Abstract
Thin type 1 alveolar epithelial (AE1) and surfactant producing type 2 alveolar epithelial (AE2) cells line the alveoli in the lung and are essential for normal lung function. Function is intimately interrelated to structure, so that detailed knowledge of the epithelial ultrastructure can significantly enhance our understanding of its function. The basolateral surface of the cells or the epithelial contact sites are of special interest, because they play an important role in intercellular communication or stabilizing the epithelium. The latter is in particular important for the lung with its variable volume. The aim of the present study was to investigate the three-dimensional (3D) ultrastructure of the human alveolar epithelium focusing on contact sites and the basolateral cell membrane of AE2 cells using focused ion beam electron microscopy and subsequent 3D reconstructions. The study provides detailed surface reconstructions of two AE1 cell domains and two AE2 cells, showing AE1/AE1, AE1/AE2 and AE2/AE2 contact sites, basolateral microvilli pits at AE2 cells and small AE1 processes beneath AE2 cells. Furthermore, we show reconstructions of a surfactant secretion pore, enlargements of the apical AE1 cell surface and long folds bordering grooves on the basal AE1 cell surface. The functional implications of our findings are discussed. These findings may lay the structural basis for further molecular investigations.
Highlights
Type 1 alveolar epithelial (AE1) and type 2 alveolar epithelial (AE2) cells form the epithelial lining of alveoli in the human lung
Volume electron microscopic (EM) techniques for 3D modeling of biological structures, including “conventional” techniques like single sectioning transmission electron microscopy and “new” techniques like serial block-face (SBF) scanning electron microscope (SEM) and focused ion beam (FIB) SEM, have been reviewed extensively recently, e.g., [9,10,11,12,13] and some of them have already been used for 3D reconstructions of lung structure: ssTEM [5,7,8,14]; electron tomography [15]; array tomography [16] and SBF SEM [6,11]
Even FIB SEM has been applied [17,18,19], but the study of Købler et al was rather focused on testing an alternative method to diamond knife ultramicrotomy and transmission electron microscopic imaging of nanotubes; the review of Ochs et al gave an outlook on the potential of this technique in lung research; and Hegermann et al demonstrated a method for correlative light and electron microscopy
Summary
Type 1 alveolar epithelial (AE1) and type 2 alveolar epithelial (AE2) cells form the epithelial lining of alveoli in the human lung. Three entire AE1 cells were modeled in three dimensions (3D) by manual segmentation of a serial block-face (SBF) scanning electron microscopic data set of a human lung sample. Both the branching capability and the chance of having more than one apical surface could be confirmed for AE1 cells by this method. The SBF data suggested a complex morphology of AE1/AE2 cell contacts, variable overlap of adjacent AE1 cells and the existence of numerous microvilli that may appear clustered in small niches of the basolateral AE2 cell surface, findings in line with those of Sirianni et al [5] and Mercurio and Rhodin [7,8]. Knowledge about the detailed 3D organization of the basolateral cell membrane of AE2 cells may help to understand the crosstalk between AE2 and other cells of the septal wall
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