Developmental dynamics of the bronchial (airway) and air sac systems of the avian respiratory system from day�3 to day 26 of life: a scanning electron microscopic study of the domestic fowl, Gallus gallus variant domesticus

Maina, John N.

doi:10.1007/s00429-003-0333-6

Cited by 39 publications

(29 citation statements)

References 35 publications

(36 reference statements)

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“…Among the extant vertebrate taxa, the avian lung is reported to be the most efficient and complex gas exchanger and is a CCGS [47], [48]. Microscopy was used to identify the functional development of the avian lung in 2006 and showed establishment of a thin BGB by the time of hatching [8], [49]–[52]. However, the lung of various domestic chicks begins to develop at E18 [8].…”

Section: Discussionmentioning

confidence: 99%

Hypoxia-Induced miR-15a Promotes Mesenchymal Ablation and Adaptation to Hypoxia during Lung Development in Chicken

Hao

et al. 2014

PLoS ONE

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The lungs undergo changes that are adaptive for high elevation in certain animal species. In chickens, animals bred at high elevations (e.g., Tibet chickens) are better able to hatch and survive under high-altitude conditions. In addition, lowland chicken breeds undergo physiological effects and suffer greater mortality when they are exposed to hypoxic conditions during embryonic development. Although these physiological effects have been noted, the mechanisms that are responsible for hypoxia-induced changes in lung development and function are not known. Here we have examined the role of a particular microRNA (miRNA) in the regulation of lung development under hypoxic conditions. When chicks were incubated in low oxygen (hypoxia), miR-15a was significantly increased in embryonic lung tissue. The expression level of miR-15a in hypoxic Tibet chicken embryos increased and remained relatively high at embryonic day (E)16–20, whereas in normal chickens, expression increased and peaked at E19–20, at which time the cross-current gas exchange system (CCGS) is developing. Bcl-2 was a translationally repressed target of miR-15a in these chickens. miR-16, a cluster and family member of miR-15a, was detected but did not participate in the posttranscriptional regulation of bcl-2. Around E19, the hypoxia-induced decrease in Bcl-2 protein resulted in apoptosis in the mesenchyme around the migrating tubes, which led to an expansion and migration of the tubes that would become the air capillary network and the CCGS. Thus, interfering with miR-15a expression in lung tissue may be a novel therapeutic strategy for hypoxia insults and altitude adaptation.

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Section: Discussionmentioning

confidence: 99%

Hypoxia-Induced miR-15a Promotes Mesenchymal Ablation and Adaptation to Hypoxia during Lung Development in Chicken

Hao

et al. 2014

PLoS ONE

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“…At maturity, however, the total number of air sacs is smaller because some of the air sacs merge. The primordia of the abdominal air sacs appear between days 5 and 7 of incubation while those of the cervical air sacs appear between days 6 and 8 (Maina 2003b). From day 15, the abdominal air sacs are the largest air sacs.…”

Section: Air Sacsmentioning

confidence: 97%

The design of the avian respiratory system: development, morphology and function

Maina

2015

J Ornithol

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The avian respiratory apparatus is separated into a gas exchanger (the lung) and ventilators (the air sacs). Synchronized bellows-like movements of the cranial and caudal air sacs ventilate the lung continuously and unidirectionally in a caudocranial direction. With the lungs practically rigid, after their insertion into the ribs and the vertebrae and on attaching to the membranous horizontal septum, surface tension is not a constraining factor to the intensity that the gas exchange tissue can subdivide. Delicate, transparent, capacious and avascular, the air sacs are not directly involved in gas exchange. The airway system comprises of a three-tiered system of passageways, namely a primary bronchus, the secondary bronchi and the tertiary bronchi (parabronchi). The crosscurrent system is formed by the perpendicular arrangement between the mass (convective) air flow in the parabronchial lumen and the centripetal (inward) flow of the venous blood in the exchange tissue; the countercurrent system consists of the centrifugal (outward) flow of air from the parabronchial lumen into the air capillaries and the centripetal (inward) flow of blood in the blood capillaries, and; the multicapillary serial arterialization system is formed by the blood capillaries and the air capillaries where venous blood is oxygenated in succession at the infinite number of points where the respiratory units contact exchange tissue. Together with the aforementioned systems, features like large capillary blood volume, extensive respiratory surface area and thin bloodgas barrier accord high pulmonary diffusing capacity of O 2 that supports the high metabolic capacities and energetic lifestyles of birds.

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“…Around this time, the chicken fetus internally pips by piercing the air cell inner membrane with its beak and begins lung ventilation [22] . Although during internal pipping, gas exchange is still partly dependent on the chorioallantoic membrane, the fetal lung is considered structurally and functionally mature [34,40] . Whether changes in prenatal oxygen environment would affect the structural maturation of the developing chicken lung warrants further investigation.…”

Section: Discussionmentioning

confidence: 99%

Pulmonary Vascular Endothelial Growth Factor Expression and Disaturated Phospholipid Content in a Chicken Model of Hypoxia-Induced Fetal Growth Restriction

et al. 2009

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Background: Prenatal hypoxia is an important cause of intrauterine growth retardation that affects fetal lung maturation, although previous studies have rendered conflicting results. The fetal chicken model allows the study of the isolated effects of hypoxia during development. Objectives: We hypothesized that prenatal hypoxia would differentially affect surfactant synthesis, depending on timing and duration of hypoxia. Pulmonary vascular endothelial growth factor (VEGF) expression was analyzed as a possible link between oxygen sensing and surfactant production. Methods: Fertilized White Leghorn eggs were incubated in normoxia, hyperoxia (60% O₂) from day 15 or hypoxia (15% O₂) from either day 6 or day 15 of incubation. Whole lung disaturated phospholipids (DSPL) and mRNA expression of VEGF isoforms were quantified at day 16 and 19. Results: Lung DSPL content increased approximately threefold between day 16 and 19 in control animals. Both hypoxia and hyperoxia from day 15 significantly increased DSPL content at day 19 versus control (103 ± 22 and 116 ± 18 vs. 81 ± 15 µg/mg protein, p < 0.01 and p < 0.001, respectively), while long-term hypoxia tended to decrease DSPL content (65 ± 17 µg/mg protein, p = 0.056). No differences in DSPL content were observed at day 16. Short-term hypoxia transiently up-regulated VEGF146 1.5-fold at day 16 (p < 0.05). A similar trend was observed for VEGF122 (p = 0.058) and VEGF190 (p = 0.08), while no differences were present at day 19. Conclusions: Both prenatal hypoxia and hyperoxia induced during critical windows of lung development differentially modulate surfactant synthesis. Our data support the concept that fetal oxygen tension is a key signal in the regulation of the surfactant system.

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Developmental dynamics of the bronchial (airway) and air sac systems of the avian respiratory system from day�3 to day 26 of life: a scanning electron microscopic study of the domestic fowl, Gallus gallus variant domesticus

Cited by 39 publications

References 35 publications

Hypoxia-Induced miR-15a Promotes Mesenchymal Ablation and Adaptation to Hypoxia during Lung Development in Chicken

Hypoxia-Induced miR-15a Promotes Mesenchymal Ablation and Adaptation to Hypoxia during Lung Development in Chicken

The design of the avian respiratory system: development, morphology and function

Pulmonary Vascular Endothelial Growth Factor Expression and Disaturated Phospholipid Content in a Chicken Model of Hypoxia-Induced Fetal Growth Restriction

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