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

Biophysical Journal

Volumn 95, Issue 5, 2008, Pages 2308-2317

  Gonzalez Horta, Azucena ^a   Andreu, David ^b   Morrow, Michael R ^c   Perez Gil, Jesús ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE; CYSTEINE; DIPALMITOYLPHOSPHATIDYLCHOLINE; SURFACTANT PROTEIN C;

ARTICLE; CHEMISTRY; LIPID BILAYER; LIPOYLATION; NUCLEAR MAGNETIC RESONANCE; TEMPERATURE;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; CHOLINE; CYSTEINE; LIPID BILAYERS; LIPOYLATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; TEMPERATURE;

EID: 51649096963     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.132845     Document Type: Article

References (69)

1. Daniels, C. B., and S. Orgeig. 2003. Pulmonary surfactant: the key to the evolution of air breathing. News Physiol. Sci. 18:151-157.
2. deMello, D. E. 2004. Pulmonary pathology. Semin. Neonatol. 9:311-329.
3. Whitsett, J. A., S. E. Wert, and Y. Xu. 2005. Genetic disorders of surfactant homeostasis. Biol. Neonate. 87:283-287.
4. Wright, J. R. 1997. Immunomodulatory functions of surfactant. Physiol. Rev. 77:931-962.
5. Goerke, J. 1998. Pulmonary surfactant functions and molecular composition. Biochim. Biophys. Acta. 1408:79-89.
6. Veldhuizen, J. A., and H. P. Haagsman. 2000. Role of pulmonary surfactant component in surface film formation and dynamics. Biochim. Biophys. Acta. 1467:255-270.
7. Whitsett, J. A., and T. E. Weaver. 2002. Hydrophobic surfactant proteins in lung function and disease. N. Engl. J. Med. 347:2141-2148.
8. Chaby, R. 2004. Lipopolysaccharide-binding molecules: transporters, blockers and sensors. Cell. Mol. Life Sci. 61:1697-1713.
9. Crouch, E. C. 1998. Structure, biologic properties and expression of surfactant protein D (SP-D). Biochim. Biophys. Acta. 1408:278-289.
10. Perez-Gil, J. 2002. Molecular interactions in pulmonary surfactant films. Biol. Neonate. 81(Suppl 1):6-15.
11. Perez-Gil, J., and K. M. Keough. 1998. Interfacial properties of surfactant proteins. Biochim. Biophys. Acta. 1408:203-217.
12. Serrano, A. G., and J. Pérez-Gil. 2006. Protein-lipid interactions and surface activity in the pulmonary surfactant system. Chem. Phys. Lipids. 141:108-115.
13. Lukovic, D., I. Plasencia, F. J. Taberner, J. Salgado, J. J. Calvete, J. Perez-Gil, and I. Mingarro. 2006. Production and characterization of recombinant forms of human pulmonary surfactant protein C (SP-C): structure and surface activity. Biochim. Biophys. Acta. 1758:509-518.
14. Oosterlaken-Dijksterhuis, M. A., H. P. Haagsman, L. M. van Golde, and R. A. Demel. 1991. Characterization of lipid insertion into mono-molecular layers mediated by lung surfactant proteins SP-B and SP-C. Biochemistry. 30:10965-10971.
15. Perez-Gil, J., J. Tucker, G. Simatos, and K. M. Keough. 1992. Interfacial adsorption of simple lipid mixtures combined with hydrophobic surfactant protein from pig lung. Biochem. Cell Biol. 70:332-338.
16. Palmblad, M., M. Gustafsson, T. Curstedt, J. Johansson, and S. Schurch. 2001. Surface activity and film formation from the surface associated material of artificial surfactant preparations. Biochim. Biophys. Acta. 1510:106-117.
17. Veldhuizen, E. J., R. V. Diemel, G. Putz, L. M. van Golde, J. J. Batenburg, and H. P. Haagsman. 2001. Effect of the hydrophobic surfactant proteins on the surface activity of spread films in the captive bubble surfactometer. Chem. Phys. Lipids. 110:47-55.
18. Glasser, S. W., M. S. Burhans, T. R. Korfhagen, C. L. Na, P. D. Sly, G. F. Ross, M. Ikegami, and J. A. Whitsett. 2001. Altered stability of pulmonary surfactant in SP-C-deficient mice. Proc. Natl. Acad. Sci. USA. 98:6366-6371.
19. Cruz, A., C. Casals, and J. Perez-Gil. 1995. Conformational flexibility of pulmonary surfactant proteins SP-B and SP-C, studied in aqueous organic solvents. Biochim. Biophys. Acta. 1255:68-76.
20. Perez-Gil, J., A. Cruz, and C. Casals. 1993. 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. 1168:261-270.
21. Vandenbussche, G., A. Clercx, T. Curstedt, J. Johansson, H. Jornvall, and J.-M. Ruysschaert. 1992. Structure and orientation of the surfactant associated protein C in a lipid bilayer. Eur. J. Biochem. 203:201-209.
22. Johansson, J., T. Szyperski, T. Curstedt, and K. Wuthrich. 1994. The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich alpha-helix. Biochemistry. 33:6015-6023.
23. Johansson, J., G. Nilson, R. Stromberg, B. Robertson, H. Jörnvall, and T. Curstedt. 1995. Secondary structure and biophysical activity of synthetic analogues of the pulmonary surfactant polypeptide SP-C. Biochem. J. 307:535-541.
24. Plasencia, I., L. Rivas, C. Casals, K. M. Keough, and J. Pérez-Gil. 2001. Intrinsic structural differences in the N-terminal segment of pulmonary surfactant protein SP-C from different species. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129:129-139.
25. Dunphy, J. T., and M. E. Linder. 1998. Signaling functions of protein palmitoylation. Biochim. Biophys. Acta. 1436:245-261.
26. Resh, M. D. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta. 1451:1-16.
27. Bijlmakers, M. J., and M. Marsh. 2003. The on-off story of protein palmitoylation. Trends Cell Biol. 13:32-42.
28. Gustafsson, M., W. J. Griffiths, E. Furusjo, and J. Johansson. 2001. The palmitoyl groups of lung surfactant protein C reduce unfolding into a fibrillogenic intermediate. J. Mol. Biol. 310:937-950.
29. Schürch, S., F. H. Green, and H. Bachofen. 1998. Formation and structure of surface films: captive bubble surfactometry. Biochim. Biophys. Acta. 1408:180-202.
30. Gustafsson, M., M. Palmblad, T. Curstedt, J. Johansson, and S. Schürch. 2000. Palmitoylation of a pulmonary surfactant protein C analogue affects the surface associated lipid reservoir and film stability. Biochim. Biophys. Acta. 1466:169-178.
31. Johansson, J. 2001. Membrane properties and amyloid fibril formation of lung surfactant proteins C. Biochem. Soc. Trans. 29:601-606.
32. Wang, Z., O. Gurel, J. E. Baatz, and R. H. Notter. 1996. Acylation of pulmonary surfactant protein-C is required for its optimal surface active interactions with phospholipids. J. Biol. Chem. 271:19104-19109.
33. Flach, C. R., A. Gericke, K. M. W. Keough, and R. Mendelsohn. 1999. Palmitoylation of lung surfactant protein SP-C alters surface thermodynamics, but not protein secondary structure or orientation in 1,2- dipalmitoylphosphatidylcholine. Biochim. Biophys. Acta. 1416:11-20.
34. Qanbar, R., S. Cheng, F. Possmayer, and S. Schurch. 1996. Role of the palmitoylation of surfactant associated protein C in surfactant film formation and stability. Am. J. Physiol. Lung Cell. Mol. Physiol. 271:L572-L580.
35. Shiffer, K., S. Hawgood, H. P. Haagsman, B. Benson, J. A. Clements, and J. Goerke. 1993. Lung surfactant proteins, SP-B and SP-C, alter the thermodynamic properties of phospholipid membranes: a differential calorimetry study. Biochemistry. 32:590-597.
36. Simatos, G. A., K. B. Forward, M. R. Morrow, and K. M. W. Keough. 1990. Interaction between perdeuterated dimyristoylphosphatidylcholine and low molecular weight pulmonary surfactant protein SP-C. Biochemistry. 29:5807-5814.
37. Pastrana-Rios, B., S. Taneva, K. M. Keough, A. J. Mautone, and R. Mendelsohn. 1995. External reflection absorption infrared spectroscopy study of lung surfactant proteins SP-B and SP-C in phospholipid monolayers at the air/water interface. Biophys. J. 69:2531-2540.
38. Perez-Gil, J., C. Casals, and D. Marsh. 1995. Interactions of hydrophobic lung surfactant proteins SP-B and SP-C with dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylglycerol bilayers studied by electron spin resonance spectroscopy. Biochemistry. 34:3964-3971.
39. Dico, A. S., S. Taneva, M. R. Morrow, and K. M. Keough. 1997. Effect of calcium on phospholipid interaction with pulmonary surfactant protein C. Biophys. J. 73:2595-2602.
40. 2H-NMR studies of the effect of pulmonary surfactant SP-C on the 1,2-dipalmitoyl-sn-glycero-3-phosphocholine headgroup: a model for transbilayer peptides in surfactant and biological membranes. Biochemistry. 32:11338-11344.
41. Plasencia, I., L. Rivas, K. M. Keough, D. Marsh, and J. Pérez-Gil. 2004. The N-terminal segment of pulmonary surfactant lipopeptide SP-C has intrinsic propensity to interact with and perturb phospholipid bilayers. Biochem. J. 377:183-193.
42. Plasencia, I., K. M. Keough, and J. Perez-Gil. 2005. Interaction of the N-terminal segment of pulmonary surfactant protein SP-C with interfacial phospholipid films. Biochim. Biophys. Acta. 1713:118-128.
43. Bi, X., C. R. Flach, J. Pérez-Gil, I. Plasencia, D. Andreu, E. Oliveira, and R. Mendelsohn. 2002. Secondary structure and lipid interactions of the N-terminal segment of pulmonary surfactant SP-C in Langmuir films: IR reflection-adsorption spectroscopy and surface pressure studies. Biochemistry. 41:8385-8395.
44. Bartlett, G. R. 1959. Phosphorus assay in column chromatography. J. Biol. Chem. 234:466-468.
45. 2H-NMR. Biochim. Biophys. Acta. 737:117-171.
46. Plasencia, I., F. Baumgart, D. Andreu, D. Marsh, and J. Perez-Gil. 2008. Effect of acylation on the lipid-protein interactions of the N-terminal segment of pulmonary surfactant protein SP-C. Biochim. Biophys. Acta. 1778:1274-1282.
47. Seelig, J., P. M. Macdonald, and P. G. Scherer. 1987. Phospholipid headgroups as sensors of electric charge in membranes. Biochemistry. 26:7535-7541.
48. Bloom, M., and I. C. P. Smith. 1985. Manifestations of lipid-protein interactions in deuterium NMR. In Progress in Protein-Lipid Interactions. Elsevier, Amsterdam. 61-76.
49. Morrow, M. R., N. Abu-Libdeh, J. Stewart, and K. M. W. Keough. 2003. Interaction of pulmonary surfactant protein SP-A with DPPC/egg-PG bilayers. Biophys. J. 85:2397-2405.
50. Scherer, P. G., and J. Seelig. 1989. Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles. Biochemistry. 28:7720-7728.
51. MacDonald, P. M., J. Leisen, and F. M. Marassi. 1991. Response of phosphatidylcholine in the gel and liquid-crystalline states to membrane surface charges. Biochemistry. 30:3558-3566.
52. Macdonald, P. M., and J. Seelig. 1987. Calcium binding to mixed phosphatidylglycerol-phosphatidylcholine bilayers as studied by deuterium nuclear magnetic resonance. Biochemistry. 26:1231-1240.
53. Davis, J. H. 1979. Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys. J. 27:339-358.
54. Seelig, J. 1977. Deuterium magnetic resonance: theory and application to lipid membranes. Q. Rev. Biophys. 10:353-418.
55. Conkright, J. J., J. P. Bridges, C. L. Na, W. F. Voorhout, S. W. Trapnell, and T. E. Weaver. 2001. Secretion of surfactant protein C (SP-C), an integral membrane protein requires the N-terminal propeptide. J. Biol. Chem. 276:14658-14664.
56. Brinke, A. T., J. J. Batenburg, B. M. Gadella, H. P. Haagsman, A. B. Vaandrager, and L.M.G. vanGolde. 2001. The juxtamembrane lysine and arginine residues of surfactant protein C precursor influence palmitoylation via effects on trafficking. Am. J. Respir. Cell Mol. Biol. 25:156-163.
57. Kramer, A., A. Wintergalen, M. Sieber, H. J. Galla, M. Amrein, and R. Guckenberger. 2000. Distribution of the surfactant-associated protein C within a lung surfactant model film investigated by near-field optical microscopy. Biophys. J. 78:458-465.
58. Malcharek, S., A. Hinz, L. Hilterhaus, and H. J. Galla. 2005. Multilayer structures in lipid monolayer films containing surfactant protein C: effects of cholesterol and POPE. Biophys. J. 88:2638-2649.
59. Wang, L., P. Cai, H. J. Galla, H. He, C. R. Flach, and R. Mendelsohn. 2005. Monolayer-multilayer transitions in a lung surfactant model: IR reflection-absorption spectroscopy and atomic force microscopy. Eur. Biophys. J. 34:243-254.
60. de Vries, A. H., S. Yefimov, A. E. Mark, and S. J. Marrink. 2005. Molecular structure of the lecithin ripple phase. Proc. Natl. Acad. Sci. USA. 102:5392-5396.
61. 2H-NMR spectroscopy in partially ordered systems. In Isotopes in the Physical and Biomedical Science, vol. 2. E. Buncel and J. R. Jones, editors. Elsevier, Amsterdam. 99-157.
62. Morrow, M. R., J. Perez-Gil, G. Simatos, C. Boland, J. Stewart, D. Absolom, V. Sarin, and K. M. W. Keough. 1993. Pulmonary surfactant-associated protein SP-B has little effect on acyl chains in dipalmitoyl-phosphatidylcholine dispersions. Biochemistry. 32:4397-4402.
63. 2H-NMR. Biophys. J. 90:3632-3642.
64. Higuchi, M., K. M. Izumi, and E. Kieff. 2001. Epstein-Barr virus latent-infection membrane proteins are palmitoylated and raft-associated: protein 1 binds to the cytoskeleton through TNF receptor cytoplasmic factors. Proc. Natl. Acad. Sci. USA. 98:4675-4680.
65. Moffett, S., D. A. Brown, and M. E. Linder. 2000. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275:2191-2198.
66. Shogomori, H., A. T. Hammond, A. G. Ostermeyer-Fay, D. J. Barr, G. W. Feigenson, E. London, and D. A. Brown. 2005. Palmitoylation and intracellular domain interactions both contribute to raft targeting of linker for activation of T cells. J. Biol. Chem. 280:18931-18942.
67. Tanimura, N., S. Saitoh, S. Kawano, A. Kosugi, and K. Miyake. 2006. Palmitoylation of LAT contributes to its subcellular localization and stability. Biochem. Biophys. Res. Commun. 341:1177-1183.
68. Pedersen, T. B., T. Kaasgaard, M. O. Jensen, S. Frokjaer, O. G. Mouritsen, and K. Jorgensen. 2005. Phase behavior and nanoscale structure of phospholipid membranes incorporated with acylated C14-peptides. Biophys. J. 89:2494-2503.
69. Yousefi-Salakdeh, E., J. Johansson, and R. Stromberg, 1999. A method for S- and O-palmitoylation of peptides: synthesis of pulmonary surfactant protein-C models. Biochem. J. 343:557-562.