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Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization.

Ackermann M, Houdek JP, Gibney BC, Ysasi A, Wagner W, Belle J, Schittny JC, Enzmann F, Tsuda A, Mentzer SJ, Konerding MA - Angiogenesis (2013)

Bottom Line: In most rodents and some other mammals, the removal of one lung results in compensatory growth associated with dramatic angiogenesis and complete restoration of lung capacity.In addition, the appearance of pillar formations and duplications on alveolar entrance ring vessels in mature alveoli are indicative of vascular remodeling.Various forms of developmental neoalveolarization may also be considered to contribute in compensatory lung regeneration.

View Article: PubMed Central - PubMed

Affiliation: Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg-University Mainz, 55128, Mainz, Germany.

ABSTRACT
In most rodents and some other mammals, the removal of one lung results in compensatory growth associated with dramatic angiogenesis and complete restoration of lung capacity. One pivotal mechanism in neoalveolarization is neovascularization, because without angiogenesis new alveoli can not be formed. The aim of this study is to image and analyze three-dimensionally the different patterns of neovascularization seen following pneumonectomy in mice on a sub-micron-scale. C57/BL6 mice underwent a left-sided pneumonectomy. Lungs were harvested at various timepoints after pneumonectomy. Volume analysis by microCT revealed a striking increase of 143 percent in the cardiac lobe 14 days after pneumonectomy. Analysis of microvascular corrosion casting demonstrated spatially heterogenous vascular densitities which were in line with the perivascular and subpleural compensatory growth pattern observed in anti-PCNA-stained lung sections. Within these regions an expansion of the vascular plexus with increased pillar formations and sprouting angiogenesis, originating both from pre-existing bronchial and pulmonary vessels was observed. Also, type II pneumocytes and alveolar macrophages were seen to participate actively in alveolar neo-angiogenesis after pneumonectomy. 3D-visualizations obtained by high-resolution synchrotron radiation X-ray tomographic microscopy showed the appearance of double-layered vessels and bud-like alveolar baskets as have already been described in normal lung development. Scanning electron microscopy data of microvascular architecture also revealed a replication of perialveolar vessel networks through septum formation as already seen in developmental alveolarization. In addition, the appearance of pillar formations and duplications on alveolar entrance ring vessels in mature alveoli are indicative of vascular remodeling. These findings indicate that sprouting and intussusceptive angiogenesis are pivotal mechanisms in adult lung alveolarization after pneumonectomy. Various forms of developmental neoalveolarization may also be considered to contribute in compensatory lung regeneration.

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Compensatory lung growth in the cardiac lobe. Left pneumonectomy in mice results in compensatory growth of the right lung. The cardiac lobe in particular extends dramatically into the left pleural cavity enabling restoration of the vital capacity within 21 days. a The cardiac lobe fills out the left pleural cavity almost completely, already 14 days after surgery. b Finite element reconstructions of the cardiac lobe originating from microCT data reveal an increase of 143 percent in volume 14 days after pneumonectomy. Reconstruction created by Nenad Filipovic, University of Kragujevac, Serbia. c, d Contrary to the vasculature of control cardiac lobes (c), low power SEM images of microvascular corrosion casts showing heterogeneous vascular densities and distributions 7 days after surgery
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Fig1: Compensatory lung growth in the cardiac lobe. Left pneumonectomy in mice results in compensatory growth of the right lung. The cardiac lobe in particular extends dramatically into the left pleural cavity enabling restoration of the vital capacity within 21 days. a The cardiac lobe fills out the left pleural cavity almost completely, already 14 days after surgery. b Finite element reconstructions of the cardiac lobe originating from microCT data reveal an increase of 143 percent in volume 14 days after pneumonectomy. Reconstruction created by Nenad Filipovic, University of Kragujevac, Serbia. c, d Contrary to the vasculature of control cardiac lobes (c), low power SEM images of microvascular corrosion casts showing heterogeneous vascular densities and distributions 7 days after surgery

Mentions: The removal of the left lung results in a compensatory growth of the right lung with the highest activity in the cardiac lobe that expands dramatically in the left pleural chest (Fig. 1a). MicroCT measurements of different volumes of thr cardiac lobe after pneumonectomy showed a steep augmentation of 143 % on day 14 as a result of the high increase in proliferation that peaks on day six after pneumonectomy as detailed in our previous work. Spatial visualization of the increase in cardiac lobe by finite element reconstructions showed a volume uptake from the regions close to the heart towards the chest wall (Fig. 1b). SEM evaluation of microvascular corrosion casts demonstrated a heterogenous distribution of vascular growth spots which were highly evident in the indentation close to the heart (Fig. 1c, d).Fig. 1


Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization.

Ackermann M, Houdek JP, Gibney BC, Ysasi A, Wagner W, Belle J, Schittny JC, Enzmann F, Tsuda A, Mentzer SJ, Konerding MA - Angiogenesis (2013)

Compensatory lung growth in the cardiac lobe. Left pneumonectomy in mice results in compensatory growth of the right lung. The cardiac lobe in particular extends dramatically into the left pleural cavity enabling restoration of the vital capacity within 21 days. a The cardiac lobe fills out the left pleural cavity almost completely, already 14 days after surgery. b Finite element reconstructions of the cardiac lobe originating from microCT data reveal an increase of 143 percent in volume 14 days after pneumonectomy. Reconstruction created by Nenad Filipovic, University of Kragujevac, Serbia. c, d Contrary to the vasculature of control cardiac lobes (c), low power SEM images of microvascular corrosion casts showing heterogeneous vascular densities and distributions 7 days after surgery
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4061467&req=5

Fig1: Compensatory lung growth in the cardiac lobe. Left pneumonectomy in mice results in compensatory growth of the right lung. The cardiac lobe in particular extends dramatically into the left pleural cavity enabling restoration of the vital capacity within 21 days. a The cardiac lobe fills out the left pleural cavity almost completely, already 14 days after surgery. b Finite element reconstructions of the cardiac lobe originating from microCT data reveal an increase of 143 percent in volume 14 days after pneumonectomy. Reconstruction created by Nenad Filipovic, University of Kragujevac, Serbia. c, d Contrary to the vasculature of control cardiac lobes (c), low power SEM images of microvascular corrosion casts showing heterogeneous vascular densities and distributions 7 days after surgery
Mentions: The removal of the left lung results in a compensatory growth of the right lung with the highest activity in the cardiac lobe that expands dramatically in the left pleural chest (Fig. 1a). MicroCT measurements of different volumes of thr cardiac lobe after pneumonectomy showed a steep augmentation of 143 % on day 14 as a result of the high increase in proliferation that peaks on day six after pneumonectomy as detailed in our previous work. Spatial visualization of the increase in cardiac lobe by finite element reconstructions showed a volume uptake from the regions close to the heart towards the chest wall (Fig. 1b). SEM evaluation of microvascular corrosion casts demonstrated a heterogenous distribution of vascular growth spots which were highly evident in the indentation close to the heart (Fig. 1c, d).Fig. 1

Bottom Line: In most rodents and some other mammals, the removal of one lung results in compensatory growth associated with dramatic angiogenesis and complete restoration of lung capacity.In addition, the appearance of pillar formations and duplications on alveolar entrance ring vessels in mature alveoli are indicative of vascular remodeling.Various forms of developmental neoalveolarization may also be considered to contribute in compensatory lung regeneration.

View Article: PubMed Central - PubMed

Affiliation: Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg-University Mainz, 55128, Mainz, Germany.

ABSTRACT
In most rodents and some other mammals, the removal of one lung results in compensatory growth associated with dramatic angiogenesis and complete restoration of lung capacity. One pivotal mechanism in neoalveolarization is neovascularization, because without angiogenesis new alveoli can not be formed. The aim of this study is to image and analyze three-dimensionally the different patterns of neovascularization seen following pneumonectomy in mice on a sub-micron-scale. C57/BL6 mice underwent a left-sided pneumonectomy. Lungs were harvested at various timepoints after pneumonectomy. Volume analysis by microCT revealed a striking increase of 143 percent in the cardiac lobe 14 days after pneumonectomy. Analysis of microvascular corrosion casting demonstrated spatially heterogenous vascular densitities which were in line with the perivascular and subpleural compensatory growth pattern observed in anti-PCNA-stained lung sections. Within these regions an expansion of the vascular plexus with increased pillar formations and sprouting angiogenesis, originating both from pre-existing bronchial and pulmonary vessels was observed. Also, type II pneumocytes and alveolar macrophages were seen to participate actively in alveolar neo-angiogenesis after pneumonectomy. 3D-visualizations obtained by high-resolution synchrotron radiation X-ray tomographic microscopy showed the appearance of double-layered vessels and bud-like alveolar baskets as have already been described in normal lung development. Scanning electron microscopy data of microvascular architecture also revealed a replication of perialveolar vessel networks through septum formation as already seen in developmental alveolarization. In addition, the appearance of pillar formations and duplications on alveolar entrance ring vessels in mature alveoli are indicative of vascular remodeling. These findings indicate that sprouting and intussusceptive angiogenesis are pivotal mechanisms in adult lung alveolarization after pneumonectomy. Various forms of developmental neoalveolarization may also be considered to contribute in compensatory lung regeneration.

Show MeSH
Related in: MedlinePlus