A FOURIER TRANSFORM INFRARED SPECTROSCOPIC STUDY OF P2 PROTEIN IN RECONSTITUTED MYELIN.
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1 Vol. 39, No. 3, June 1996 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL Pages A FOURIER TRANSFORM INFRARED SPECTROSCOPIC STUDY OF P2 PROTEIN IN RECONSTITUTED MYELIN. B.H. Smart Department of Materials Science, University of Technology Sydney, P.O. Box 123, Broadway N.S.W. 2007, Australia. Received March 29, 1996 Summary The secondary structure of P2 protein, isolated from bovine peripheral nervous system myelin, in reconstituted myelin was studied using Fourier transform infrared (FTIR) spectroscopy. Spectra of the protein in aqueous solution and in the lipid environment were compared and notable changes were observed. It was proposed that there are significant differences in the conformation of the protein in the contrasting environments. An increase in a-helical structure was observed for the protein in myelin and the significant amount of 13-structure observed in aqueous solution was reduced. The degree of a-helix appears to be related to the neuritogenic activity of the P2 protein. The findings of this study also support the view that the presence of both et-helices and 13-structure plays a significant role in membrane proteins. Keywords: FTIR spectroscopy; P2 protein; myelin Introduction P2 protein is one of the major extrinsic proteins of the peripheral nervous system (PNS) and has been identified as a possible neuritogenic agent for the induction of experimental allergic neuritis (EAN) (1), a model for the human demyelinating disease, Guillain-Barr~ syndrome (2). There is an interest in studying the interaction of P2 with myelin as it may provide information about the role of the protein in its native environment. P2 is also believed to have a structural role in the myelin sheath. It has also been found that P2 when complexed with certain myelin lipids enhances the induction of EAN (3). The amino acid sequence of bovine P2 protein is shown in Figure 1. The conformation of P2 in aqueous solution has been studied by circular dichroism (CD) and nuclear magnetic resonance (NMR) spectroscopy (4). However, these techniques are of limited value for the investigation of P2 in the native state. P2 complexed with myelin lipids forms multilayered structures of lipid bilayers with P2 sandwiched between them (5). The large size of the multilayers slows down the tumbling rate in NMR; a rapid tumbling motion is necessary for high resolution NMR spectra. In CD, the multilayers cause excessive light scattering. However, infrared spectroscopy does not suffer from these drawbacks since it does not depend on tumbling motion and scattering is negligible. Fourier transform infrared (FTIR) spectroscopy has developed in recent years as an effective technique for the examination of membrane structure (6) /96/030629~) /0 Copyright 1996 by Academic Press Australia. All rights of reproduction in any form reserved.
2 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL AcSNKFLGTWKLVS SENFD E YMK ALGVGLATRKLGNLAKPR;qlISK KGDIITIRTESPFKNTEISFKLGQ EFEETTADNRKTKSTVTLARGSL NQVQKWNGNETTIKRKLVDGKM VVECKMKDVVCTRIYEKV Figure 1. The amino acid sequence of bovine P2 protein; letters represent the one-letter code for amino acids. FTIR spectroscopy has been used to investigate the secondary structure of bovine P2 protein in deuterium oxide 032 O) (7). The amide I band of the P2 spectrum was analysed quantitatively using resolution enhancement and band-fitting procedures. The assignment of the various components of the amide I band to particular secondary structures was based upon a study by Byler and Susi (8) of a series of well-characterised proteins in D20 solution. The protein was found to consists mainly of 13-structure (61%), with a small amount of ~x-helix (11%). In this study the conformation of P2 protein in PNS myelin is studied using FTIR spectroscopy. As it is impossible to examine the conformation of the protein in its truly native state because of the presence of other proteins, P2 was interacted with myelin with all protein removed. Methods Extraction procedures P2 protein was isolated from bovine spinal root myelin according to the method described by Stuart and McFarlane (9). Bovine spinal root tissue was obtained from the N.S.W. State Abbatoir, Australia. A feature of the composition of myelin is the high proportion of lipid to protein, with lipids constituting 70-75% of the dry weight of myelin. PNS myelin lipids were extracted from PNS myelin according to the method of Bligh and Dyer (11). The myelin was obtained from bovine spinal root tissue and homogenised in a chloroform/methanol (1:2) mixture. Water was added to the mixture to give a chloroform:methanol:water ratio of 1:2:1. The methanol/water layer was removed and the chloroform layer, containing the lipids, was dried using a rotary evaporator. Sample preparation The protein samples were deuterated by lyophilising twice from D20. The buffer used was 60 mm 2-[4-(2-hydroxyethyl)-l-piperazinyl] ethanesulphonic acid (HEPES) (Merck) in deuterium oxide 032 O, 99.96%; Aldrich) at ph 7.4. The samples were prepared in buffer at a concentration of 10 mg m1-1. Vesicles were formed by sonicating the lipids in buffer using a Bronson B-32 sonicator at a lipid concentration of 5 mg ml "1. Protein-lipid complexes were prepared by adding protein in buffer to the lipid vesicles. The mixture was vortexed immediately and shaken for two hours at room temperature. The complex was then centrifuged (10000 rev min -1, 30 rain, 4 C) in a Beckman ultracentrifuge and the supernatent was removed and analysed for unbound protein (12). The lipid-protein complex was resuspended in buffer at a lipid concentration of 100 mg ml "1. P2 protein in buffer were added to produce a composition of 17 mg protein and 100 mg lipid per ml in the final mixture. A similar procedure has been shown by Sedzik et al.(5) to produce reconstituted P2/myelin-lipid multilayers. 630
3 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL FTIR spectroscopy Spectra were recorded using a Digilab FTS-20/80 spectrometer equipped with a liquid nitrogen-cooled mercury cadmium telluride (MCT) detector. For each spectrum, 4000 interferograms were co-added, apodised with a triangular function, and Fourier transformed to give a resolution of 2 cm -1. The instrument was purged continuously with dry nitrogen in order to eliminate spectral contributions from atmospheric water vapour. Samples were contained in a demountable infrared cell with CaF 2 windows. Myelin-flee protein samples were examined with a pathlength of nun and myelin-containing samples with a pathlength of mm. The overlapping bands were resolved by Fourier self-deconvolution (13) and derivative spectroscopy (14) using standard Digilab soitware supplied with the spectrometer. The spectrum of P2 in D20 was deconvolved using a half-width Lorentzian line of 14 cm -1 and a k value of 2.0. The spectrum of P2 in myelin was deconvolved using a half-width Lorentzian line of 18 em -1 and a k value of 2.2. The derivative spectra were calculated using a power of 2 and a passband edge of 0.3. The number of component amide I bands and wavenumber of these bands were obtained from both the resulting deconvolved spectra and the second derivative of the original spectrum. To obtain the fractions of the various secondary components, a curve-fitting programme based on a Ganss-Newton least-squares minimisation procedure was used (15). Gaussian band shapes were assumed in the program and the relative areas of the component bands gave the required fractions (8). Iteration was continued to convergence at a low root mean square error (ca %). Results and Discussion The FTIR spectrum of P2 in a D20 solution was recorded. The amide I band was deconvolved and curve-fit and the results are illustrated in Figure 2. The FTIR spectrum of P2 in a D20 solution was discussed in detail by Smart and McFarlane (7) and the analysed amide I band of P2 in D20 is shown here for comparison with the P2-myelin data. Table 2 shows the wavenumber and fractional area of each component of the amide I band of P2 in D20. The FTIR spectrum of P2 protein after reconstitution in myelin was also recorded. The results of deconvolution and band-fitting the amide I band of P2 in myelin are shown in Figure 3. There are significant changes observed to the amide I band of P2 when the protein is complexed with myelin. There is a notable change in the shape of the amide I band of P2 in myelin compared to that observed in aqueous solution, and ten component bands are observed. The frequency and fractional area of each component of the amide I band of P2 in myelin is listed in Table 1. In Figure 3 the two small components at 1608 and 1618 cm -1 occur in the frequency range normally attributed to side chain contributions (18). The component at 1630 em -1 is assigned to low-frequency [5-structure (8) with a high-frequency component due to [5- structure observed at 1677 cm -1. These bands are the only components present which can be unequivocably assigned to [3-structure and contribute to 28% of the total band area. This estimation indicates a notable reduction in the amount of [5-structure when the results are compared to those obtained for P2 in D20 where 61% [5-structure is observed. The major component in Figure 3 is that at 1654 cm "1, contributing to 46% to the total amide I band area. This is assigned to or-helix in the protein (8). If this component is attributed to a-helix, 631
4 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL vvavemunber / cm -t Figure 2. Amide I band of P2 in D20 with the best-fitted individual component bands. The symbols et,13,t,r,s stand for a-helix, 13-sheet, turns and bends, random coil and side chain contributions, respectively. o ~ o m 3 I wavmlumber / cm i Figure 3. Amide I band of P2 in reconstituted myelin with the best-fitted individual component bands. Details for the spectra are given in the legend to Figure
5 BIOCHEMISTRYand MOLECULAR BIOLOGY INTERNATIONAL Table 1. Summary of the analyses of amide I bands of P2 protein before and after interaction with myelin. The wavenumber (in em -1) of each component is listed first, with relative areas in parentheses. P2/D20 P2/myelin 1623(28%) 1635(22%) 1630(24%) 1645(9%) 1642(2%) 1652(11%) 1654(46%) 1662(14%) 1670(10%) 1674(11%) 1677(4%) 1684(5 %) 1685 (10%) 1696(4%) reconstitution of P2 in myelin produces a significant increase in the amount of a-helix present in the protein in the predominantly lipid environment. The small component at 1642 cm -1 appears at a frequency normally attributed to random coil (8). The remainder of the components in Figure 3 at 1670, 1685 and 1696 cm -1 are assigned to turns in the protein. Thus, it appears that after P2 protein is reconstituted into protein-free myelin there are significant conformational changes to the protein. Notably, there appears to be the formation ofcx-helical structure at the expense of 13-structure in P2. In aqueous solution the protein has a large degree of 13-structure (61%), while only 28% 13-structure is determined for the exposed to the myelin environment. The increase in a-helix in a lipid environment supports the findings of earlier CD studies (17). Spectroscopic observations have been interpreted as indicating increases in the a-helix content of the antigenic protein, produced in particular by interaction with the lipid phosphatidylserine (PS). It is believed that increases in the content of a-helix are related to the observed enhancement of induction of EAN after complexation. The ability of P2 to induce EAN is enhanced greatly by complexing the protein with PS (3). Additionally, the association of a number of polypeptides and proteins with phospholipids have been reported to be connected with an increase in a-helical conformation. It is generally accepted that the most common protein conformation in the hydrophobic lipid environment is the a-helix (18,19), but more recent studies have indicated also the presence of 13-structure in membrane proteins (20-22). The FTIR study reported here demonstrates that both these secondary structures contribute significantly to the conformation of P2 in a lipid environment. Acknowledgements The author wishes to thank Dr Ernest McFarlane and Mrs Dallas McFarlane. The experiments reported here were carried out in the School of Chemistry, University of Sydney, Australia. 633
6 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL References 1. Brostoff, S.W., Levitt, S. and Powers, J.M. (1977) Nature 268, Ballin, 1LH.M. and Thomas, P.K. (1969) J. Neurol. Sei. 8, Eylar, E.H., Ishaque, A. and Szymanska, I. (1980) in Myelin: Chemistry and Biology (Hashim, G.A., Ed.), pp 37-53, Alan 1L Liss, New York. 4. Shin, H.C. and MeFarlane, E.F. (1987) Bioehem. Biophys. Aeta 913, Sedzik, J., Blauroek, A.E. and Hoeehli, M. (1985) J. Neurochem. 45, Jackson, M. and Mantseh, H.H. (1993) Speetroehim. Aeta 15, Smart, B.H. and McFarlane, E.F. (1991) Aust. J. Chem. 44, Byler, D.M. and Susi, H. (1986) Biopolymers 25, Stuart, B.H. and MeFarlane, E.F. (1994) Int. J. Biol. Maeromol. 16, Norton, W.T. and Crammer, W. (1984) in Myelin (Morell, P., Ed.), pp , Plenum, New York. 11. Bligh, E.G. and Dyer, W.J. (1959) Canad. J. Bioehem. Physiol. 37, Lowry, D.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) J. Biol. Chem. 193, Kauppinen, J.K., Moffat, D.J., Mantseh, H.H. and Cameron, D.G. (1981) Appl. Speetrose. 35, Susi, H. and Byler, D.M. (1983) Bioehem. Biophys. Res. Commun. 115, Fraser, 1LD.B. and Suzuki, E. (1969) Anal. Chem. 41, Chirgadze, Y.N., Fedorov, O.V. and Trushina, N.P. (1975) Biopolymers 14, Shin, H.C. (1989) Doctor of Philosophy Thesis, University of Sydney, Australia. 18. Engelman, D.M., Henderson, R., MeLaehlan, A.D. and Wallace, B.A. (1980) Proe. Natl. Aead. Sei. U.S.A. 77, Engelman, D.M. and Steitz, T.A. (1981) Cell 23, Tobkes, N., Wallace, B.A. and Bayley, H.(1985) Biochemistry 24, Lee, D.C., Hayward, J.A., Restall, C.J. and Chapman, D. (1985) Biochemistry 24, Surewiez, W.K., Mosearello, M.A. and Mantseh, H.H. (1987) J. Biol. Chem. 262,
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