Structural model for an AxxxG-mediated dimer of surfactant-associated protein C

European Journal of Biochemistry

Volumn 271, Issue 11, 2004, Pages 2086-2092

  Kairys, Visvaldas ^a   Gilson, Michael K ^a   Luy, Burkhard ^b  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Dimerization; Docking; Surfactant associated protein C (SP C)

Indexed keywords

DIMER; GLYCOPHORIN A; SURFACTANT; SURFACTANT PROTEIN C;

ARTICLE; DIMERIZATION; EXPERIMENTAL MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; ANIMALS; COMPUTATIONAL BIOLOGY; DIMERIZATION; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C;

SUIDAE;

EID: 2942577480     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04107.x     Document Type: Article

References (58)

1. Avery, M.E. & Mead, J. (1959) Surface properties in relation to atelectasis and hyaline membrane disease. Am. J. Dis. Child. 97, 917.
2. Shapiro, D.L. & Notter, R.H. (1989) Surfactant Replacement Therapy. Alan R. Liss, New York.
3. Robertson, B. & Halliday, H.L. (1998) Principles of surfactant replacement therapy. Biochim. Biophys. Acta 1408, 346-361.
4. Nogee, L.M., Garnier, G., Dietz, H.C., Singer, L., Murphy, A.M., deMello, D.E. & Colten, H.R. (1994) A mutation in the surfactant protein B gene responsible for fatal neonatal respiratory disease in multiple kindreds. J. Clin. Invest. 93, 1860-1863.
5. Wert, S.E., Profitt, S.A., Whitsett, J.A. & Nogee, L.M. (1998) Distinct patterns of surfactant protein (sp) expression in neonatal lung disease. Am. J. Respir. Crit. Care Med. 157, A698.
6. Nogee, L.M., Dunbar, A.E., Wert, S.E., Askin, F., Hamvas, A. & Whitsett, J.A. (2001) Brief report: a mutation in the surfactant protein C gene associated with familial interstitial lung disease. N. Engl. J. Med. 344, 573-579.
7. Jobe, A.H. (1998) Hot topics in and new strategies for surfactant research. Biol. Neonate 74, 3-8.
8. Halliday, H.L. (1996) Natural vs. synthetic surfactants in neonatal respiratory distress syndrome. Drugs 51, 226-237.
9. Veldhuizen, E.J.A., Waring, A.J., Walther, F.J., Batenburg, J.J., van Golde, L.M.G. & Haagsman, H.P. (2000) Dimeric N-terminal segment of human surfactant protein B (dSP-B (1-25)) has enhanced surface properties compared to monomeric (SP-B (1-25)). Biophys. J. 79, 377-384.
10. Veldhuizen, E.J.A. & Haagsman, H.P. (2000) Role of pulmonary surfactant components in surface film formation and dynamics. Biochim. Biophys. Acta 1467, 255-270.
11. Curstedt, T., Jörnvall, 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.
12. Takamoto, D.Y., Lipp, M.M., von Nahmen, A., Lee, K.Y.C., Waring, A.J. & Zasadzinski, J.A. (2001) Interaction of lung surfactant proteins with anionic phospholipids. Biophys. J. 81, 153-169.
13. Lipp, M.M., Lee, K.Y.C., Takamoto, D.Y., Zasadzinski, J.A. & Waring, A.J. (1996) Coexistence of buckled and flat monolayers. Phys. Rev. Lett. 81, 1650-1653.
14. Lipp, M.M., Lee, K.Y., Waring, A. & Zasadzinski, J.A. (1997) Fluorescence, polarized fluorescence, and Brewster angle microscopy of palmitic acid and lung surfactant protein B monolayers. Biophys. J. 72, 2783-2804.
15. Lee, K.Y.C., Majewski, J., Kuhl, T.L., Howes, P.B., Kjaer, K., Lipp, M.M., Waring, A.J., Zasadzinski, J.A. & Smith, G.S. (2001) Synchrotron X-ray study of lung surfactant-specific protein SP-B in lipid monolayers. Biophys. J. 81, 572-585.
16. Kruger, P., Schalke, M., Wang, Z., Notter, R.H., Dluhy, R.A. & Losche, M. (1999) Effect of hydrophobic surfactant peptides SP-B and SP-C on binary phospholipid monolayers. I. Fluorescence and dark-field microscopy. Biophys. J. 77, 903-914.
17. Johansson, J., Szyperski, T., Curstedt, T. & Wüthrich, K. (1994) NMR solution structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich alpha-helix. Biochemistry 33, 6015-6023.
18. Johansson, J. (1998) Structure and properties of surfactant protein C. Biochim. Biophys. Acta 1408, 203-217.
19. MacKenzie, K.R., Prestegard & Engelman, D.M. (1997) A transmembrane helix dimer: structure and implications. Science 276, 131-133.
20. Smith, S.O., Song, D., Shekar, S., Groesbeek, M., Ziliox, M. & Aimoto, S. (2001) Structure of the transmembrane dimer interface of Glycophorin A in membrane bilayers. Biochemistry 40, 6553-6558.
21. Luy, B., Diener, A., Hummel, R.-P., Sturm, E., Ulrich, W.-R. & 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.
22. Nilges, M. & Brunger, A.T. (1993) Successful prediction of the coiled coil geometry of the GCN4 leucine zipper domain by simulated annealing: comparison to the X-ray structure. Protein Struct. Funct. Gen. 15, 133-146.
23. Adams, P.D., Engelman, D.M. & Brunger, A.T. (1996) Improved prediction for the structure of the dimeric transmembrane domain of Glycophorin A obtained through global searching. Protein Struct. Funct. Gen. 26, 257-261.
24. Head, M.S., Given, J.A. & Gilson, M.K. (1997) 'Mining Minima': direct computation of conformational free energy. J. Phys. Chem. 101, 1609-1618.
25. David, L., Luo, R. & Gilson, M.K. (2001) Ligand-receptor docking with the mining minima optimizer. J. Comput. Aided Mol. Des. 15, 157-171.
26. Szyperski, T., Vandenbussche, G., Curstedt, T., Ruysschaert, J.M., Wüthrich, 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.
27. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S. & Karplus, M. (1983) CHARMM: a program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4, 187-217.
28. Gilson, M.K. & Honig, B. (1991) The inclusion of electrostatic hydration energies in molecular mechanics calculations. J. Comput. Aided Mol. Des. 5, 5-20.
29. Still, W.C., Tempczyk, A., Hawley, R.C. & Hendrickson, T. (1990) Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112, 6127-6129.
30. Qiu, D., Shenkin, P.S., Hollinger, P.P. & Still, W.C. (1997) The GB/SA continuum model for solvation. a fast analytical method for the calculation of approximate born radii. J. Phys. Chem. 101, 3005-3014.
31. Gericke, A., Flach, C.R. & Mendelsohn, R. (1997) Structure and orientation of lung surfactant SP-C and 1-alpha-dipalmitoylphosphatidylcholine in aqueous monolayers. Biophys. J. 73, 492-499.
32. Derewenda, Z.G., Lee, L. & Derewenda, U. (1995) The occurence of C-H⋯O hydrogen bonds in proteins. J. Mol. Biol. 252, 248-262.
33. Bella, J. & Berman, H.M. (1996) Crystallographic evidence for C (alpha) -H⋯O=C hydrogen bonds in a collagen triple helix. J. Mol. Biol. 264, 734-742.
34. Vargas, R., Garza, J., Dixon, D.A. & Hay, B.P. (2000) How strong is the C(alpha)-H⋯O hydrogen bond? J. Am. Chem. Soc. 122, 4750-4755.
35. Scheiner, S., Kar, T. & Gu, Y. (2001) Strength of the C(alpha)-H⋯O hydrogen bond of amino acid residues. J. Biol. Chem. 276, 9832-9837.
36. Senes, A., Ubarretxena-Belandia, I. & Engelman, D.M. (2001) The C(alpha)-H⋯O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions. Proc. Natl Acad. Sci. USA 98, 9056-9061.
37. Eilers, M., Patel, A.B., Liu, W. & Smith, S.O. (2002) Comparison of helix interactions in membrane and soluble alpha-bundle proteins. Biophys. J. 82, 2720-2736.
38. Smith, S.O., Eilers, M., Song, D., Crocker, E., Ying, W., Groesbeek, M., Metz, G., Ziliox, M. & Aimoto, S. (2002) Implications of threonine hydrogen bonding in the Glycophorin A transmembrane helix dimer. Biophys. J. 82, 2476-2486.
39. Eilers, M., Shekar, S.C., Shieh, T., Smith, S.O. & Fleming, P.J. (2000) Internal packing of helical membrane proteins. Proc. Natl Acad. Sci. USA 97, 5796-5801.
40. Javadpour, M.M., Eilers, M., Groesbeek, M. & Smith, S.O. (1999) Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys. J. 77, 1609-1618.
41. Russ, W.P. & Engelman, D.M. (1998) The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296, 911-919.
42. Senes, A., Gerstein, M. & Engelman, D.M. (2000) Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions. J. Mol. Biol. 296, 921-936.
43. Mendrola, J.M., Berger, M.B., King, M.C. & Lemmon, M.A. (2002) The single transmembrane domains of ErbB receptors self-associate in cell membranes. J. Biol. Chem. 277, 4704-4712.
44. Sternberg, M.J. & Gullick, W.J. (1989) Neu receptor dimerization. Nature (London) 339, 587.
45. Sternberg, M.J. & Gullick, W.J. (1990) A sequence motif in the transmembrane region of growth factors with tyrosine kinase activity mediates dimerization. Protein Eng. 3, 245-248.
46. Smith, S.O., Smith, C., Shekar, S., Peersen, O., Ziliox, M. & Aimoto, S. (2002) Transmembrane interactions in the activation of the Neu receptor tyrosine kinase. Biochemistry 41, 9321-9332.
47. Gottschalk, K.E., Adams, P.D., Brunger, A.T. & Kessler, H. (2002) Transmembrane signal transduction of the alpha-IIb beta-3 integrin. Protein Sci. 11, 1800-1812.
48. Kleiger, G., Grothe, R. & Mallick, P. (2002) GXXXG and AXXXA: common alpha-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41, 5990-5997.
49. Kleiger, G. & Eisenberg, D. (2002) GXXXG and GXXXA motifs stabilize FAD and NAD (P)-binding Rossmann folds through C-alpha-H⋯O hydrogen bonds and van der Waals interactions. J. Mol. Biol. 323, 69-76.
50. Bernhard, W., Mottaghian, J., Gebert, A., Rau, G.A., von der Hardt, H. & Poets, C.F. (2000) Commercial versus native surfactants. Surface activity, molecular components and the effect of calcium. Am. J. Respir. Crit. Care Med. 162, 1524-1533.
51. Przybylski, M., Maier, C., Hägele, K., Bauer, E., Hannappel, E., Nave, R., Melchers, K., Krüger, U., Schäfer, K.P. (1994) Primary structure elucidation, surfactant function and specific formation of supramolecular dimer structures of lung surfactant associated SP-C proteins. In Peptides, Chemistry, Structure and Biology (Hodges, R.S. & Smith, J.A., eds), pp. 338-340. Escom Science Publishers, Leiden.
52. Mayer-Fligge, P., Volz, J., Krüger, U., Sturm, E., Gernandt, W., Schäfer, K.P. & Przybylski, M. (1998) Synthesis and structural characterization of human-identical lung surfactant SP-C protein. J. Pept. Sci. 4, 355-363.
53. Wang, W., Russo, S.J., Mulugeta, S. & Beers, M.F. (2002) Biosynthesis of surfactant protein C (SP-C). Sorting of SP-C proprotein involves homomeric association via a signal anchor domain. J. Biol. Chem. 277, 19929-19937.
54. Seidl, A. (2003) Massenspektrometrische Analyse: Chemische Modifizierung und Synthese von Lipoproteinen. PhD Thesis, Gorre-Verlag, Konstanz, Germany.
55. Epand, R.M. & Epand, R.F. (2000) Modulation of membrane curvature by peptides. Biopol. Pept. Sci. 55, 358-363.
56. Zasadzinski, J.A., Ding, J., Warringer, H.E., Bringezu, F. & Waring, A.J. (2001) The physics and physiology of lung surfactants. Curr. Opin. Coll. Inter. Sci. 506-513.
57. Word, J.M., Lovett, S.C., LaBean, T.H., Taylor, H.C., Zalis, M.C., Presley, B.K., Richardson, J.S. & Richardson, D.C. (1999) Visualizing and quantifying molecular goodness-of-fit: small probe contact dots with explicit hydrogen atoms. J. Mol. Biol. 285, 1711-1733.
58. Richardson, D.C. & Richardson, J.S. (1992) The kinemage: a tool for scientific communication. Protein Sci. 1, 3-9.