Implicit mechanistic role of the collagen, smooth muscle, and elastic tissue components in strengthening the air and blood capillaries of the avian lung

Abstract

To identify the forces that may exist in the parabronchus of the avian lung and that which may explain the reported strengths of the terminal respiratory units, the air capillaries and the blood capillaries, the arrangement of the parabronchial collagen fibers (CF) of the lung of the domestic fowl, Gallus gallus variant domesticus was investigated by discriminatory staining, selective alkali digestion, and vascular casting followed by alkali digestion. On the luminal circumference, the atrial and the infundibular CF are directly connected to the smooth muscle fibers and the elastic tissue fibers. The CF in this part of the parabronchus form the internal column (the axial scaffold), whereas the CF in the interparabronchial septa and those associated with the walls of the interparabronchial blood vessels form the external, i.e. the peripheral, parabronchial CF scaffold. Thin CF penetrate the exchange tissue directly from the interparabronchial septa and indirectly by accompanying the intraparabronchial blood vessels. Forming a dense network that supports the air and blood capillaries, the CF weave through the exchange tissue. The exchange tissue, specifically the air and blood capillaries, is effectively suspended between CF pillars by an intricate system of thin CF, elastic and smooth muscle fibers. The CF course through the basement membranes of the walls of the blood and air capillaries. Based on the architecture of the smooth muscle fibers, the CF, the elastic muscle fibers, and structures like the interparabronchial septa and their associated blood vessels, it is envisaged that dynamic tensional, resistive, and compressive forces exist in the parabronchus, forming a tensegrity (tension integrity) system that gives the lung rigidity while strengthening the air and blood capillaries.

Structural failures of the blood–gas barrier and the epithelial–epithelial cell connections in the different vascular regions of the lung of the domestic fowl, Gallus gallus variant domesticus, at rest and during exercise

“…After comparing the strengths (stress tolerance) of the blood capillaries in the rabbit lungs, the dog lungs, and the horse lungs, Birks et al observed that stress failure may correlate with the thickness of the BGB (Birks et al, 1994), a property consistent with Laplace's relationship which states that wall stress is proportional to capillary radius but inversely proportional to wall thickness. We have demonstrated collagen fibers in the basement membrane of the BGB and the EECCs of the lung of the chicken (Maina et al, 2010) and immunolocalized type-IV collagen (Jimoh and Maina, 2013), a protein family of triple helical isoforms that form strong two-dimensional planar network of fibers (Timpl, 1989; Hudson et al, 1993; West, 2009), in the exchange tissue of the lung of the domestic fowl. The strength of the BGB of the mammalian lung has been attributed to presence of type-IV collagen in the basement membrane (Crouch et al, 1997; West and Mathieu-Costello, 1999; Maina and West, 2005; West, 2009).…”

The Effect of Membrane Thickness on a Microvascular Gas Exchange Unit

“…Inspired by nature, we are working towards the goal of building a platform analogous to the natural lung, a modular gas exchange system that has a low footprint, high-selectivity, and requires little energy. [ 16 ] Many methods have been developed to create vascular structures in soft materials for self-healing materials, tissue-growth, and autonomic cooling. [ 31 ] We have recently demonstrated the synthesis of biomimetic gas exchange units capable of capturing CO 2 .…”

Immuno-localization of type-IV collagen in the blood-gas barrier and the epithelial–epithelial cell connections of the avian lung

“…T-IVc is a distinctively high tensile strength, non-fibrillar, particularly molecularly well-organized form of collagen [22]. The T-IVc localized here in the BMs of the BGB and the E-ECCs, together with other possible forms of collagen, connects to the peripheral and the central parabronchial 'pillars' of CFs [13], with the gas ET being effectively 'suspended' between the 'columns'. A closely related family of proteins with similar amino acid sequences and similar chemical and physical properties [33], collagens, form 20 per cent of the total protein in mammals [34] and supporting cells [35].…”

“…Here, we noted that T-IVc exists within the relatively much thinner and less conspicuous BM of the E-ECCs and the epithelial cells connect periodically. The E-ECCs appear to form a part of an integrated support system of the avian lung [13], directly strengthening the ACs and indirectly strengthening the BCs. This study was funded by the National Research Foundation (NRF) of South Africa.…”