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J. Biol. Chem., Vol. 279, Issue 39, 40715-40722, September 24, 2004

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Cholesterol Rules

DIRECT OBSERVATION OF THE COEXISTENCE OF TWO FLUID PHASES IN NATIVE PULMONARY SURFACTANT MEMBRANES AT PHYSIOLOGICAL TEMPERATURES^*

Jorge Bernardino de la Serna, Jesus Perez-Gil, Adam C. Simonsen, and Luis A. Bagatolli¶||

From the Departmento de Bioquímica, Facultad de Biología, Universidad Complutense, 28040 Madrid, Spain and the MEMPHYS-Center for Biomembrane Physics, the Department of Physics and the ^¶Department of Biochemistry and Molecular Biology, University of Southern Denmark, 5230 Odense, Denmark

Pulmonary surfactant, the lipid-protein material that stabilizes the respiratory surface of the lungs, contains approximately equimolar amounts of saturated and unsaturated phospholipid species and significant proportions of cholesterol. Such lipid composition suggests that the membranes taking part in the surfactant structures could be organized heterogeneously in the form of inplane domains, originating from particular distributions of specific proteins and lipids. Here we report novel results concerning the lateral organization of bilayer membranes made of native pulmonary surfactant where the coexistence of two distinct micrometer sized fluid phases (fluid ordered and fluid disordered-like phases) is observed at physiological temperatures by using fluorescence microscopy and atomic force microscopy. Additional experiments using fluorescent-labeled proteins SP-B and SP-C show that at physiological temperatures these hydrophobic proteins are located exclusively in the fluid disordered-like phase. Most interestingly, the microscopic coexistence of fluid phases is maintained up to 37.5 °C, where most fluid ordered phases melt. This observation suggests that the particular composition of this material is naturally designed to be at the "edge" of a lateral structure transition under physiological conditions, likely providing particular structural and dynamic properties for its mechanical function. The observed lateral structure in native pulmonary surfactant membranes is dramatically affected by the extraction of cholesterol, an effect not observed upon extraction of the surfactant proteins. Furthermore, the spreading properties of the native surfactant material at the air-liquid interface were also greatly affected by cholesterol extraction, suggesting a connection between the observed lateral structure and a physiologically relevant function of the material. We suggest that the particular lipid composition of surfactant could be finely tuned to provide, under physiological conditions, a structural scaffold for surfactant proteins to act at appropriate local densities and lipid composition.

Received for publication, April 27, 2004 , and in revised form, June 23, 2004.

^* This work was supported by Dirección General de Educación Superior e Investigaciones Científicas Grant BIO2003-09056 (to J. B. S. and J. P.-G.), Comunidad Autónoma de Madrid Grant 08.2/0054, and by Danish Natural Science Research Council Grant 21-03-0569 (to L. A. B.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed: MEMPHYS-Center for Biomembrane Physics, Dept. of Biochemistry and Molecular Biology, University of Southern Denmark, 5230 Odense M, Denmark. Tel.: 45-65-50-34-76; Fax: 45-66-15-87-60; E-mail: bagatolli{at}memphys.sdu.dk.

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