Interfacial behavior of recombinant forms of human pulmonary surfactant protein SP-C

Langmuir

Volumn 28, Issue 20, 2012, Pages 7811-7825

  Lukovic, Dunja ^a   Cruz, Antonio ^b   Gonzalez Horta, Azucena ^b,d   Almlen, Andrea ^c   Curstedt, Tore ^c   Mingarro, Ismael ^a   Pérez Gil, Jesus ^b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

AIR LIQUID INTERFACES; ANIONIC PHOSPHOLIPIDS; COMPRESSION ISOTHERM; COMPRESSION-EXPANSION; DIPALMITOYLPHOSPHATIDYLCHOLINE BILAYERS; EPIFLUORESCENCE MICROSCOPY; HIGH PRESSURE; INTERFACIAL ADSORPTION; INTERFACIAL BEHAVIORS; LIPID MIXTURES; LIPID MOLECULES; N-TERMINALS; NATIVE PROTEINS; PULMONARY SURFACTANTS; QUASI-STATIC; STRUCTURAL TRANSITIONS; SURFACE PRESSURES; SURFACTANT PROTEINS;

ADSORPTION; AMINO ACIDS; DYES; LIPID BILAYERS; PHOSPHOLIPIDS; SURFACE ACTIVE AGENTS;

RECOMBINANT PROTEINS;

PEPTIDE FRAGMENT; PHOSPHOLIPID; RECOMBINANT PROTEIN; SURFACTANT PROTEIN C;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; SURFACE PROPERTY;

AMINO ACID SEQUENCE; ANIMALS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHOLIPIDS; PROTEIN CONFORMATION; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; RECOMBINANT PROTEINS; SURFACE PROPERTIES;

EID: 84861386006     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la301134v     Document Type: Article

References (61)

1. Daniels, C. B.; Orgeig, S. Pulmonary surfactant: the key to the evolution of air breathing News Physiol. Sci. 2003, 18, 151-7
2. Perez-Gil, J.; Weaver, T. E. Pulmonary surfactant pathophysiology: current models and open questions Physiology (Bethesda) 2010, 25 (3) 132-41
3. Matthay, M. A.; Zemans, R. L. The acute respiratory distress syndrome: pathogenesis and treatment Annu. Rev. Pathol. 2010, 6, 147-63
4. Whitsett, J. A.; Wert, S. E.; Weaver, T. E. Alveolar surfactant homeostasis and the pathogenesis of pulmonary disease Annu. Rev. Med. 2010, 61, 105-19
5. Veldhuizen, R.; Nag, K.; Orgeig, S.; Possmayer, F. The role of lipids in pulmonary surfactant Biochim. Biophys. Acta 1998, 1408 (2-3) 90-108
6. Perez-Gil, J. Structure of pulmonary surfactant membranes and films: the role of proteins and lipid-protein interactions Biochim. Biophys. Acta 2008, 1778 (7-8) 1676-95
7. Serrano, A. G.; Perez-Gil, J. Protein-lipid interactions and surface activity in the pulmonary surfactant system Chem. Phys. Lipids 2006, 141 (1-2) 105-18
8. Clark, J. C.; Wert, S. E.; Bachurski, C. J.; Stahlman, M. T.; Stripp, B. R.; Weaver, T. E.; Whitsett, J. A. Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (17) 7794-8
9. Melton, K. R.; Nesslein, L. L.; Ikegami, M.; Tichelaar, J. W.; Clark, J. C.; Whitsett, J. A.; Weaver, T. E. SP-B deficiency causes respiratory failure in adult mice Am. J. Physiol.: Lung Cell. Mol. Physiol. 2003, 285 (3) L543-9
10. Glasser, S. W.; Burhans, M. S.; Korfhagen, T. R.; Na, C. L.; Sly, P. D.; Ross, G. F.; Ikegami, M.; Whitsett, J. A. Altered stability of pulmonary surfactant in SP-C-deficient mice Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (11) 6366-71
11. Glasser, S. W.; Detmer, E. A.; Ikegami, M.; Na, C. L.; Stahlman, M. T.; Whitsett, J. A. Pneumonitis and emphysema in sp-C gene targeted mice J. Biol. Chem. 2003, 278 (16) 14291-8
12. Krol, S.; Ross, M.; Sieber, M.; Kunneke, S.; Galla, H. J.; Janshoff, A. Formation of three-dimensional protein-lipid aggregates in monolayer films induced by surfactant protein B Biophys. J. 2000, 79 (2) 904-18
13. Possmayer, F.; Nag, K.; Rodriguez, K.; Qanbar, R.; Schurch, S. Surface activity in vitro: role of surfactant proteins Comp. Biochem. Physiol., A: Mol. Integr. Physiol. 2001, 129 (1) 209-20
14. Gomez-Gil, L.; Schurch, D.; Goormaghtigh, E.; Perez-Gil, J. Pulmonary surfactant protein SP-C counteracts the deleterious effects of cholesterol on the activity of surfactant films under physiologically relevant compression-expansion dynamics Biophys. J. 2009, 97 (10) 2736-45
15. Johansson, J.; Szyperski, T.; Curstedt, T.; Wuthrich, K. The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich α-helix Biochemistry 1994, 33 (19) 6015-23
16. Vandenbussche, G.; Clercx, A.; Curstedt, T.; Johansson, J.; Jornvall, H.; Ruysschaert, J. M. Structure and orientation of the surfactant-associated protein C in a lipid bilayer Eur. J. Biochem. 1992, 203 (1-2) 201-9
17. Brown, N. J.; Johansson, J.; Barron, A. E. Biomimicry of surfactant protein C Acc. Chem. Res. 2008, 41 (10) 1409-17
18. Hawgood, S.; Ogawa, A.; Yukitake, K.; Schlueter, M.; Brown, C.; White, T.; Buckley, D.; Lesikar, D.; Benson, B. Lung function in premature rabbits treated with recombinant human surfactant protein-C Am. J. Respir. Crit. Care Med. 1996, 154 (2, Part 1) 484-90
19. Mingarro, I.; Lukovic, D.; Vilar, M.; Perez-Gil, J. Synthetic pulmonary surfactant preparations: new developments and future trends Curr. Med. Chem. 2008, 15 (4) 393-403
20. Hilgendorff, A.; Doerner, M.; Rawer, D.; Leick, J.; Trotter, A.; Ebsen, M.; Ruppert, C.; Gunther, A.; Gortner, L.; Reiss, I. Effects of a recombinant surfactant protein-C-based surfactant on lung function and the pulmonary surfactant system in a model of meconium aspiration syndrome Crit. Care Med. 2006, 34 (1) 203-10
21. Foot, N. J.; Orgeig, S.; Donnellan, S.; Bertozzi, T.; Daniels, C. B. Positive selection in the N-terminal extramembrane domain of lung surfactant protein C (SP-C) in marine mammals J. Mol. Evol. 2007, 65 (1) 12-22
22. Lukovic, D.; Plasencia, I.; Taberner, F. J.; Salgado, J.; Calvete, J. J.; Perez-Gil, J.; Mingarro, I. Production and characterisation of recombinant forms of human pulmonary surfactant protein C (SP-C): structure and surface activity Biochim. Biophys. Acta 2006, 1758 (4) 509-18
23. Baumgart, F.; Ospina, O. L.; Mingarro, I.; Rodriguez-Crespo, I.; Perez-Gil, J. Palmitoylation of pulmonary surfactant protein SP-C is critical for its functional cooperation with SP-B to sustain compression/expansion dynamics in cholesterol-containing surfactant films Biophys. J. 2010, 99 (10) 3234-43
24. Bligh, E. G.; Dyer, W. J. A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 1959, 37 (8) 911-7
25. Taeusch, H. W.; Bernardino de la Serna, J.; Perez-Gil, J.; Alonso, C.; Zasadzinski, J. A. Inactivation of pulmonary surfactant due to serum-inhibited adsorption and reversal by hydrophilic polymers: experimental Biophys. J. 2005, 89 (3) 1769-79
26. Perez-Gil, J.; Cruz, A.; 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 1993, 1168 (3) 261-70
27. Rouser, G.; Siakotos, A. N.; Fleischer, S. Quantitative analysis of phospholipids by thin-layer chromatography and phosphorus analysis of spots Lipids 1966, 1 (1) 85-6
28. Serrano, A. G.; Cruz, A.; Rodriguez-Capote, K.; Possmayer, F.; Perez-Gil, J. Intrinsic structural and functional determinants within the amino acid sequence of mature pulmonary surfactant protein SP-B Biochemistry 2005, 44 (1) 417-30
29. Perez-Gil, J.; Nag, K.; Taneva, S.; Keough, K. M. Pulmonary surfactant protein SP-C causes packing rearrangements of dipalmitoylphosphatidylcholine in spread monolayers Biophys. J. 1992, 63 (1) 197-204
30. Cruz, A.; Perez-Gil, J. Langmuir films to determine lateral surface pressure on lipid segregation Methods Mol. Biol. 2007, 400, 439-57
31. Wang, L.; Cruz, A.; Flach, C. R.; Perez-Gil, J.; Mendelsohn, R. Langmuir-Blodgett films formed by continuously varying surface pressure. Characterization by IR spectroscopy and epifluorescence microscopy Langmuir 2007, 23 (9) 4950-8
32. Schoel, W. M.; Schurch, S.; Goerke, J. The captive bubble method for the evaluation of pulmonary surfactant: surface tension, area, and volume calculations Biochim. Biophys. Acta 1994, 1200 (3) 281-90
33. Schurch, D.; Ospina, O. L.; Cruz, A.; Perez-Gil, J. Combined and independent action of proteins SP-B and SP-C in the surface behavior and mechanical stability of pulmonary surfactant films Biophys. J. 2010, 99 (10) 3290-9
34. Oosterlaken-Dijksterhuis, M. A.; Haagsman, H. P.; van Golde, L. M.; Demel, R. A. Characterization of lipid insertion into monomolecular layers mediated by lung surfactant proteins SP-B and SP-C Biochemistry 1991, 30 (45) 10965-71
35. Perez-Gil, J.; Tucker, J.; Simatos, G.; Keough, K. M. Interfacial adsorption of simple lipid mixtures combined with hydrophobic surfactant protein from pig lung Biochem. Cell Biol. 1992, 70 (5) 332-8
36. Taneva, S.; Keough, K. M. Pulmonary surfactant proteins SP-B and SP-C in spread monolayers at the air-water interface: II. Monolayers of pulmonary surfactant protein SP-C and phospholipids Biophys. J. 1994, 66 (4) 1149-57
37. Wustneck, N.; Wustneck, R.; Perez-Gil, J.; Pison, U. Effects of oligomerization and secondary structure on the surface behavior of pulmonary surfactant proteins SP-B and SP-C Biophys. J. 2003, 84 (3) 1940-9
38. Wustneck, R.; Perez-Gil, J.; Wustneck, N.; Cruz, A.; Fainerman, V. B.; Pison, U. Interfacial properties of pulmonary surfactant layers Adv. Colloid Interface Sci. 2005, 117 (1-3) 33-58
39. Creuwels, L. A.; Demel, R. A.; van Golde, L. M.; Benson, B. J.; Haagsman, H. P. Effect of acylation on structure and function of surfactant protein C at the air-liquid interface J. Biol. Chem. 1993, 268 (35) 26752-8
40. Cruz, A.; Worthman, L. A.; Serrano, A. G.; Casals, C.; Keough, K. M.; Perez-Gil, J. Microstructure and dynamic surface properties of surfactant protein SP-B/dipalmitoylphosphatidylcholine interfacial films spread from lipid-protein bilayers Eur. Biophys. J. 2000, 29 (3) 204-13
41. Perez-Gil, J.; Casals, C.; 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 1995, 34 (12) 3964-71
42. Kruger, P.; Baatz, J. E.; Dluhy, R. A.; Losche, M. Effect of hydrophobic surfactant protein SP-C on binary phospholipid monolayers. Molecular machinery at the air/water interface Biophys. Chem. 2002, 99 (3) 209-28
43. Kruger, P.; Schalke, M.; Wang, Z.; Notter, R. H.; Dluhy, R. A.; Losche, M. Effect of hydrophobic surfactant peptides SP-B and SP-C on binary phospholipid monolayers. I. Fluorescence and dark-field microscopy Biophys. J. 1999, 77 (2) 903-14
44. Nag, K.; Perez-Gil, J.; Cruz, A.; Keough, K. M. Fluorescently labeled pulmonary surfactant protein C in spread phospholipid monolayers Biophys. J. 1996, 71 (1) 246-56
45. Plasencia, I.; Keough, K. M.; Perez-Gil, J. Interaction of the N-terminal segment of pulmonary surfactant protein SP-C with interfacial phospholipid films Biochim. Biophys. Acta 2005, 1713 (2) 118-28
46. Gustafsson, M.; Curstedt, T.; Jornvall, H.; Johansson, J. Reverse-phase HPLC of the hydrophobic pulmonary surfactant proteins: detection of a surfactant protein C isoform containing Nε-palmitoyl-lysine Biochem. J. 1997, 326 (Part 3) 799-806
47. Gustafsson, M.; Thyberg, J.; Naslund, J.; Eliasson, E.; Johansson, J. Amyloid fibril formation by pulmonary surfactant protein C FEBS Lett. 1999, 464 (3) 138-42
48. Rodriguez-Capote, K.; Manzanares, D.; Haines, T.; Possmayer, F. Reactive oxygen species inactivation of surfactant involves structural and functional alterations to surfactant proteins SP-B and SP-C Biophys. J. 2006, 90 (8) 2808-21
49. Taneva, S. G.; Stewart, J.; Taylor, L.; Keough, K. M. Method of purification affects some interfacial properties of pulmonary surfactant proteins B and C and their mixtures with dipalmitoylphosphatidylcholine Biochim. Biophys. Acta 1998, 1370 (1) 138-50
50. Gomez-Gil, L.; Perez-Gil, J.; Goormaghtigh, E. Cholesterol modulates the exposure and orientation of pulmonary surfactant protein SP-C in model surfactant membranes Biochim. Biophys. Acta 2009, 1788 (9) 1907-15
51. Augusto, L. A.; Li, J.; Synguelakis, M.; Johansson, J.; Chaby, R. Structural basis for interactions between lung surfactant protein C and bacterial lipopolysaccharide J. Biol. Chem. 2002, 277 (26) 23484-92
52. Kairys, V.; Gilson, M. K.; Luy, B. Structural model for an AxxxG-mediated dimer of surfactant-associated protein C Eur. J. Biochem. 2004, 271 (11) 2086-92
53. Luy, B.; Diener, A.; Hummel, R. P.; Sturm, E.; Ulrich, W. R.; Griesinger, C. Structure and potential C-terminal dimerization of a recombinant mutant of surfactant-associated protein C in chloroform/methanol Eur. J. Biochem. 2004, 271 (11) 2076-85
54. Serrano, A. G.; Ryan, M.; Weaver, T. E.; Perez-Gil, J. Critical structure-function determinants within the N-terminal region of pulmonary surfactant protein SP-B Biophys. J. 2006, 90 (1) 238-49
55. Gericke, A.; Flach, C. R.; Mendelsohn, R. Structure and orientation of lung surfactant SP-C and L-α-dipalmitoylphosphatidylcholine in aqueous monolayers Biophys. J. 1997, 73 (1) 492-9
56. Bi, X.; Flach, C. R.; Perez-Gil, J.; Plasencia, I.; Andreu, D.; Oliveira, E.; 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 2002, 41 (26) 8385-95
57. Wimley, W. C.; White, S. H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 1996, 3 (10) 842-8
58. Gonzalez-Horta, A.; Andreu, D.; Morrow, M. R.; Perez-Gil, J. Effects of palmitoylation on dynamics and phospholipid-bilayer-perturbing properties of the N-terminal segment of pulmonary surfactant protein SP-C as shown by 2H-NMR Biophys. J. 2008, 95 (5) 2308-17
59. Davis, A. J.; Jobe, A. H.; Hafner, D.; Ikegami, M. Lung function in premature lambs and rabbits treated with a recombinant SP-C surfactant Am. J. Respir. Crit. Care Med. 1998, 157 (2) 553-9
60. Spragg, R. G.; Lewis, J. F.; Walmrath, H. D.; Johannigman, J.; Bellingan, G.; Laterre, P. F.; Witte, M. C.; Richards, G. A.; Rippin, G.; Rathgeb, F.; Hafner, D.; Taut, F. J.; Seeger, W. Effect of recombinant surfactant protein C-based surfactant on the acute respiratory distress syndrome N. Engl. J. Med. 2004, 351 (9) 884-92
61. Schurch, S.; Green, F. H.; Bachofen, H. Formation and structure of surface films: captive bubble surfactometry Biochim. Biophys. Acta 1998, 1408 (2-3) 180-202