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Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution.

ABSTRACT: Two opposing selective pressures have shaped the evolution of the structure of the blood-gas barrier in air breathing vertebrates. The first pressure, which has been recognized for 100 years, is to facilitate diffusive gas exchange. This requires the barrier to be extremely thin and have a large area. The second pressure, which has only recently been appreciated, is to maintain the mechanical integrity of the barrier in the face of its extreme thinness. The most important tensile stress comes from the pressure within the pulmonary capillaries, which results in a hoop stress. The strength of the barrier can be attributed to the type IV collagen in the extracellular matrix. In addition, the stress is minimized in mammals and birds by complete separation of the pulmonary and systemic circulations. Remarkably, the avian barrier is about 2.5 times thinner than that in mammals and also is much more uniform in thickness. These advantages for gas exchange come about because the avian pulmonary capillaries are unique among air breathers in being mechanically supported externally in addition to the strength that comes from the structure of their walls. This external support comes from epithelial plates that are part of the air capillaries, and the support is available because the terminal air spaces in the avian lung are extremely small due to the flow-through nature of ventilation in contrast to the reciprocating pattern in mammals.

SUBMITTER: West JB

PROVIDER: S-EPMC2803621 | biostudies-literature | 2009 Dec

REPOSITORIES: biostudies-literature

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Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution.

West John B JB

American journal of physiology. Regulatory, integrative and comparative physiology 20090930 6

Two opposing selective pressures have shaped the evolution of the structure of the blood-gas barrier in air breathing vertebrates. The first pressure, which has been recognized for 100 years, is to facilitate diffusive gas exchange. This requires the barrier to be extremely thin and have a large area. The second pressure, which has only recently been appreciated, is to maintain the mechanical integrity of the barrier in the face of its extreme thinness. The most important tensile stress comes fr ...[more]

PMID: 19793953

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Project description:BACKGROUND:Montane birds which engage in elevational movements have evolved to cope with fluctuations in environmental hypoxia, through changes in physiological parameters associated with blood oxygen-carrying capacity such as haemoglobin concentration (Hb) and haematocrit (Hct). In particular, elevational migrants which winter at low elevations, encounter varying intensities of avian haemosporidian parasites as they traverse heterogeneous environments. Whilst high intensity parasite infections lead to anaemia, one can expect that the ability to cope with haemosporidian infections should be a key trait for elevational migrants that must be balanced against reducing the oxygen-carrying capacity of blood in response to high elevation. In this study, we explored the links between environmental hypoxia, migration, and disease ecology by examining natural variation in infections status and intensity of avian haemoporidians across a suite of Himalayan birds with different migratory strategies while controlling for host phylogeny. RESULTS:We found predictably large variation in haemoglobin levels across the elevational gradient and this pattern was strongly influenced by season and whether birds are elevational migrants. The overall malaria infection intensity declined with elevation whereas Hb and Hct decreased with increase in parasite intensity, suggesting an important role of malaria parasites on hypoxia stressed birds in high elevation environments. CONCLUSIONS:Our results provide a key insight into how physiological measures and sub-clinical infections might affect dynamics of high-elevation bird populations. We suggest a potential impact of avian elevational migration on disease dynamics and exposure to high intensity infections with disease spread in the face of climate change, which will exacerbate hypoxic stress and negative effects of chronic avian malaria infection on survival and reproductive success in wild birds. Future work on chronic parasite infections must consider parasite intensity, rather than relying on infection status alone.

Project description:ObjectivesAcute respiratory distress syndrome represents the devastating result of acute lung injury, with high mortality. Limited methods are available for rehabilitation of lungs affected by acute respiratory distress syndrome. Our laboratory has demonstrated rehabilitation of sepsis-injured lungs via normothermic ex vivo and in vivo perfusion with Steen solution (Steen). However, mechanisms responsible for the protective effects of Steen remain unclear. This study tests the hypothesis that Steen directly attenuates pulmonary endothelial barrier dysfunction and inflammation induced by lipopolysaccharide.MethodsPrimary pulmonary microvascular endothelial cells were exposed to lipopolysaccharide for 4 hours and then recovered for 8 hours in complete media (Media), Steen, or Steen followed by complete media (Steen/Media). Oxidative stress, chemokines, permeability, interendothelial junction proteins, and toll-like receptor 4-mediated pathways were assessed in pulmonary microvascular endothelial cells using standard methods.ResultsLipopolysaccharide treatment of pulmonary microvascular endothelial cells and recovery in Media significantly induced reactive oxygen species, lipid peroxidation, expression of chemokines (eg, chemokine [C-X-C motif] ligand 1 and C-C motif chemokine ligand 2) and cell adhesion molecules (P-selectin, E-selectin, and vascular cell adhesion molecule 1), permeability, neutrophil transmigration, p38 mitogen-activated protein kinase and nuclear factor kappa B signaling, and decreased expression of tight and adherens junction proteins (zonula occludens-1, zonula occludens-2, and vascular endothelial-cadherin). All of these inflammatory pathways were significantly attenuated after recovery of pulmonary microvascular endothelial cells in Steen or Steen/Media.ConclusionsSteen solution preserves pulmonary endothelial barrier function after lipopolysaccharide exposure by promoting an anti-inflammatory environment via attenuation of oxidative stress, toll-like receptor 4-mediated signaling, and conservation of interendothelial junctions. These protective mechanisms offer insight into the advancement of methods for in vivo lung perfusion with Steen for the treatment of severe acute respiratory distress syndrome.

Dataset Information

Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution.

Publications

Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution.

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