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

Publication type:
Journal article
Metadata:
Autoren
  • Maximilian Ackermann
  • Jan P Houdek
  • Barry C Gibney
  • Alexandra Ysasi
  • Willi Wagner
  • Janeil Belle
  • Johannes C Schittny
  • Frieder Enzmann
  • Akira Tsuda
  • Steven J Mentzer
  • Moritz A Konerding
Autoren-URL
https://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=fis-test-1&SrcAuth=WosAPI&KeyUT=WOS:000338213400009&DestLinkType=FullRecord&DestApp=WOS_CPL
DOI
10.1007/s10456-013-9399-9
eISSN
1573-7209
Externe Identifier
  • Clarivate Analytics Document Solution ID: AK1XU
  • PubMed Identifier: 24150281
ISSN
0969-6970
Ausgabe der Veröffentlichung
3
Zeitschrift
ANGIOGENESIS
Schlüsselwörter
  • Intussusceptive angiogenesis
  • Pneumonectomy
  • Septal alveolarization
  • Corrosion cast
  • Synchrotron radiation tomographic microscopy
  • Lung surgery
Paginierung
541 - 551
Datum der Veröffentlichung
2014
Status
Published
Titel
Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization
Sub types
  • Article
Ausgabe der Zeitschrift
17

Data source: Web of Science (Lite)

Other metadata sources:
Autoren
  • Maximilian Ackermann
  • Jan P Houdek
  • Barry C Gibney
  • Alexandra Ysasi
  • Willi Wagner
  • Janeil Belle
  • Johannes C Schittny
  • Frieder Enzmann
  • Akira Tsuda
  • Steven J Mentzer
  • Moritz A Konerding
DOI
10.1007/s10456-013-9399-9
eISSN
1573-7209
ISSN
0969-6970
Ausgabe der Veröffentlichung
3
Zeitschrift
Angiogenesis
Sprache
en
Online publication date
2013
Paginierung
541 - 551
Datum der Veröffentlichung
2014
Status
Published
Herausgeber
Springer Science and Business Media LLC
Herausgeber URL
http://dx.doi.org/10.1007/s10456-013-9399-9
Datum der Datenerfassung
2019
Titel
Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization
Ausgabe der Zeitschrift
17

Data source: Crossref

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.
Addresses
  • Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg-University Mainz, 55128, Mainz, Germany.
Autoren
  • Maximilian Ackermann
  • Jan P Houdek
  • Barry C Gibney
  • Alexandra Ysasi
  • Willi Wagner
  • Janeil Belle
  • Johannes C Schittny
  • Frieder Enzmann
  • Akira Tsuda
  • Steven J Mentzer
  • Moritz A Konerding
DOI
10.1007/s10456-013-9399-9
eISSN
1573-7209
Externe Identifier
  • PubMed Identifier: 24150281
  • PubMed Central ID: PMC4061467
Funding acknowledgements
  • NHLBI NIH HHS: HL007734
  • NHLBI NIH HHS: R01 HL075426
  • NHLBI NIH HHS: HL75426
  • NHLBI NIH HHS: R01 HL047078
  • NHLBI NIH HHS: HL94567
  • NHLBI NIH HHS: T32 HL007734
  • NHLBI NIH HHS: R01 HL094567
Open access
true
ISSN
0969-6970
Ausgabe der Veröffentlichung
3
Zeitschrift
Angiogenesis
Schlüsselwörter
  • Pulmonary Alveoli
  • Animals
  • Mice, Inbred C57BL
  • Tomography
  • Pneumonectomy
  • Corrosion Casting
  • Neovascularization, Physiologic
  • Synchrotrons
  • Vascular Remodeling
Sprache
eng
Medium
Print-Electronic
Online publication date
2013
Open access status
Open Access
Paginierung
541 - 551
Datum der Veröffentlichung
2014
Status
Published
Publisher licence
CC BY
Datum der Datenerfassung
2013
Titel
Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization.
Sub types
  • Research Support, Non-U.S. Gov't
  • research-article
  • Journal Article
  • Research Support, N.I.H., Extramural
Ausgabe der Zeitschrift
17

Files

https://link.springer.com/content/pdf/10.1007/s10456-013-9399-9.pdf https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24150281/pdf/?tool=EBI https://europepmc.org/articles/PMC4061467?pdf=render

Data source: Europe PubMed Central

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.
Date of acceptance
2013
Autoren
  • Maximilian Ackermann
  • Jan P Houdek
  • Barry C Gibney
  • Alexandra Ysasi
  • Willi Wagner
  • Janeil Belle
  • Johannes C Schittny
  • Frieder Enzmann
  • Akira Tsuda
  • Steven J Mentzer
  • Moritz A Konerding
Autoren-URL
https://www.ncbi.nlm.nih.gov/pubmed/24150281
DOI
10.1007/s10456-013-9399-9
eISSN
1573-7209
Externe Identifier
  • PubMed Central ID: PMC4061467
Funding acknowledgements
  • NHLBI NIH HHS: HL007734
  • NHLBI NIH HHS: R01 HL047078
  • NHLBI NIH HHS: HL75426
  • NHLBI NIH HHS: R01 HL094567
  • NHLBI NIH HHS: HL94567
  • NHLBI NIH HHS: R01 HL075426
  • NHLBI NIH HHS: T32 HL007734
Ausgabe der Veröffentlichung
3
Zeitschrift
Angiogenesis
Schlüsselwörter
  • Animals
  • Corrosion Casting
  • Mice, Inbred C57BL
  • Neovascularization, Physiologic
  • Pneumonectomy
  • Pulmonary Alveoli
  • Synchrotrons
  • Tomography
  • Vascular Remodeling
Sprache
eng
Country
Germany
Paginierung
541 - 551
Datum der Veröffentlichung
2014
Status
Published
Datum, an dem der Datensatz öffentlich gemacht wurde
2015
Titel
Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization.
Sub types
  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
Ausgabe der Zeitschrift
17

Data source: PubMed

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