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      How high resolution 3-dimensional imaging changes our understanding of postnatal lung development

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          Abstract

          During the last 10 + years biologically and clinically significant questions about postnatal lung development could be answered due to the application of modern cutting-edge microscopic and quantitative histological techniques. These are in particular synchrotron radiation based X-ray tomographic microscopy (SRXTM), but also 3Helium Magnetic Resonance Imaging, as well as the stereological estimation of the number of alveoli and the length of the free septal edge. First, the most important new finding may be the following: alveolarization of the lung does not cease after the maturation of the alveolar microvasculature but continues until young adulthood and, even more important, maybe reactivated lifelong if needed to rescue structural damages of the lungs. Second, the pulmonary acinus represents the functional unit of the lung. Because the borders of the acini could not be detected in classical histological sections, any investigation of the acini requires 3-dimensional (imaging) methods. Based on SRXTM it was shown that in rat lungs the number of acini stays constant, meaning that their volume increases by a factor of ~ 11 after birth. The latter is very important for acinar ventilation and particle deposition.

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          The online version of this article (10.1007/s00418-018-1749-7) contains supplementary material, which is available to authorized users.

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          Most cited references93

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          Regulation of early lung morphogenesis: questions, facts and controversies.

          During early respiratory system development, the foregut endoderm gives rise to the tracheal and lung cell progenitors. Through branching morphogenesis, and in coordination with vascular development, a tree-like structure of epithelial tubules forms and differentiates to produce the airways and alveoli. Recent studies have implicated the fibroblast growth factor, sonic hedgehog, bone morphogenetic protein, retinoic acid and Wnt signaling pathways, and various transcription factors in regulating the initial stages of lung development. However, the precise roles of these molecules and how they interact in the developing lung is subject to debate. Here, we review early stages in lung development and highlight questions and controversies regarding their molecular regulation.
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            Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction.

            Cellular mechanisms contributing to renewal of terminal bronchioles remain poorly defined. Our previous studies identified pollutant-resistant Clara cell secretory protein (CCSP)-expressing stem cells that localize to the neuroepithelial body (NEB) and contribute to renewal of the proximal bronchiolar epithelium. However, activation of NEB-associated stem cells is unlikely to contribute to renewal of terminal bronchiolar epithelium because of the paucity of NEBs at this location. Goals of this study were to determine the location and properties of cells contributing to renewal of terminal bronchioles after Clara cell depletion. Pollutant-resistant CCSP-expressing cells were identified that localized to the bronchoalveolar duct junction (BADJ) and contribute to restoration of a phenotypically diverse epithelium. CCSP-expressing cells comprise the predominant proliferative population in initial terminal bronchiolar repair and include a population of label-retaining cells suggesting that they maintain characteristics of a stem cell population. Furthermore, immunohistochemical co-localization studies involving CCSP and the NEB-specific marker calcitonin gene-related peptide indicate that BADJ-associated CCSP-expressing stem cells function independently of NEB microenvironments. These studies identify a BADJ-associated, NEB-independent, CCSP-expressing stem cell population in terminal bronchioles and support the notion that regiospecific stem cell niches function to maintain epithelial diversity after injury.
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              Fetal and postnatal development of the lung.

              P Burri (1983)
              The life of a human lung can be subdivided into five distinct phases: embryonic, pseudoglandular, canalicular, saccular, and alveolar. The embryonic period, during which the lung primordium is laid down as a diverticulum of the foregut, lasts for about seven weeks. From the 5th to the 17th week the lung looks much like a tubulo-acinar gland, with epithelial tubes sprouting and branching into the surrounding mesenchyme. In the last week of this pseudoglandular stage the prospective conductive airways have been formed, and the acinar limits can be recognized. The events of the subsequent canalicular phase (17th-26th week) can be summarized as the widening of the peripheral tubules, the differentiation of the cuboidal epithelium into type I and type II cells, the formation of the first thin air-blood barriers, and the start of surfactant production. During the saccular stage, which follows and lasts until birth, the growth of the pulmonary parenchyma, the thinning of the connective tissue between the airspaces, and the further maturation of the surfactant system are the most important steps towards life. At birth, although already functional, the lung is structurally still in an immature condition, because alveoli, the gas exchange units of the adult lung, are practically missing. The airspaces present are smooth-walled transitory ducts and saccules with primitive type septa that are thick and contain a double capillary network. During the first 1-3 years of postnatal life, alveoli are formed through a septation process that greatly increases the gas exchange surface area. The primitive septa with their capillaries undergo a complete remodeling, gaining the mature slender morphology found in the adult lung.
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                Author and article information

                Contributors
                +41-31-631-4635 , johannes.schittny@ana.unibe.ch
                Journal
                Histochem Cell Biol
                Histochem. Cell Biol
                Histochemistry and Cell Biology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0948-6143
                1432-119X
                2 November 2018
                2 November 2018
                2018
                : 150
                : 6
                : 677-691
                Affiliations
                ISNI 0000 0001 0726 5157, GRID grid.5734.5, Institute of Anatomy, , University of Bern, ; Baltzerstrasse 2, 3012 Bern, Switzerland
                Author information
                http://orcid.org/0000-0003-4025-3961
                Article
                1749
                10.1007/s00418-018-1749-7
                6267404
                30390117
                6e938745-aef3-48f3-ae22-ed80d2e2232e
                © The Author(s) 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 19 October 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 310030_153468
                Award ID: 310030_175953
                Award Recipient :
                Categories
                Review
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2018

                Cell biology
                lung development,pulmonary alveolarization,microvascular maturation,angiogenesis,pulmonary acinus

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