Structure and influence on stability and activity of the N-terminal propeptide part of lung surfactant protein C

FEBS Journal

Volumn 273, Issue 5, 2006, Pages 926-935

  Li, Jing ^a   Liepinsh, Edvards ^a   Almlén, Andreas ^a   Thyberg, Johan ^a   Curstedt, Tore ^a   Jörnvall, Hans ^a   Johansson, Jan ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Peptide aggregation; Peptide structure analysis; Proprotein processing; Surface activity; Surfactant protein

Indexed keywords

ALCOHOL; DODECYLPHOSPHORYLCHOLINE; LUNG SURFACTANT; PEPTIDE; SURFACTANT PROTEIN C;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONFORMATION; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PEPTIDE SYNTHESIS; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RACEMIC MIXTURE; SURFACE PROPERTY;

ANIMALS; CIRCULAR DICHROISM; DRUG STABILITY; HUMANS; HYDROGEN-ION CONCENTRATION; MICELLES; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN PRECURSORS; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; RABBITS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SWINE;

EID: 33644940734     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05124.x     Document Type: Article

References (46)

1. Johansson J Curstedt T 1997 Molecular structures and interactions of pulmonary surfactant components Eur J Biochem 244 675 693
2. Goerke J 1998 Pulmonary surfactant: functions and molecular composition Biochim Biophys Acta 1408 79 89
3. Whitsett JA Weaver TE 2002 Hydrophobic surfactant proteins in lung function and disease N Engl J Med 347 2141 2148
4. Garcia-Verdugo I Sanchez-Barbero F Soldau K Tobias PS Casals C 2005 Interaction of surfactant protein A (SP-A) with bacterial rough lipopolysaccharide (Re-LPS) and effects of SP-A on the binding of Re-LPS to CD14 and LPS binding protein Biochem J 391 115 124
5. Chaby R Garcia-Verdugo I Espinassous Q Augusto LA 2005 Interactions between LPS and lung surfactant proteins J Endotoxin Res 11 181 185
6. Senft AP Korfhagen TR Whitsett JA Shapiro SD LeVine AM 2005 Surfactant protein-D regulates soluble CD14 through matrix metalloproteinase-12 J Immunol 174 4953 4959
7. Glasser SW Korfhagen TR Bruno MD Dey C Whitsett JA 1990 Structure and expression of the pulmonary surfactant protein SP-C gene in the mouse J Biol Chem 265 21986 21991
8. Augusto L Le Blay K Auger G Blanot D Chaby R 2001 Interaction of bacterial lipopolysaccharide with mouse surfactant protein C inserted into lipid vesicles Am J Physiol Lung Cell Mol Physiol 281 L776 L785
9. Johansson J 1998 Structure and properties of surfactant protein C Biochim Biophys Acta 1408 161 172
10. Curstedt T Johansson J Persson P Eklund A Robertson B Lowenadler B Jornvall H 1990 Hydrophobic surfactant-associated polypeptides: SP-C is a lipopeptide with two palmitoylated cysteine residues, whereas SP-B lacks covalently linked fatty acyl groups Proc Natl Acad Sci USA 87 2985 2989
11. Wustneck N Wustneck R Perez-Gil J Pison U 2003 Effects of oligomerization and secondary structure on the surface behavior of pulmonary surfactant proteins SP-B and SP-C Biophys J 84 1940 1949
12. Gustafsson M Thyberg J Naslund J Eliasson E Johansson J 1999 Amyloid fibril formation by pulmonary surfactant protein C FEBS Lett 464 138 142
13. Szyperski T Vandenbussche G Curstedt T Ruysschaert JM Wuthrich K Johansson J 1998 Pulmonary surfactant-associated polypeptide C in a mixed organic solvent transforms from a monomeric alpha-helical state into insoluble beta-sheet aggregates Protein Sci 7 2533 2540
14. Luy B Diener A Hummel RP Sturm E Ulrich WR Griesinger C 2004 Structure and potential C-terminal dimerization of a recombinant mutant of surfactant-associated protein C in chloroform/methanol Eur J Biochem 271 2076 2085
15. Dluhy RA Shanmukh S Leapard JB Kruger P Baatz JE 2003 Deacylated pulmonary surfactant protein SP-C transforms from alpha-helical to amyloid fibril structure via a pH-dependent mechanism: an infrared structural investigation Biophys J 85 2417 2429
16. Gustafsson M Griffiths WJ Furusjo E Johansson J 2001 The palmitoyl groups of lung surfactant protein C reduce unfolding into a fibrillogenic intermediate J Mol Biol 310 937 950
17. Kallberg Y Gustafsson M Persson B Thyberg J Johansson J 2001 Prediction of amyloid fibril-forming proteins J Biol Chem 276 12945 12950
18. Hosia W Johansson J Griffiths WJ 2002 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 1 592 597
19. Beers MF Kim CY Dodia C Fisher AB 1994 Localization, synthesis, and processing of surfactant protein SP-C in rat lung analyzed by epitope-specific antipeptide antibodies J Biol Chem 269 20318 20328
20. Vorbroker DK Voorhout WF Weaver TE Whitsett JA 1995 Posttranslational processing of surfactant protein C in rat type II cells Am J Physiol 269 L727 L733
21. 2-terminal flanking domain are cleaved in late compartments Am J Respir Cell Mol Biol 24 253 263
22. Conkright JJ Bridges JP Na CL Voorhout WF Trapnell B Glasser SW Weaver TE 2001 Secretion of surfactant protein C, an integral membrane protein, requires the N-terminal propeptide J Biol Chem 276 14658 14664
23. Nogee LM Garnier G Dietz HC Singer L Murphy AM deMello DE Colten HR 1994 A mutation in the surfactant protein B gene responsible for fatal neonatal respiratory disease in multiple kindreds J Clin Invest 93 1860 1863
24. Hamvas A Cole FS deMello DE Moxley M Whitsett JA Colten HR Nogee LM 1994 Surfactant protein B deficiency: antenatal diagnosis and prospective treatment with surfactant replacement J Pediatr 125 356 361
25. Hamvas A Nogee LM Mallory GB Jr. Spray TL Huddleston CB August A Dehner LP deMello DE Moxley M Nelson R Cole FS Colten HR 1997 Lung transplantation for treatment of infants with surfactant protein B deficiency J Pediatr 130 231 239
26. Beers MF Hamvas A Moxley MA Gonzales LW Guttentag SH Solarin KO Longmore WJ Nogee LM Ballard PL 2000 Pulmonary surfactant metabolism in infants lacking surfactant protein B Am J Respir Cell Mol Biol 22 380 391
27. Vorbroker DK Profitt SA Nogee LM Whitsett JA 1995 Aberrant processing of surfactant protein C in hereditary SP-B deficiency Am J Physiol 268 L647 L656
28. Li J Ikegami M Na CL Hamvas A Espinassous Q Chaby R Nogee LM Weaver TE Johansson J 2004 N-terminally extended surfactant protein (SP) C isolated from SP-B-deficient children has reduced surface activity and inhibited lipopolysaccharide binding Biochemistry 43 3891 3898
29. Li J Hosia W Hamvas A Thyberg J Jornvall H Weaver TE Johansson J 2004 The N-terminal propeptide of lung surfactant protein C is necessary for biosynthesis and prevents unfolding of a metastable alpha-helix J Mol Biol 338 857 862
30. Chander A 1992 Dicyclohexylcarbodiimide and vanadate sensitive ATPase of lung lamellar bodies Biochim Biophys Acta 1123 198 206
31. Johansson J Szyperski T Wuthrich K 1995 Pulmonary surfactant-associated polypeptide SP-C in lipid micelles: CD studies of intact SP-C and NMR secondary structure determination of depalmitoyl-SP-C (1-17) FEBS Lett 362 261 265
32. Wishart DS Sykes BD Richards FM 1992 The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy Biochemistry 31 1647 1651
33. Plasencia I Rivas L Casals C Keough KM Perez-Gil J 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
34. Bi X Flach CR Perez-Gil J Plasencia I Andreu D Oliveira E Mendelsohn R 2002 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 8385 8395
35. Beers MF 1996 Inhibition of cellular processing of surfactant protein C by drugs affecting intracellular pH gradients J Biol Chem 271 14361 14370
36. Plasencia I Rivas L Keough KM Marsh D Perez-Gil J 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
37. Plasencia I Keough KM Perez-Gil J 2005 Interaction of the N-terminal segment of pulmonary surfactant protein SP-C with interfacial phospholipid films Biochim Biophys Acta 1713 118 128
38. Johansson J Persson P Lowenadler B Robertson B Jornvall H Curstedt T 1991 Canine hydrophobic surfactant polypeptide SP-C. A lipopeptide with one thioester-linked palmitoyl group FEBS Lett 281 119 122
39. Johansson J Some M Linderholm BM Almlen A Curstedt T Robertson B 2003 A synthetic surfactant based on a poly-Leu SP-C analog and phospholipids: effects on tidal volumes and lung gas volumes in ventilated immature newborn rabbits J Appl Physiol 95 2055 2063
40. Stark M Wang Y Danielsson O Jornvall H Johansson J 1998 Determination of proteins, phosphatidylethanolamine, and phosphatidylserine in organic solvent extracts of tissue material by analysis of phenylthiocarbamyl derivatives Anal Biochem 265 97 102
41. Curstedt T Jornvall H Robertson B Bergman T Berggren P 1987 Two hydrophobic low-molecular-mass protein fractions of pulmonary surfactant. Characterization and biophysical activity Eur J Biochem 168 255 262
42. Gustafsson M Curstedt T Jornvall H Johansson J 1997 Reverse-phase HPLC of the hydrophobic pulmonary surfactant proteins: detection of a surfactant protein C isoform containing Nε-palmitoyl-lysine Biochem J 326 799 806
43. Wuthrich K 1986 NMR of Proteins and Nucleic Acid Wiley New York
44. Guntert P Mumenthaler C Wuthrich K 1997 Torsion angle dynamics for NMR structure calculation with the new program DYANA J Mol Biol 273 283 298
45. Luginbuhl P Guntert P Billeter M Wuthrich K 1996 The new program OPAL for molecular dynamics simulations and energy refinements of biological macromolecules J Biomol NMR 8 136 146
46. Schurch S Bachofen H Goerke J Possmayer F 1989 A captive bubble method reproduces the in situ behavior of lung surfactant monolayers J Appl Physiol 67 2389 2396