The anatomy, physics, and physiology of gas exchange surfaces: is there a universal function for pulmonary surfactant in animal respiratory structures?

Abstract

(Orgeig and Daniels) This surfactant symposium reflects the integrative and multidisciplinary aims of the 1st ICRB, by encompassing in vitro and in vivo research, studies of vertebrates and invertebrates, and research across multiple disciplines. We explore the physical and structural challenges that face gas exchange surfaces in vertebrates and insects, by focusing on the role of the surfactant system. Pulmonary surfactant is a complex mixture of lipids and proteins that lines the air-liquid interface of the lungs of all air-breathing vertebrates, where it functions to vary surface tension with changing lung volume. We begin with a discussion of the extraordinary conservation of the blood-gas barrier among vertebrate respiratory organs, which has evolved to be extremely thin, thereby maximizing gas exchange, but simultaneously strong enough to withstand significant distension forces. The principal components of pulmonary surfactant are highly conserved, with a mixed phospholipid and neutral lipid interfacial film that is established, maintained and dynamically regulated by surfactant proteins (SP). A wide variation in the concentrations of individual components exists, however, and highlights lipidomic as well as proteomic adaptations to different physiological needs. As SP-B deficiency in mammals is lethal, oxidative stress to SP-B is detrimental to the biophysical function of pulmonary surfactant and SP-B is evolutionarily conserved across the vertebrates. It is likely that SP-B was essential for the evolutionary origin of pulmonary surfactant. We discuss three specific issues of the surfactant system to illustrate the diversity of function in animal respiratory structures. (1) Temperature: In vitro analyses of the behavior of different model surfactant films under dynamic conditions of surface tension and temperature suggest that, contrary to previous beliefs, the alveolar film may not have to be substantially enriched in the disaturated phospholipid, dipalmitoylphosphatidylcholine (DPPC), but that similar properties of rate of film formation can be achieved with more fluid films. Using an in vivo model of temperature change, a mammal that enters torpor, we show that film structure and function varies between surfactants isolated from torpid and active animals. (2) Spheres versus tubes: Surfactant is essential for lung stabilization in vertebrates, but its function is not restricted to the spherical alveolus. Instead, surfactant is also important in narrow tubular respiratory structures such as the terminal airways of mammals and the air capillaries of birds. (3). Insect tracheoles: We investigate the structure and function of the insect tracheal system and ask whether pulmonary surfactant also has a role in stabilizing these minute tubules. Our theoretical analysis suggests that a surfactant system may be required, in order to cope with surface tension during processes, such as molting, when the tracheae collapse and fill with water. Hence, despite observations by Wigglesworth in the 1930s of fluid-filled tr...

Synthetic Pulmonary Surfactant Preparations: New Developments and Future Trends

“…Efficient gas exchange requires a large enough surface to be continuously exposed to air while minimising the barriers for oxygen and carbon dioxide to diffuse between air and the blood compartment [1]. At the same time, a selection of combined defence mechanisms is required to help keep such an essentially exposed area sterile of potential pathogenic microorganisms.…”

Overcoming the pulmonary barrier: new insights to improve the efficiency of inhaled therapeutics

“…Their shape is rather cuboidal and they play a secretory role within the alveolar region. Indeed, pulmonary surfactant, a complex mixture of lipids and proteins that lines the alveolar surface, is synthesized, stored and secreted by type II pneumocytes (32,33). The main function of this surfactant layer is to avoid alveolar collapse by reducing surface tension within the alveoli, while the hydrophilic surfactant-associated proteins (SPs) A and D also play a role in the innate immune defense of the lungs (34,35).…”

Leptin integrates vertebrate evolution: From oxygen to the blood–gas barrier

“…As a result, the interaction of temperature with the physicochemical properties of the lipid mixture has evolutionarily constrained the surfactant system, and has driven the evolution of surfactant lipid composition. Temperature has selected both the broad-scale evolutionary differences in surfactant lipid composition between the vertebrate groups, and the acute changes in surfactant composition, structure and function within individuals (Lang et al, 2005; Orgeig et al, 2007). For example, those vertebrate groups with lower preferred body temperatures, i.e.…”

“…Moreover, these compositional and functional changes are reversible upon arousal (Codd et al 2003; Lopatko et al 1999). It has been recently shown that these functional changes correlate with structural differences at the molecular level of the surfactant film (Orgeig et al 2007). The molecular, biophysical and thermodynamic mechanisms underlying these differences are currently being investigated.…”