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Perturbation of DPPC bilayers by high concentrations of pulmonary surfactant protein SP-B

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Abstract

Deuterium (2H) NMR has been used to observe perturbation of dipalmitoylphosphatidylcholine (DPPC) bilayers by the pulmonary surfactant protein B (SP-B) at concentrations up to 17% (w/w). Previous 2H NMR studies of DPPC/dipalmitoylphosphatidylglycerol (DPPG) (7:3) bilayers containing up to 11% (w/w) SP-B and DPPC bilayers containing up to 11% (w/w) synthetic SP-B indicated a slight effect on bilayer chain order and a more substantial effect on motions that contribute to decay of quadrupole echoes obtained from bilayers of deuterated DPPC. This is consistent with the perturbation of headgroup-deuterated DPPC reported here for bilayers containing 6 and 9% (w/w) SP-B. For the higher concentrations of SP-B investigated in the present work, 2H NMR spectra of DPPC deuterated in both the headgroup and chain display a prominent narrow component consistent with fast, large amplitude reorientation of some labeled lipid. Similar spectral perturbations have been reported for bilayers in the presence of the antibiotic polypeptide nisin. The observation of large amplitude lipid reorientation at high SP-B concentration could indicate that SP-B can induce regions of high bilayer curvature and thus provides some insight into local interaction of SP-B with DPPC. Such local interactions may be relevant to the formation, in vitro and in vivo, of tubular myelin, a unique structure found in extracellular pulmonary surfactant, and to the delivery of surfactant material to films at the air–water interface.

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Fig. 1a–d
Fig. 2
Fig. 3a, b
Fig. 4a, b

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Abbreviations

DPPC:

1,2-dipalmitoyl-sn-glycero-3-phosphocholine

DPPG:

1,2-dipalmitoyl-sn-glycero-3-phosphoglycerol

DPPC-d 62 :

1,2-perdeuterodipalmitoyl-sn-glycero-3-phosphocholine

DPPC-d 4 :

1,2-dipalmitoyl-sn-glycero-3-phospho-(α,β perdeutero)-choline

References

  • Abragam A (1961) The principles of nuclear magnetism. Oxford University Press, London

  • Andersson M, Curstedt T, Jörnvall H, Johansson J (1995) An amphipathic helical motif common to tumorolytic polypeptide NK-lysin and pulmonary surfactant polypeptide SP-B. FEBS Lett 362:328–332

    Article  CAS  PubMed  Google Scholar 

  • Bartlett G (1959) Phosphorus assay in column chromatography. J Biol Chem 234:466–468

    CAS  Google Scholar 

  • Bloom M, Evans E (1991) Observation of surface undulations on the mesoscopic length scale by NMR. In: Peliti L (ed) Biologically inspired physics. Plenum, New York, pp 137–147

  • Bloom M, Sternin E (1987) Transverse nuclear spin relaxation in phospholipid bilayer membranes. Biochemistry 26:2101–2105

    CAS  Google Scholar 

  • Cruz A, Casals C, Plasencia I, Marsh D, Pérez-Gil J (1998) Depth profiles of pulmonary surfactant B in phosphatidylcholine bilayers studied by fluorescence and electron spin resonance spectroscopy. Biochemistry 37:9488–9496

    Article  CAS  PubMed  Google Scholar 

  • Curstedt T, Johansson J, Barros-Soderling J, Robertson B, Nilsson G, Westberg M, Jornvall H (1988) Low-molecular-mass surfactant protein type 1. The primary structure of a hydrophobic 8-kDa polypeptide with eight half-cystine residues. Eur J Biochem 172:521–525

    CAS  PubMed  Google Scholar 

  • Curstedt T, Johansson J, Persson P, Eklund A, Robertson B, Löwenadler B, Jörnvall 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

    CAS  PubMed  Google Scholar 

  • Davis J, Jeffrey K, Bloom M, Valic M, Higgs T (1976) Quadrupole echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem Phys Lett 42:390–394

    Article  CAS  Google Scholar 

  • Davis J (1983) The description of membrane lipid conformation, order and dynamics by 2H-NMR. Biochim Biophys Acta 737:117–171

    Article  CAS  PubMed  Google Scholar 

  • Dico A, Hancock J, Morrow M, Stewart J, Harris S, Keough K (1997) Pulmonary surfactant protein SP-B interacts similarly with dipalmitoylphosphatidylglycerol and dipalmitoylphosphatidylcholine in phosphatidylcholine/phosphatidylglycerol mixture. Biochemistry 36:4172–4177

    Article  CAS  PubMed  Google Scholar 

  • El Jastimi R, Edwards K, Lafleur M (1999) Characterization of permeability and morphological perturbations induced by nisin on phosphatidylcholine membranes. Biophys J 77:842–852

    PubMed  Google Scholar 

  • Fiech D, Bonev B, Morrow M (1998) Effect of pressure on dimyristoylphosphatidylcholine headgroup dynamics. Phys Rev E 57:3334–3343

    Article  CAS  Google Scholar 

  • Goerke J (1998) Pulmonary surfactant: functions and molecular composition. Biochim Biophys Acta 1408:79–89

    Article  CAS  PubMed  Google Scholar 

  • Hawgood S, Derrick M, Poulain F (1998) Structure and properties of surfactant protein B. Biochim Biophys Acta 1408:150–160

    CAS  PubMed  Google Scholar 

  • Keough K, Kariel N (1987) Differential scanning calorimetric studies of aqueous dispersions of phosphatidylcholines containing two polyenoic chains. Biochim Biophys Acta 902:11–18

    Article  CAS  PubMed  Google Scholar 

  • Kilfoil M, Morrow M (1998) Slow motions in bilayers containing anionic phospholipids. Physica A 261:82–94

    Article  CAS  Google Scholar 

  • Morrow M, Pérez-Gil J, Simatos G, Boland C, Stewart J, Absolom D, Sarin V, Keough K (1993a) Pulmonary surfactant-associated protein SP-B has little effect on acyl chains in dipalmitoylphosphatidylcholine dispersions. Biochemistry 32:4397–4402

    CAS  PubMed  Google Scholar 

  • Morrow M, Taneva S, Simatos G, Allwood L, Keough K (1993b) 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

    CAS  PubMed  Google Scholar 

  • Pauls K, MacKay A, Söderman O, Bloom M, Tangea A, Hodges R (1985) Dynamic properties of the backbone of an integral membrane polypeptide measured by 2H-NMR. Eur Biophys J 12:1–11

    CAS  PubMed  Google Scholar 

  • Poulain F, Allen L, Williams M, Hamilton R, Hawgood S (1992) Effects of surfactant apolipoproteins on liposome structure: implications for tubular myelin formation. Am J Physiol 262 (Lung Cell Mol Physiol 6):L730–L739

    CAS  PubMed  Google Scholar 

  • Prosser R, Davis J, Dahlquist F, Lindorfer M (1991) 2H nuclear magnetic resonance of the gramicidin A backbone in a phospholipid bilayer. Biochemistry 30:4687–4696

    CAS  PubMed  Google Scholar 

  • Sarin V, Gupta S, Leung T, Taylor V, Ohning B, Whitsett J, Fox J (1990) Biophysical and biological activity of a synthetic 8.7 kDa hydrophobic pulmonary surfactant protein SP-B. Proc Natl Acad Sci USA 87:2633–2637

    CAS  PubMed  Google Scholar 

  • Seelig J, Macdonald P, Scherer P (1987) Phospholipid head groups as sensors of electric charge in membranes. Biochemistry 26:7535–7541

    CAS  PubMed  Google Scholar 

  • Simatos G, Forward K, Morrow M, Keough K (1990) Interaction between perdeuterated dimyristoylphosphatidylcholine and low molecular weight pulmonary surfactant protein SP-C. Biochemistry 29:5807–5814

    CAS  PubMed  Google Scholar 

  • Stohrer J, Gröbner G, Reimer D, Weisz K, Mayer C, Kothe G (1991) Collective lipid motions in bilayer membranes studied by transverse deuteron spin relaxation. J Chem Phys 95:672–678

    Article  CAS  Google Scholar 

  • Suzuki Y, Fujita, Y, Kogishi K (1989) Reconstitution of tubular myelin from synthetic lipids and proteins associated with pig pulmonary surfactant. Am Rev Respir Dis 140:75–81

    CAS  PubMed  Google Scholar 

  • Taneva S, Keough K (1994) Pulmonary surfactant proteins SP-B and SP-C in spread monolayers at the air–water interface. I. Monolayers of pulmonary surfactant protein SP-B and phospholipids. Biophysical J 66:1137–1148

    CAS  Google Scholar 

  • Taneva S, Keough K (1995) Calcium ions and interactions of pulmonary surfactant proteins SP-B and SP-C with phospholipids in spread monolayers at the air/water interface. Biochim Biophys Acta 1236:185–195

    Article  CAS  PubMed  Google Scholar 

  • Udenfriend S, Stein S, Bohlen P, Dairman W, Loimgrukes W, Weigele M (1972) Fluorescamine: a reagent for assay of amino acids, peptides, and primary amines in the picomole range. Science 178:871–872

    CAS  PubMed  Google Scholar 

  • Veldhuizen R, Nag K, Argeig S, Possmayer F (1998) The role of lipids in pulmonary surfactant. Biochim Biophys Acta 1408:90–108

    CAS  PubMed  Google Scholar 

  • Williams M, Hawgood S, Hamilton R (1991) Changes in lipid structure produced by surfactant proteins SP-A, SP-B, and SP-C. Am J Respir Cell Mol Biol 5:41–50

    CAS  PubMed  Google Scholar 

  • Yu S, Smith N, Harding P, Possmayer F (1983) Bovine pulmonary surfactant: chemical composition and physical properties. Lipids 18:522–529

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

K.W.M.K. is Chief Scientist, Health Canada, Ottawa, Ontario, Canada. This research was supported by grants from the Natural Science and Engineering Research Council of Canada to M.R.M. and from the Canadian Institutes of Health Research to K.M.W.K. The authors are grateful to Dr. Maria Kilfoil for DPPC-d 62 data used for comparison in this work.

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Authors and Affiliations

  1. Department of Physics and Physical Oceanography, Memorial University of Newfoundland, St. John's, NF, A1B 3X7, Canada

    Michael R. Morrow & Awel Dico

  2. Department of Biochemistry, Memorial University of Newfoundland, St. John's, NF, A1B 3X9, Canada

    June Stewart & Svetla Taneva

  3. Department of Biochemistry and Discipline of Pediatrics, Memorial University of Newfoundland, St. John's, NF, A1B 3X9, Canada

    Kevin M. W. Keough

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  1. Michael R. Morrow
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  2. June Stewart
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  3. Svetla Taneva
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  4. Awel Dico
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  5. Kevin M. W. Keough
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Correspondence to Michael R. Morrow.

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Morrow, M.R., Stewart, J., Taneva, S. et al. Perturbation of DPPC bilayers by high concentrations of pulmonary surfactant protein SP-B. Eur Biophys J 33, 285–290 (2004). https://doi.org/10.1007/s00249-003-0357-0

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