Skip to main content

Prenatal and Postnatal Development of the Vertebrate Blood–Gas Barrier

  • Chapter
  • First Online:
The Vertebrate Blood-Gas Barrier in Health and Disease

Abstract

The vertebrate lung inaugurates as a primitive endodermal bud from the ventral aspect of the primitive foregut. The bud divides into primitive airways that form gas exchanging chambers, where a thin blood–gas barrier (BGB) is accomplished. Salient differences have been observed between the development of the compliant mammalian lung and the noncompliant avian one. In the former, formation of BGB entails conversion of columnar cells of the migrating tubes to primitive type II cells and lowering of the apical intercellular tight junctions so that the gaps between the cells enlarge. The latter cells give rise to the definitive alveolar type II (AT-II) and type I (AT-I) cells. Extrusion of the lamellar bodies thinning and stretching of the cells attains the squamous phenotype, characteristic of AT-I cells. Diminution of interstitial tissue, fusion of capillaries, and apposition of capillaries to the alveolar epithelium results in formation of a thin BGB. In birds, attenuation proceeds through cell-cutting processes, referred to as secarecytosis. Several morphoregulatory molecules including transcription factors such as Nkx2.1, GATA, HNF-3, WNT5a, signaling molecules including FGF, BMP-4, Shh and TFG-β, and extracellular matrix proteins and their receptors have been implicated. In the postnatal period, alterations in the BGB may occur during late phases of alveolarization or as repair subsequent to lung injury. Such changes are effected through rapid changes in expression of the relevant genes and consequent structural alterations. While an appreciable amount of data regarding molecular control of lung development in mammals exists, the information on avian species is scanty.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AC:

Air capillaries

AT-I:

Alveolar type I cell

AT-II:

Alveolar type II cell

BC:

Blood capillaries

bFGF:

Basic fibroblast growth factor

BGB:

Blood gas barrier

BMP-4:

Bone morphogenetic protein 4

CCSP:

Clara cell secretory protein

ECM:

Extracellular matrix

EGF:

Epithelial growth factor

EGFR:

Epithelial growth factor receptor

ELF5:

E74-like factor 5

ErbB:

Epidermal growth factor receptor

ERK:

Extracellular signal-regulated kinases

ETS:

E26 transformation-specific family

FGF:

Fibroblast growth factor

FGFRs:

Fibroblast growth factor receptors

FosB:

FBJ murine osteosarcoma viral oncogene homolog B

FOX:

Forkhead orthologs

GR:

Glucocorticoid receptor

HA:

Human influenza hemagglutinin

HIF2α:

Hypoxia inducible factor 2α

HNF-3:

Hepatocyte nuclear factor

MPK-1:

Mitogen-activated protein kinase

mRNA:

Messenger RNA

mutHIF2α:

Mutant hypoxia inducible factor 2α

NICD:

Notch intracellular domain

PDGF:

Platelet derived growth factor

RA:

Retinoic acid

RAR:

Retinoic acid receptor

Sema3A:

Semaphorin 3A

Shh:

Sonic hedge hog

SMA:

Smooth muscle actin

SP:

Surfactant proteins

TFG-β:

Transforming growth factor β

TGF-β1:

Transforming growth factor β1

TTF-1:

Thyroid transcription factor 1

VEGF:

Vascular endothelial growth factor

WNT5a:

Wingless type 5a

References

  • Anderson-Berry A, O’Brien EA, Bleyl SB, Lawson A, Gundersen N, Ryssman D, Sweeley J, Dahl MJ, Drake CJ, Schoenwolf GC, Albertine KH. Vasculogenesis drives pulmonary vascular growth in the developing chick embryo. Dev Dyn. 2005;233:145–53.

    Article  CAS  PubMed  Google Scholar 

  • Aumuller G, Wilhelm B. Seitz J. Apocrine secretion—fact or artifact? Ann Anat. 1999;181:437–46.

    Article  CAS  PubMed  Google Scholar 

  • Becker PM, Tran TS, Delannoy MJ, He C, Shannon JM, McGrath-Morrow S. Semaphorin 3A contributes to distal pulmonary epithelial cell differentiation and lung morphogenesis. PLoS ONE. 2011;6:e27449.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bellairs R, Osmond M. The atlas of chick development. New York: Academic; 1998.

    Google Scholar 

  • Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BL. Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development. 1996;122:1693–702.

    CAS  PubMed  Google Scholar 

  • Berg JT, Fu Z, Breen EC, Tran HC, Mathieu-Costello O, West JB. High lung inflation increases mRNA levels of ECM components and growth factors in lung parenchyma. J Appl Physiol. 1997;83:120–8.

    CAS  PubMed  Google Scholar 

  • Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, West JB. Comparative aspects of the strength of pulmonary capillaries in rabbit, dog, and horse. Respir Physiol. 1994;97:235–46.

    Article  CAS  PubMed  Google Scholar 

  • Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, West JB. Very high pressures are required to cause stress failure of pulmonary capillaries in thoroughbred racehorses. J Appl Physiol. 1997;82:1584–92.

    CAS  PubMed  Google Scholar 

  • Burri PH. Fetal and postnatal development of the lung. Annu Rev Physiol. 1984;46:617–28.

    Article  CAS  PubMed  Google Scholar 

  • Burri PH, Weibel ER. Ultrastructure and morphometry of the developing lung. In: Hudson WA, editor. Development of the lung. New York: Mercwel Dekker; 1977; p. 215–268.

    Google Scholar 

  • Burri PH, Haenni B, Tschanz SA, Makanya AN. Morphometry and allometry of the postnatal marsupial lung development: an ultrastructural study. Respir Physiol Neurobiol. 2003;138(2–3):309–24.

    Google Scholar 

  • Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473:298–307.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cole TJ, Solomon NM, Van Driel R, Monk JA, Bird D, Richardson SJ, Dilley RJ, Hooper SB. Altered epithelial cell proportions in the fetal lung of glucocorticoid receptor null mice. Am J Respir Cell Mol Biol. 2004;30:613–9.

    Article  CAS  PubMed  Google Scholar 

  • Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, Nemery B, Dewerchin M, Van Veldhoven P, Plate K, Moons L, Collen D, Carmeliet P. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med. 2002;8:702–10.

    Article  CAS  PubMed  Google Scholar 

  • Dang TP, Eichenberger S, Gonzalez A, Olson S, Carbone DP. Constitutive activation of Notch3 inhibits terminal epithelial differentiation in lungs of transgenic mice. Oncogene. 2003;22:1988–97.

    Article  CAS  PubMed  Google Scholar 

  • Demayo F, Minoo P, Plopper CG, Schuger L, Shannon J, Torday JS. Mesenchymal–epithelial interactions in lung development and repair: are modeling and remodeling the same process? Am J Physiol Lung Cell Mol Physiol. 2002;283:L510–7.

    Article  CAS  PubMed  Google Scholar 

  • Devriendt K, Vanhole C, Matthijs G, de Zegher F. Deletion of thyroid transcription factor-1 gene in an infant with neonatal thyroid dysfunction and respiratory failure. N Engl J Med. 1998;338:1317–8.

    Article  CAS  PubMed  Google Scholar 

  • Deyrup-Olsen I, Luchtel DL. Secretion of mucous granules and other membrane-bound structures: a look beyond exocytosis. Int Rev Cytol. 1998;183:95–141.

    Article  CAS  PubMed  Google Scholar 

  • Fernandes MN, da Cruz AL, da Costa OT, Perry SF. Morphometric partitioning of the respiratory surface area and diffusion capacity of the gills and swim bladder in juvenile Amazonian air-breathing fish, Arapaima gigas. Micron. 2012;43:961–70.

    Article  PubMed  Google Scholar 

  • Fleetwood JN, Munnell JF. Morphology of the airways and lung parenchyma in hatchlings of the loggerhead sea turtle, Caretta caretta. J Morphol. 1996;227:289–304.

    Article  Google Scholar 

  • Gehr P, Bachofen M, Weibel ER. The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir Physiol. 1978;32:121–40.

    Article  CAS  PubMed  Google Scholar 

  • Gesase AP, Satoh Y. Apocrine secretory mechanism: recent findings and unresolved problems. Histol Histopathol. 2003;18:597–608.

    CAS  PubMed  Google Scholar 

  • Guseh JS, Bores SA, Stanger BZ, Zhou Q, Anderson WJ, Melton DA, Rajagopal J. Notch signaling promotes airway mucous metaplasia and inhibits alveolar development. Development. 2009;136:1751–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Henk WG, Haldiman JT. Microanatomy of the lung of the bowhead whale Balaena mysticetus. Anat Rec. 1990;226:187–97.

    Article  CAS  PubMed  Google Scholar 

  • Herbert SP, Stainier DYR. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol. 2011;12:551–64.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Herriges JC, Yi L, Hines EA, Harvey JF, Xu G, Gray PA, Ma Q, Sun X. Genome-scale study of transcription factor expression in the branching mouse lung. Dev Dyn. 2012;241(9):1432–53.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hopkins SR, Schoene RB, Henderson WR, Spragg RG, Martin TR, West JB. Intense exercise impairs the integrity of the pulmonary blood–gas barrier in elite athletes. Am J Respir Crit Care Med. 1997;155:1090–4.

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Wang Y, Nayak PS, Dammann CE, Sanchez-Esteban J. Stretch-induced fetal type II cell differentiation is mediated via ErbB1–ErbB4 interactions. J Biol Chem. 2012a;287:18091–102.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang Y, Kempen MB, Munck AB, Swagemakers S, Driegen S, Mahavadi P, Meijer D, van IW, van der Spek P, Grosveld F, Gunther A, Tibboel D, Rottier RJ. Hypoxia-inducible factor 2-alpha plays a critical role in the formation of alveoli and surfactant. Am J Respir Cell Mol Biol. 2012b;46:224–32.

    Article  CAS  PubMed  Google Scholar 

  • Johnston SD, Daniels CB, Cenzato D, Whitsett JA, Orgeig S. The pulmonary surfactant system matures upon pipping in the freshwater turtle Chelydra serpentina. J Exp Biol. 2002;205:415–25.

    PubMed  Google Scholar 

  • Keijzer R, van Tuyl M, Meijers C, Post M, Tibboel D, Grosveld F, Koutsourakis M. The transcription factor GATA6 is essential for branching morphogenesis and epithelial cell differentiation during fetal pulmonary development. Development. 2001;128:503–11.

    CAS  PubMed  Google Scholar 

  • Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev. 1996;10:60–9.

    Article  CAS  PubMed  Google Scholar 

  • Kliewer M, Fram EK, Brody AR, Young SL. Secretion of surfactant by rat alveolar type II cells: morphometric analysis and three-dimensional reconstruction. Exp Lung Res. 1985;9:351–61. (1996)

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Fryer JD, Kang H, Crespo-Barreto J, Bowman AB, Gao Y, Kahle JJ, Hong JS, Kheradmand F, Orr HT, Finegold MJ, Zoghbi HY. ATXN1 protein family and CIC regulate extracellular matrix remodeling and lung alveolarization. Dev Cell. 2011;21:746–57.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu C, Ikegami M, Stahlman MT, Dey CR, Whitsett JA. Inhibition of alveolarization and altered pulmonary mechanics in mice expressing GATA-6. Am J Physiol Lung Cell Mol Physiol. 2003;285:L1246–54.

    Article  CAS  PubMed  Google Scholar 

  • Loscertales M, Mikels AJ, Hu JK, Donahoe PK, Roberts DJ. Chick pulmonary Wnt5a directs airway and vascular tubulogenesis. Development. 2008;135:1365–76.

    Article  CAS  PubMed  Google Scholar 

  • Macuhova J, Tancin V, Bruckmaier RM. Effects of oxytocin administration on oxytocin release and milk ejection. J Dairy Sci. 2004;87:1236–44.

    Article  CAS  PubMed  Google Scholar 

  • Maeda Y, Dave V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev. 2007;87:219–44.

    Article  CAS  PubMed  Google Scholar 

  • Maina JN. The morphology of the lung of the black mamba Dendroaspis polylepis (Reptilia: Ophidia: Elapidae). A scanning and transmission electron microscopic study. J Anat. 1989a;167:31–46.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maina JN. The morphology of the lung of the East African tree frog Chiromantis petersi with observations on the skin and the buccal cavity as secondary gas exchange organs: a TEM and SEM study. J Anat. 1989b;165:29–43.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maina JN. Structure, function and evolution of the gas exchangers: comparative perspectives. J Anat. 2002;201:281–304.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maina JN. A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus. Tissue Cell. 2003;35:375–91.

    Article  CAS  PubMed  Google Scholar 

  • Maina JN, King AS. A morphometric study of the lung of a Humboldt penguin (Sphenicus humboldti). Anat Histol Embryol. 1987;16:293–7.

    CAS  PubMed  Google Scholar 

  • Maina JN, King AS. The lung of the emu, Dromaius novaehollandiae: a microscopic and morphometric study. J Anat. 1989;163:67–73.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maina JN, Nathaniel C. A qualitative and quantitative study of the lung of an ostrich, Struthio camelus. J Exp Biol. 2001;204:2313–30.

    CAS  PubMed  Google Scholar 

  • Maina JN, West JB. Thin and strong! The bioengineering dilemma in the structural and functional design of the blood–gas barrier. Physiol Rev. 2005;85:811–44.

    Article  CAS  PubMed  Google Scholar 

  • Maina JN, Thomas SP, Hyde DM. A morphometric study of the lungs of different sized bats: correlations between structure and function of the chiropteran lung. Philos Trans R Soc Lond B Biol Sci. 1991;333:31–50.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Djonov V. Development and spatial organization of the air conduits in the lung of the domestic fowl, Gallus gallus variant domesticus. Microsc Res Tech. 2008;71:689–702.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Djonov V. Parabronchial angioarchitecture in developing and adult chickens. J Appl Physiol. 2009;106:1959–69.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Sparrow MP, Warui CN, Mwangi DK, Burri PH. Morphological analysis of the postnatally developing marsupial lung: the quokka wallaby. Anat Rec. 2001;262:253–65.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Hlushchuk R, Duncker HR, Draeger A, Djonov V. Epithelial transformations in the establishment of the blood–gas barrier in the developing chick embryo lung. Dev Dyn. 2006;235:68–81.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Hlushchuk R, Baum O, Velinov N, Ochs M, Djonov V. Microvascular endowment in the developing chicken embryo lung. Am J Physiol Lung Cell Mol Physiol. 2007a;292:L1136–46.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Tschanz SA, Haenni B, Burri PH. Functional respiratory morphology in the newborn quokka wallaby (Setonix brachyurus). J Anat. 2007b;211:26–36.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Makanya AN, Hlushchuk R, Djonov V. The pulmonary blood–gas barrier in the avian embryo: inauguration, development and refinement. Respir Physiol Neurobiol. 2011;178:30–8.

    Article  CAS  PubMed  Google Scholar 

  • Makanya AN, Koller T, Hlushchuk R, Djonov V. Pre-hatch lung development in the ostrich. Respir Physiol Neurobiol. 2012;180:183–92.

    Article  CAS  PubMed  Google Scholar 

  • Makanya A, Anagnostopoulou A, Djonov V. Development and remodeling of the vertebrate blood–gas barrier. Biomed Res Int. 2013;2013:101597.

    Article  PubMed Central  PubMed  Google Scholar 

  • Massaro GD, Massaro D, Chambon P. Retinoic acid receptor-alpha regulates pulmonary alveolus formation in mice after, but not during, perinatal period. Am J Physiol Lung Cell Mol Physiol. 2003;284:L431–L3.

    Article  CAS  PubMed  Google Scholar 

  • Meban C. Thickness of the air–blood barriers in vertebrate lungs. J Anat. 1980;131:299–307.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mercurio AR, Rhodin JA. An electron microscopic study on the type I pneumocyte in the cat: pre-natal morphogenesis. J Morphol. 1978;156:141–55.

    Article  CAS  PubMed  Google Scholar 

  • Metzger DE, Stahlman MT, Shannon JM. Misexpression of ELF5 disrupts lung branching and inhibits epithelial differentiation. Dev Biol. 2008;320:149–60.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miettinen PJ, Warburton D, Bu D, Zhao JS, Berger JE, Minoo P, Koivisto T, Allen L, Dobbs L, Werb Z, Derynck R. Impaired lung branching morphogenesis in the absence of functional EGF receptor. Dev Biol. 1997;186:224–36.

    Article  CAS  PubMed  Google Scholar 

  • Millien G, Spira A, Hinds A, Wang J, Williams MC, Ramirez MI. Alterations in gene expression in T1 alpha null lung: a model of deficient alveolar sac development. BMC Dev Biol. 2006;6:35.

    Article  PubMed Central  PubMed  Google Scholar 

  • Moura RS, Coutinho-Borges JP, Pacheco AP, Damota PO, Correia-Pinto J. FGF signaling pathway in the developing chick lung: expression and inhibition studies. PLoS ONE. 2011;6:e17660.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mucenski ML, Wert SE, Nation JM, Loudy DE, Huelsken J, Birchmeier W, Morrisey EE, Whitsett JA. Beta-catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J Biol Chem. 2003;278:40231–8.

    Article  CAS  PubMed  Google Scholar 

  • Nagata K, Masumoto K, Esumi G, Teshiba R, Yoshizaki K, Fukumoto S, Nonaka K, Taguchi T. Connexin43 plays an important role in lung development. J Pediatr Surg. 2009;44:2296–301.

    Article  PubMed  Google Scholar 

  • Parker JC, Breen EC, West JB. High vascular and airway pressures increase interstitial protein mRNA expression in isolated rat lungs. J Appl Physiol. 1997;83:1697–705.

    CAS  PubMed  Google Scholar 

  • Perry SF. Gas exchange strategy in the Nile crocodile: a morphometric study. J Comp Physiol B: Biochen Syst Eviron Physiol. 1990;159:761–9.

    Article  Google Scholar 

  • Raaberg L, Nexo E, Jorgensen PE, Poulsen SS, Jakab M. Fetal effects of epidermal growth factor deficiency induced in rats by autoantibodies against epidermal growth factor. Pediatr Res. 1995;37:175–81.

    Article  CAS  PubMed  Google Scholar 

  • Ravikumar P, Bellotto DJ, Johnson RL Jr, Hsia CC. Permanent alveolar remodeling in canine lung induced by high-altitude residence during maturation. J Appl Physiol. 2009;107:1911–7.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sakiyama J, Yamagishi A, Kuroiwa A. Tbx4-Fgf10 system controls lung bud formation during chicken embryonic development. Development. 2003;130:1225–34.

    Article  CAS  PubMed  Google Scholar 

  • Scheuermann DW, Klika E, de Groodt-Lasseel MH, Bazantova I, Switka A. The development and differentiation of the parabronchial unit in quail (Coturnix coturnix). Eur J Morphol. 1998;36:201–15.

    Article  CAS  PubMed  Google Scholar 

  • Schittny JC, Burri PH. Morphogenesis of the mammalian lung: aspects of structure and extracellular matrix. In: Massaro JD, Massaro G, Chambon P, editors. Lung development and regeneration. New York: Mercel Dekker; 2003. p. 275–317.

    Google Scholar 

  • Schittny JC, Burri PH. Development and growth of the lung. In: Fishman AP, Elias JA, A. FJ, Grippi MA, Kaiser LR, Senior RM, editors. Fishman’s pulmonary diseases and disorders. New-York: McGraw-Hill; 2008. p. 91–114.

    Google Scholar 

  • Schittny JC, Djonov V, Fine A, Burri PH. Programmed cell death contributes to postnatal lung development. Am J Respir Cell Mol Biol. 1998;18:786–93.

    Article  CAS  PubMed  Google Scholar 

  • Schittny JC, Miserocchi G, Sparrow MP. Spontaneous peristaltic airway contractions propel lung liquid through the bronchial tree of intact and fetal lung explants. Am J Respir Cell Mol Biol. 2000;23:11–8.

    Article  CAS  PubMed  Google Scholar 

  • Shannon JM, Hyatt BA. Epithelial–mesenchymal interactions in the developing lung. Annu Rev Physiol. 2004;66:625–45.

    Article  CAS  PubMed  Google Scholar 

  • Shook D, Keller R. Mechanisms, mechanics and function of epithelial–mesenchymal transitions in early development. Mech Dev. 2003;120:1351–83.

    Article  CAS  PubMed  Google Scholar 

  • Stoeckelhuber M, Sliwa A, Welsch U. Histo-physiology of the scent-marking glands of the penile pad, anal pouch, and the forefoot in the aardwolf (Proteles cristatus). Anat Rec. 2000;259:312–26.

    Article  CAS  PubMed  Google Scholar 

  • Stoeckelhuber M, Stoeckelhuber BM, Welsch U. Human glands of Moll: histochemical and ultrastructural characterization of the glands of moll in the human eyelid. J Invest Dermatol. 2003;121:28–36.

    Article  CAS  PubMed  Google Scholar 

  • Tsao PN, Chen F, Izvolsky KI, Walker J, Kukuruzinska MA, Lu J, Cardoso WV. Gamma-secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung. J Biol Chem. 2008;283:29532–44.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tschanz SA, Makanya AN, Haenni B, Burri PH. Effects of neonatal high-dose short-term glucocorticoid treatment on the lung: a morphologic and morphometric study in the rat. Pediatr Res. 2003;53:72–80.

    Article  CAS  PubMed  Google Scholar 

  • Tsukimoto K, Mathieu-Costello O, Prediletto R, Elliott AR, West JB. Ultrastructural appearances of pulmonary capillaries at high transmural pressures. J Appl Physiol. 1991;71:573–82.

    CAS  PubMed  Google Scholar 

  • Volberg T, Geiger B, Kartenbeck J, Franke WW. Changes in membrane-microfilament interaction in intercellular adherens junctions upon removal of extracellular Ca2+ ions. J Cell Biol. 1986;102:1832–42.

    Article  CAS  PubMed  Google Scholar 

  • Wan H, Xu Y, Ikegami M, Stahlman MT, Kaestner KH, Ang SL, Whitsett JA. Foxa2 is required for transition to air breathing at birth. Proc Natl Acad Sci U S A. 2004;101:14449–54.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wan H, Dingle S, Xu Y, Besnard V, Kaestner KH, Ang SL, Wert S, Stahlman MT, Whitsett JA. Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. J Biol Chem. 2005;280:13809–16.

    Article  CAS  PubMed  Google Scholar 

  • Warburton D, Bellusci S, De Langhe S, Del Moral PM, Fleury V, Mailleux A, Tefft D, Unbekandt M, Wang K, Shi W. Molecular mechanisms of early lung specification and branching morphogenesis. Pediatr Res. 2005;57:26R–37R.

    Article  PubMed  Google Scholar 

  • Watson RR, Fu Z, West JB. Morphometry of the extremely thin pulmonary blood–gas barrier in the chicken lung. Am J Physiol Lung Cell Mol Physiol. 2007;292:L769–77.

    Article  CAS  PubMed  Google Scholar 

  • Weibel ER. The pathway for oxygen. Cambridge: Harvard University Press.

    Google Scholar 

  • Wells JM, Melton DA. Vertebrate endoderm development. Annu Rev Cell Dev Biol. 1999;15:393–410. (1984)

    Article  CAS  PubMed  Google Scholar 

  • West JB. Invited review: pulmonary capillary stress failure. J Appl Physiol. 2000;89:2483–9. (discussion 2497).

    CAS  PubMed  Google Scholar 

  • West JB. Comparative physiology of the pulmonary blood–gas barrier: the unique avian solution. Am J Physiol Regul Integr Comp Physiol. 2009;297:R1625–34.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • West JB, Mathieu-Costello O. Pulmonary blood–gas barrier—a physiological dilemma. News Physiol Sci. 1993;8:249–53.

    Google Scholar 

  • West JB, Mathieu-Costello O. Stress-induced injury of pulmonary capillaries. Proc Assoc Am Physicians. 1998;110:506–12.

    CAS  PubMed  Google Scholar 

  • West JB, Mathieu-Costello O. Structure, strength, failure, and remodeling of the pulmonary blood–gas barrier. Annu Rev Physiol. 1999;61:543–72.

    Article  CAS  PubMed  Google Scholar 

  • Wongtrakool C, Malpel S, Gorenstein J, Sedita J, Ramirez MI, Underhill TM, Cardoso WV. Down-regulation of retinoic acid receptor alpha signaling is required for sacculation and type I cell formation in the developing lung. J Biol Chem. 2003;278:46911–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang L, Naltner A, Yan C. Overexpression of dominant negative retinoic acid receptor alpha causes alveolar abnormality in transgenic neonatal lungs. Endocrinology. 2003;144:3004–11.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew Makanya .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Makanya, A., Djonov, V. (2015). Prenatal and Postnatal Development of the Vertebrate Blood–Gas Barrier. In: Makanya, A. (eds) The Vertebrate Blood-Gas Barrier in Health and Disease. Springer, Cham. https://doi.org/10.1007/978-3-319-18392-3_3

Download citation

Publish with us

Policies and ethics