of the proximal tubule at different stages of nephrogenesis. Methods Electron microscopy was used and guided by computer‐assisted tubular tracing to identify the cellular structures. Results Renal vesicles and S‐shaped bodies revealed more proliferative features, such as densely‐packed fusiform‐shaped cells with numerous protein‐producing organelles than membrane specializations typical for mature tubules. At the capillary‐loop stage the proximal tubules demonstrated all characteristics of the mature tubules, but not as developed, including shorter but densely packed microvilli, fewer lateral processes with cell‐cell contacts, lower basal membrane infoldings, and lower mitochondrial volume density. However, they exhibited an elaborated endocytic system above the nucleus, indicating a membrane transport is being established. Abundant free‐ and endoplasmic reticulum‐adhered ribosomes and Golgi complexes reflected active protein synthesis for cell growth and proliferation. Interestingly, electron dense cells were occasionally intermixed with electron lucent cells characterized by various organelles in less cytosol and a larger nucleus with abundant euchromatin, which is a feature of active proliferation. Conclusions These ultrastructures indicate that the morphogenesis of the developing proximal tubule corresponds to the gradually established physiological activities. The two different cellular electron densities may suggest distinctive differentiation of the cells along the tubule.https://doi.org/10.1002/vms3.558developing kidneyproximal tubulerenal vesicleS‐shaped bodyultrastructure
spellingShingle Jing Cong
Shi‐Jie Chang
Jesper Skovhus Thomsen
Arne Andreasen
Xue Chen
Jia Xing
Jie Zhang
Ling Gu
Xiao‐Yue Zhai
Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction
Veterinary Medicine and Science
developing kidney
proximal tubule
renal vesicle
S‐shaped body
ultrastructure
title Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction
title_full Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction
title_fullStr Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction
title_full_unstemmed Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction
title_short Ultrastructural identification of developing proximal tubules based on three‐dimensional reconstruction
title_sort ultrastructural identification of developing proximal tubules based on three dimensional reconstruction
topic developing kidney
proximal tubule
renal vesicle
S‐shaped body
ultrastructure
url https://doi.org/10.1002/vms3.558
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