Pulmonary and gastric surfactants. A comparison of the effect of surface requirements on function and phospholipid composition

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Abstract

Surfactant is present in the alveoli and conductive airways of mammalian lungs. The presence of surface active agents was, moreover, demonstrated for avian tubular lungs and for the stomach and intestine. As the surface characteristics of these organs differ from each other, their surfactants possess distinct biochemical and functional characteristics. In the stomach so-called ‘gastric surfactant’ forms a hydrophobic barrier to protect the mucosa against acid back-diffusion. For this purpose gastric mucosal cells secrete unsaturated phosphatidylcholines (PC), but no dipalmitoyl-PC (PC16:0/16:0). By contrast, surfactant from conductive airways, lung alveoli and tubular avian lungs contain PC16:0/16:0 as their main component in similar concentrations. Hence, there is no biochemical relation between gastric and pulmonary surfactant. Alveolar surfactant, being designed for preventing alveolar collapse under the highly dynamic conditions of an oscillating alveolus, easily reaches values of <5 mN/m upon cyclic compression. Surfactants from tubular air-exposed structures, however, like the conductive airways of mammalian lungs and the exclusively tubular avian lung, display inferior compressibility as they only reach minimal surface tension values of approximately 20 mN/m. Hence, the highly dynamic properties of alveolar surfactant do not apply for surfactants designed for air–liquid interfaces of tubular lung structures.

Introduction

Since the discovery of surface tension as the primary cause of pulmonary retraction by von Neergaard (1929) and the pioneering work of Pattle and Clements characterising pulmonary surfactant (Clements, 1957, Pattle, 1958), much emphasis has been put on the functional and biochemical characterisation of surfactant in mammalian lungs, primarily due to the need of finding therapeutic strategies for treating intensive care patients (Obladen, 1992). However, in addition to its location and essential function in the alveolar regions of mammalian lungs, surfactant components have also been demonstrated on non-alveolar surfaces of the body. Such surfaces are either air-exposed, for instance conducting airways of mammalian lungs and air capillaries of avian lungs which lack any alveolar structures (Scheid and Piiper, 1971), or are covered with liquid, such as the stomach and gut. While all these epithelial surfaces are covered with a phospholipid-rich layer, the function of this layer differs considerably depending on its location (Hills, 1996, Ethell et al., 1999). Consequently, the phospholipid compositions of these various biological surfactants are also very different.

The role of pulmonary surfactant to maintain alveolar function in mammalian lungs is well recognised. The high resistance to compression of solid dipalmitoyl phosphatidylcholine (PC16:0/16:0), the major surface active component of lung surfactant, opposes surface tension forces in the alveolus, generates a very high surface pressure, and so prevents alveolar collapse at end expiration. This is critical for efficient respiration as, in the absence of surfactant, the collapsing pressure in the alveolus would increase in inverse proportion to alveolar radius (according to the law of Laplace applied to a sphere: P=2γ/r, where P=pressure, γ=surface tension, r=alveolar radius), so preventing alveolar expansion on inspiration. In addition, during inspiration surfactant has to fill into the gaps of the enlarging alveolar surface area. As the frequency of breathing in some mammalian species is extremely high (for instance >200/min for small rodents), and since the tidal volumes and breathing frequencies vary depending on metabolic activity of a given species, highly dynamic properties and good compressibility of the surfactant associated with the air–liquid interface are required to prevent alveolar collapse (Keough, 1992).

These properties, particularly the rapid, dynamic area change during the breathing cycle coupled with a very high surface area:volume ratio, are unique to the alveolus. No other epithelial surface undergoes comparable changes, and consequently other functions have been attributed to the phospholipid-rich surfactant layers lining those surfaces. The high surface pressure of the surfactant has been proposed both to keep open the non-cartilagenous conducting airways of mammalian lungs and to prevent oedema and mucus plugging of such airways (Enhorning, 1996). It may also serve a comparable function in the tubular gas-exchange regions of the non-alveolar avian lung (Daniels et al., 1998). In contrast, so-called gastric surfactant, synthesised and secreted from cells of the gastric mucosa, is thought to form a barrier to prevent back-diffusion of hydrogen ions and consequent damage to mucosal surfaces in the stomach (Lichtenberger, 1995, Hills, 1996). While surface adsorption is an essential requirement for any surface-active agent, on air-exposed alveolar and tubular lung structures as well as on gastrointestinal surfaces, characteristics of compressibility and achievement of minimal surface tension (γmin) values below 5 mN/m upon compression may only apply for the pulsating lung alveolus.

We have previously reported the molecular compositions of surface-active phospholipids isolated from mucosal surfaces of the rat and pig stomach (Bernhard et al., 1995) and the molecular compositions and functional properties of airway surfactant isolated from the pig lung (Bernhard et al., 1997). Here we contrast the molecular species compositions of lung and gastric surfactants from the pig and the rat, and compare surface tension function and phospholipid composition of duck and chicken lung surfactants with those of alveolar and conductive airway surfactants from porcine and human lungs. The aim here was to correlate compositions with functions of the various surfactants, and hence to determine which components are essential for each different function.

Section snippets

Materials

Hydrogen peroxide (30%, analytical grade) was from Boehringer Ingelheim (Ingelheim, FRG) and perchloric acid (70%, analytical grade) was from Merck (Darmstadt, FRG). Organic solvents were of HPLC grade and from Baker (Deventer, NL). Dimyristoylphosphatidylcholine (PC14:0/14:0) was obtained from Sigma-Aldrich (Deisenhofen, FRG). All other chemicals were of analytical grade and obtained from various commercial sources.

Surfactant preparation

Alveolar surfactant was isolated by differential ultra-centrifugation of

Statistics

One-way analyses of variance were calculated using GraphPad Instat Version 1.11a (GraphPad Software, San Diego, CA, USA). Group differences were tested by two-sided t-test. A P-value of less than 0.05 was considered significant. Bonferroni correction for multiple group comparison was performed consistently.

Comparison of phosphatidylcholine compositions of pulmonary and gastric surfactants from the rat and pig

Phospholipid-rich fractions were obtained by lavage both of lung and stomach of the rat and the pig. However, the PC compositions of pulmonary and gastric surfactants were very different (Fig. 1). The major molecular species of PC in the gastric-derived material were palmitoyloleoyl-PC (PC16:0/18:1) and palmitoyllinoleoyl-PC (PC16:0/18:2) for both rat and pig (Fig. 1a). In contrast, these two species were minor components of lung surfactant from rat and pig (Fig. 1b), which were dominated by

Surfactant in the gastrointestinal tract compared to the lung

The comparison of PC molecular species of gastric and pulmonary surfactants (Fig. 1) shows clearly that these preparations have very different compositions. The observation that similar differences between gastric and pulmonary surfactant PC compositions were apparent for both rat and pig also demonstrated that these PC compositions were probably tissue and not animal-specific. Our previous report of the absence of phosphatidylglycerol (PG) in gastric surfactant (Bernhard et al., 1995) provides

Acknowledgements

We gratefully acknowledge the excellent technical assistence of Mrs Christa Acevedo and Ms Ivonne Strenger. This work was in part supported by the Deutsche Forschungsgemeinschaft, grant: Ha1959/2.

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