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Research article

A combined action of pulmonary surfactant proteins SP-B and SP-C modulates permeability and dynamics of phospholipid membranes

Elisa Parra, Lara H. Moleiro, Ivan López-Montero, Antonio Cruz, Francisco Monroy, Jesús Pérez-Gil
Biochemical Journal Sep 15, 2011, 438 (3) 555-564; DOI: 10.1042/BJ20110681
Elisa Parra
Dept. Bioquímica, Fac. Biología, Universidad Complutense, Ciudad Universitaria s/n, 28040 Madrid, Spain
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Lara H. Moleiro
Dept. Química Fisica, Fac. CC. Quimicas, Universidad Complutense, Ciudad Universitaria s/n, 28040 Madrid, Spain
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Ivan López-Montero
Dept. Química Fisica, Fac. CC. Quimicas, Universidad Complutense, Ciudad Universitaria s/n, 28040 Madrid, Spain
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Antonio Cruz
Dept. Bioquímica, Fac. Biología, Universidad Complutense, Ciudad Universitaria s/n, 28040 Madrid, Spain
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Francisco Monroy
Dept. Química Fisica, Fac. CC. Quimicas, Universidad Complutense, Ciudad Universitaria s/n, 28040 Madrid, Spain
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Jesús Pérez-Gil
Dept. Bioquímica, Fac. Biología, Universidad Complutense, Ciudad Universitaria s/n, 28040 Madrid, Spain
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  • For correspondence: jpg@bbm1.ucm.es
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Abstract

Proteins SP-B and SP-C are essential to promote formation of surface-active films at the respiratory interface, but their mechanism of action is still under investigation. In the present study we have analysed the effect of the proteins on the accessibility of native, quasi-native and model surfactant membranes to incorporation of the fluorescent probes Nile Red (permeable) and FM 1-43 (impermeable) into membranes. We have also analysed the effect of single or combined proteins on membrane permeation using the soluble fluorescent dye calcein. The fluorescence of FM 1-43 was always higher in membranes containing SP-B and/or SP-C than in protein-depleted membranes, in contrast with Nile Red which was very similar in all of the materials tested. SP-B and SP-C promoted probe partition with markedly different kinetics. On the other hand, physiological proportions of SP-B and SP-C caused giant oligolamellar vesicles to incorporate FM 1-43 from the external medium into apparently most of the membranes instantaneously. In contrast, oligolamellar pure lipid vesicles appeared to be mainly labelled in the outermost membrane layer. Pure lipidic vesicles were impermeable to calcein, whereas it permeated through membranes containing SP-B and/or SP-C. Vesicles containing only SP-B were stable, but prone to vesicle–vesicle interactions, whereas those containing only SP-C were extremely dynamic, undergoing frequent fluctuations and ruptures. Differential structural effects of proteins on vesicles were confirmed by electron microscopy. These results suggest that SP-B and SP-C have different contributions to inter- and intra-membrane lipid dynamics, and that their combined action could provide unique effects to modulate structure and dynamics of pulmonary surfactant membranes and films.

  • lipid–protein interaction
  • lung surfactant
  • membrane permeability
  • membrane perturbation
  • membrane pore
  • membrane protein

Abbreviations: GV, giant vesicle; LB, lamellar body; LUV, large unilamellar vesicle; MLV, multilamellar membrane suspension; POPC, 1-palmitoyl-2-oleoyl phosphatidylcholine; SUV, small unilamellar vesicle

  • © The Authors Journal compilation © 2011 Biochemical Society
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September 2011

Volume: 438 Issue: 3

Biochemical Journal: 438 (3)
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A combined action of pulmonary surfactant proteins SP-B and SP-C modulates permeability and dynamics of phospholipid membranes
Elisa Parra, Lara H. Moleiro, Ivan López-Montero, Antonio Cruz, Francisco Monroy, Jesús Pérez-Gil
Biochemical Journal Sep 2011, 438 (3) 555-564; DOI: 10.1042/BJ20110681
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A combined action of pulmonary surfactant proteins SP-B and SP-C modulates permeability and dynamics of phospholipid membranes
Elisa Parra, Lara H. Moleiro, Ivan López-Montero, Antonio Cruz, Francisco Monroy, Jesús Pérez-Gil
Biochemical Journal Sep 2011, 438 (3) 555-564; DOI: 10.1042/BJ20110681

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Keywords

lipid–protein interaction
lung surfactant
membrane permeability
membrane perturbation
membrane pore
membrane protein

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