Cholesterol modulates the exposure and orientation of pulmonary surfactant protein SP-C in model surfactant membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 9, 2009, Pages 1907-1915

  Gomez Gil L ^a   Perez Gil J ^b   Goormaghtigh, E ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

ATR FTIR; Cholesterol; Lipid protein interaction; Membrane protein dynamics; Structure; Transmembrane protein

Indexed keywords

CHOLESTEROL; DEUTERIUM; DIPALMITOYLPHOSPHATIDYLCHOLINE; DIPALMITOYLPHOSPHATIDYLGLYCEROL; GLYCEROPHOSPHOLIPID; HYDROGEN; LUNG SURFACTANT; OLEOYLPALMITOYLLECITHIN; PALMITOYLOLEOYLPHOSPHATIDYLGLYCEROL; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ANIMAL TISSUE; ARTICLE; BILAYER MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DYNAMICS; EXPOSURE; FILM; INFRARED SPECTROSCOPY; KINETICS; MODEL; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SWINE;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; AMIDES; DEUTERIUM EXCHANGE MEASUREMENT; LIPID BILAYERS; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PRINCIPAL COMPONENT ANALYSIS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; PULMONARY SURFACTANTS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 68749105867     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.05.011     Document Type: Article

References (61)

1. Seeger W., Gunther A., Walmrath H.D., Grimminger F., and Lasch H.G. Alveolar surfactant and adult respiratory distress syndrome. Pathogenetic role and therapeutic prospects. Clin. Investig. 71 (1993) 177-190
2. Hallman M., Glumoff V., and Ramet M. Surfactant in respiratory distress syndrome and lung injury. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 129 (2001) 287-294
3. Veldhuizen R., Nag K., Orgeig S., and Possmayer F. The role of lipids in pulmonary surfactant. Biochim. Biophys. Acta. 1408 (1998) 90-108
4. Perez-Gil J. Protein modulation of membrane structure. Preface. Biochim. Biophys. Acta 1778 (2008) 1527
5. Johansson J. Structure and properties of surfactant protein C. Biochim. Biophys. Acta 1408 (1998) 161-172
6. Serrano A.G., and Perez-Gil J. Protein-lipid interactions and surface activity in the pulmonary surfactant system. Chem. Phys. Lipids 141 (2006) 105-118
7. Glasser S.W., Burhans M.S., Korfhagen T.R., Na C.L., Sly P.D., Ross G.F., Ikegami M., and Whitsett J.A. Altered stability of pulmonary surfactant in SP-C-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6366-6371
8. Glasser S.W., Detmer E.A., Ikegami M., Na C.L., Stahlman M.T., and Whitsett J.A. Pneumonitis and emphysema in sp-C gene targeted mice. J. Biol. Chem. 278 (2003) 14291-14298
9. von Nahmen A., Schenk M., Sieber M., and Amrein M. The structure of a model pulmonary surfactant as revealed by scanning force microscopy. Biophys. J. 72 (1997) 463-469
10. Wang L., Cai P., Galla H.J., He H., Flach C.R., and Mendelsohn R. Monolayer-multilayer transitions in a lung surfactant model: IR reflection-absorption spectroscopy and atomic force microscopy. Eur. Biophys. J. 34 (2005) 243-254
11. Malcharek S., Hinz A., Hilterhaus L., and Galla H.J. Multilayer structures in lipid monolayer films containing surfactant protein C: effects of cholesterol and POPE. Biophys. J. 88 (2005) 2638-2649
12. Taneva S., and Keough K.M. Cholesterol modifies the properties of surface films of dipalmitoylphosphatidylcholine plus pulmonary surfactant-associated protein B or C spread or adsorbed at the air-water interface. Biochemistry 36 (1997) 912-922
13. Perez-Gil J., Cruz A., and Casals C. Solubility of hydrophobic surfactant proteins in organic solvent/water mixtures. Structural studies on SP-B and SP-C in aqueous organic solvents and lipids. Biochim. Biophys. Acta 1168 (1993) 261-270
14. Plasencia I., Cruz A., Lopez-Lacomba J.L., Casals C., and Perez-Gil J. Selective labeling of pulmonary surfactant protein SP-C in organic solution. Anal. Biochem. 296 (2001) 49-56
15. Fringeli U.P., and Gunthard H.H. Infrared membrane spectroscopy. Mol. Biol. Biochem. Biophys. 31 (1981) 270-332
16. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Secondary structure and dosage of soluble and membrane proteins by attenuated total reflection Fourier-transform infrared spectroscopy on hydrated films. Eur. J. Biochem. 193 (1990) 409-420
17. Vandenbussche G., Clercx A., Clercx M., Curstedt T., Johansson J., Jornvall H., and Ruysschaert J.M. Secondary structure and orientation of the surfactant protein SP-B in a lipid environment. A Fourier transform infrared spectroscopy study. Biochemistry 31 (1992) 9169-9176
18. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. II. Experimental aspects, side chain structure, and H/D exchange. Subcell. Biochem. 23 (1994) 363-403
19. Goormaghtigh E., and Ruysschaert J.M. Subtraction of atmospheric water contribution in Fourier transform infrared spectroscopy of biological membranes and proteins. Spectrochim. Acta 50A (1994) 2137-2144
20. Raussens V., Narayanaswami V., Goormaghtigh E., Ryan R.O., and Ruysschaert J.M. Hydrogen/deuterium exchange kinetics of apolipophorin-III in lipid-free and phospholipid-bound states. An analysis by Fourier transform infrared spectroscopy. J. Biol. Chem. 271 (1996) 23089-23095
21. Isaksson T., Yang H., Kemeny G.J., Jackson R.S., Wang Q., Alam M.K., and Griffiths P.R. Accurate wavelength measurements of a putative standard for near-infrared diffuse reflection spectrometry. Appl. Spectrosc. 57 (2003) 176-185
22. Raussens V., Ruysschaert J.M., and Goormaghtigh E. Analysis of 1H/2H exchange kinetics using model infrared spectra. Appl. Spectrosc. 58 (2004) 68-82
23. Harrick N.J. Internal Reflection Spectroscopy (1967), Interscience Publishers, New York
24. Goormaghtigh E., Raussens V., and Ruysschaert J.M. Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim. Biophys. Acta 1422 (1999) 105-185
25. Gremlich H.U., Fringeli U.P., and Schwyzer R. Conformational changes of adrenocorticotropin peptides upon interaction with lipid membranes revealed by infrared attenuated total reflection spectroscopy. Biochemistry 22 (1983) 4257-4264
26. Marsh D., Muller M., and Schmitt F.J. Orientation of the infrared transition moments for an alpha-helix. Biophys. J. 78 (2000) 2499-2510
27. Marsh D., and Pali T. Infrared dichroism from the X-ray structure of bacteriorhodopsin. Biophys. J. 80 (2001) 305-312
28. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. III. Secondary structures. Subcell. Biochem. 23 (1994) 405-450
29. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. I. Assignments and model compounds. Subcell. Biochem. 23 (1994) 329-362
30. Mendelsohn R., Davies M.A., Brauner J.W., Schuster H.F., and Dluhy R.A. Quantitative determination of conformational disorder in the acyl chains of phospholipid bilayers by infrared spectroscopy. Biochemistry 28 (1989) 8934-8939
31. Moore D.J., Wyrwa M., Reboulleau C.P., and Mendelsohn R. Quantitative IR studies of acyl chain conformational order in fatty acid homogeneous membranes of live cells of Acholeplasma laidlawii B. Biochemistry 32 (1993) 6281-6287
32. Kim P.S. Amide proton exchange as a probe of protein folding pathways. Methods Enzymol. 131 (1986) 136-156
33. In: Lumry R. (Ed). Protein-Solvent Interactions (1995), Dekker Inc., New York
34. Grimard V., Vigano C., Margolles A., Wattiez R., van Veen H.W., Konings W.N., Ruysschaert J.M., and Goormaghtigh E. Structure and dynamics of the membrane-embedded domain of LmrA investigated by coupling polarized ATR-FTIR spectroscopy and (1)H/(2)H exchange. Biochemistry 40 (2001) 11876-11886
35. Scheirlinckx F., Raussens V., Ruysschaert J.M., and Goormaghtigh E. Conformational changes in gastric H+/K+-ATPase monitored by difference Fourier-transform infrared spectroscopy and hydrogen/deuterium exchange. Biochem. J. 382 (2004) 121-129
36. Hosia W., Johansson J., and Griffiths W.J. Hydrogen/deuterium exchange and aggregation of a polyvaline and a polyleucine alpha-helix investigated by matrix-assisted laser desorption ionization mass spectrometry. Mol. Cell. Proteomics 1 (2002) 592-597
37. Johansson J., Weaver T.E., and Tjernberg L.O. Proteolytic generation and aggregation of peptides from transmembrane regions: lung surfactant protein C and amyloid beta-peptide. Cell. Mol. Life Sci. 61 (2004) 326-335
38. Fink A.L., Oberg K.A., and Seshadri S. Discrete intermediates versus molten globule models for protein folding: characterization of partially folded intermediates of apomyoglobin. Fold. Des. 3 (1998) 19-25
39. Lefevre T., and Subirade M. Formation of intermolecular beta-sheet structures: a phenomenon relevant to protein film structure at oil-water interfaces of emulsions. J. Colloid Interface Sci. 263 (2003) 59-67
40. Navarra G., Giacomazza D., Leone M., Librizzi F., Militello V., and San Biagio P.L. Thermal aggregation and ion-induced cold-gelation of bovine serum albumin. Eur. Biophys. J. 38 (2009) 437-446
41. Acosta E.J., Gitiafroz R., Zuo Y.Y., Policova Z., Cox P.N., Hair M.L., and Neumann A.W. Effect of humidity on lung surfactant films subjected to dynamic compression/expansion cycles. Respir. Physiol. Neurobiol. 155 (2007) 255-267
42. Arrais D., and Martins J. Bilayer polarity and its thermal dependency in the l(o) and l(d) phases of binary phosphatidylcholine/cholesterol mixtures. Biochim. Biophys. Acta. 1768 (2007) 2914-2922
43. Theunissen J.J., Jackson R.L., Kempen H.J., and Demel R.A. Membrane properties of oxysterols. Interfacial orientation, influence on membrane permeability and redistribution between membranes. Biochim. Biophys. Acta 860 (1986) 66-74
44. I. Garcia-Verdugo, E. Garcia de Paco, Q. Espinannous, A. Gonzalez-Horta, M. Synguelakis, L. Rivas, J. Kanellopoulos, R. Chaby, J. and Perez-Gil, Synthetic peptides representing the N-terminal segment of surfactant protein C modulate LPS-stimulated TNF-alpha production by macrophages, Innate immunity, 15 (2009) 53-62.
45. Allende D., and McIntosh T.J. Lipopolysaccharides in bacterial membranes act like cholesterol in eukaryotic plasma membranes in providing protection against melittin-induced bilayer lysis. Biochemistry 42 (2003) 1101-1108
46. Baumgart F., Loura L., Prieto M., and Perez-Gil J. Pulmonary surfactant protein C reduces the size of liquid ordered domains in a ternary membrane model system. Biophys. J. 96 (2009) 608a-609a
47. Bi X., Flach C.R., Perez-Gil J., Plasencia I., Andreu D., Oliveira E., and Mendelsohn R. Secondary structure and lipid interactions of the N-terminal segment of pulmonary surfactant SP-C in Langmuir films: IR reflection-absorption spectroscopy and surface pressure studies. Biochemistry 41 (2002) 8385-8395
48. Gericke A., Flach C.R., and Mendelsohn R. Structure and orientation of lung surfactant SP-C and l-alpha-dipalmitoylphosphatidylcholine in aqueous monolayers. Biophys. J. 73 (1997) 492-499
49. Bernardino de la Serna J., Perez-Gil J., Simonsen A.C., and Bagatolli L.A. Cholesterol rules: direct observation of the coexistence of two fluid phases in native pulmonary surfactant membranes at physiological temperatures. J. Biol. Chem. 279 (2004) 40715-40722
50. Cruz A., Marsh D., and Perez-Gil J. Rotational dynamics of spin-labelled surfactant-associated proteins SP-B and SP-C in dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylglycerol bilayers. Biochim. Biophys. Acta 1415 (1998) 125-134
51. Perez-Gil J., Casals C., and Marsh D. Interactions of hydrophobic lung surfactant proteins SP-B and SP-C with dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylglycerol bilayers studied by electron spin resonance spectroscopy. Biochemistry 34 (1995) 3964-3971
52. Plasencia I., Cruz A., Casals C., and Perez-Gil J. Superficial disposition of the N-terminal region of the surfactant protein SP-C and the absence of specific SP-B-SP-C interactions in phospholipid bilayers. Biochem. J. 359 (2001) 651-659
53. Plasencia I., Keough K.M., and Perez-Gil J. Interaction of the N-terminal segment of pulmonary surfactant protein SP-C with interfacial phospholipid films. Biochim. Biophys. Acta 1713 (2005) 118-128
54. Johansson J., Curstedt T., and Robertson B. The proteins of the surfactant system. Eur. Respir. J. 7 (1994) 372-391
55. Horowitz A.D., Baatz J.E., and Whitsett J.A. Lipid effects on aggregation of pulmonary surfactant protein SP-C studied by fluorescence energy transfer. Biochemistry 32 (1993) 9513-9523
56. Wustneck R., Perez-Gil J., Wustneck N., Cruz A., Fainerman V.B., and Pison U. Interfacial properties of pulmonary surfactant layers. Adv. Colloid. Interface Sci. 117 (2005) 33-58
57. Rodriguez-Casado A., Molina M., and Carmona P. Spectroscopic study of conformational changes accompanying self-assembly of HCV core protein. Proteins 66 (2007) 110-117
58. Iloro I., Narvaez D., Guillen N., Camacho C.M., Guillen L., Cora E., and Pastrana-Rios B. The kinetics of the hydrogen/deuterium exchange of epidermal growth factor receptor ligands. Biophys. J. 94 (2008) 4041-4055
59. Suzuki Y. Effect of protein, cholesterol, and phosphatidylglycerol on the surface activity of the lipid-protein complex reconstituted from pig pulmonary surfactant. J. Lipid Res. 23 (1982) 62-69
60. Gunasekara L., Schurch S., Schoel W.M., Nag K., Leonenko Z., Haufs M., and Amrein M. Pulmonary surfactant function is abolished by an elevated proportion of cholesterol. Biochim. Biophys. Acta 1737 (2005) 27-35
61. Schram V., and Hall S.B. Thermodynamic effects of the hydrophobic surfactant proteins on the early adsorption of pulmonary surfactant. Biophys. J. 81 (2001) 1536-1546