In Situ Investigation of Peptide–Lipid Interaction BetweenKhoi Tan Nguyen1,2 Received: 14 September 2015 / Accepted: 6 February 2016 Springer Science+Business Media New York 2016 Abstra
Trang 1In Situ Investigation of Peptide–Lipid Interaction Between
Khoi Tan Nguyen1,2
Received: 14 September 2015 / Accepted: 6 February 2016
Springer Science+Business Media New York 2016
Abstract Sum frequency generation vibrational
spec-troscopy (SFG) was utilized to investigate the interaction
between PAP248–286and the two lipid bilayer systems The
present study also provides spectroscopic evidence to
confirm that, although PAP248–286 is unable to penetrate
into the hydrophobic core of the lipid bilayers, it is capable
of interacting more intimately with the fluid-phase POPG/
POPC than with the gel-phase DPPG/DPPC lipid bilayer
The helical structure content of lipid-bound PAP248–286
was also observed to be high, in contrast to the results
previously reported using nuclear magnetic resonance
(NMR) Collectively, our SFG data suggest that
lipid-bound PAP248–286actually resembles its structure in 50 %
2,2,2-trifluoroethanol better than the structure when the
peptide binds to SDS micelles This present study questions
the use of SDS micelles as the model membrane for NMR
studies of PAP248–286due to its protein denaturing activity
Keywords Gel-phase and fluid-phase model lipid
bilayers PAP248–286 Peptide conformation SDS
micelles
Introduction The entry of the human immunodeficiency virus (HIV) into the host cell is believed to be increased 4–5 orders of magnitude by amyloid fibrils contained in semen, specifically, semen-derived enhancer of viral infection (SEVI) (Munch et al 2007; Rusert et al 2004) These amyloid fibrils allow HIV, which would normally be considered a weak pathogen, to easily enter the host cells and hence facilitate the AIDS pandemic that has killed 40 million people since it was first clinically observed in
1981 It has recently been found that SEVI fibrils form by self-assembly of the peptide PAP248–286, a proteolytic cleavage product of prostatic acid phosphate protein abundantly found in semen.(Arnold et al 2012; Munch
et al 2007; Roan et al 2011) To shed light on the mechanism of this viral entry enhancement of these amyloid fibrils, an extensive amount of research has been done using nuclear magnetic resonance, circular dichro-ism, differential scanning calorimetry and transmission electron microscopy (Brender et al 2009, Brender et al
2011; Easterhoff et al 2011; Nanga et al 2009; Olsen
et al 2012) However, the mechanism of the fibril for-mation remains poorly understood due to its inherited structural complexity as well as the hard to achieve physiological conditions of the phenomenon
In the current study, sum frequency generation vibra-tional spectroscopy (SFG) was used to investigate the interaction between PAP248–286and model cell membranes
at very low peptide concentrations within the range of 0.2–1.0 lM As an intrinsically surface sensitive technique with superior sensitivity, SFG has been utilized extensively
in studies of protein–lipid interactions in the last decade (Mauri et al.2014; Nguyen2015; Volkov and Bonn2013; Weidnerw and Castner 2013; Yan et al 2014; Ye et al
Electronic supplementary material The online version of this
article (doi: 10.1007/s00232-016-9878-1 ) contains supplementary
material, which is available to authorized users.
& Khoi Tan Nguyen
k.nguyen9@uq.edu.au
1 School of Chemical Engineering, The University of
Queensland, Brisbane, QLD 4072, Australia
2 School of Biotechnology, International University, Vietnam
National University, Ho Chi Minh City, Vietnam
DOI 10.1007/s00232-016-9878-1
Trang 22014; Zhang et al 2014) It has been generally known
that PAP248–286is not toxic to the cell due to its inability
to penetrate into the hydrophobic core of the lipid The
molecular conformation of PAP248–286(in 50 % TFE as
well as the SDS micelle-bound form) has been solved by
solution state NMR (Brender et al 2011; Nanga et al
2009) The helical content of PAP248–286 in 50 % TFE
was observed to be 57 %, significantly higher than its
SDS-bound form (30 %) (Brender et al 2009) In both
environments, the helical content of PAP248–286is
divi-ded into two helical segments which are almost
perpen-dicular to each other in the case of 50 % TFE (Fig.1,
PDB 2L77) In addition, the 3-10 helical component
which was suggested to play a role in the fibril formation
of the peptide (Nanga et al.2009) does not seem to exist
in the NMR structure of the peptide We believe that the
discrepancies between the structural properties proposed
by these NMR measurements originate from the possible
protein denaturing activity of SDS (Seddon et al 2004;
Warschawski et al 2011), making this surfactant an
inappropriate model membrane system at least for studies
of interactions between cell membranes and PAP248–286
While SDS micelles have been reported to be an
excel-lent model membrane system for studies of robust
transmembrane peptides/proteins (Tulumello and Deber
2009), it has been reported to denature some membrane
proteins/peptides, especially when these structures do not
penetrate into the hydrophobic core of the micelles
(Seddon et al.2004; Warschawski et al 2011) Because
the amyloidogenic activity of peptides is directly dictated
by their interactions with the surrounding media, it is
important to choose a model membrane system for
studies of PAP248–286 that does not alter the structural
property of the peptide To overcome the possibility of
protein denaturation by SDS surfactant, phospholipid
mixtures were used to make lipid bilayers mimicking
model membranes in our study
Experimental Section Materials
The PAP248–286peptide ([95 % purity) was purchased from Biomatik (Toronto, ON) Phospholipids POPC (1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine), POPG (1-palmi-toyl-2-sn-glycero-3-phospho-(10-rac-glycerol)), hydro-genated and deuterated DPPG/DPPC (1,2-dipalmitoyl (D62)-sn-glycero-3-phospho-glycerol/choline) were pur-chased from Avanti Polar Lipids Inc (Alabaster, AL) Freshly purified water (Ultrapure Milli-Q unit from Mil-lipore, USA) with a resistivity of 18.2 MX cm was used to make all the solutions in the experiments These lipid species chosen in our study have been commonly used in studies of the interactions between the lipid and peptides/ proteins Deposition of the lipid bilayers on to CaF2prisms were prepared by sequentially depositing the distal and proximal layers using a 622 Nima LB trough (Chen et al
2007) In brief, the CaF2prism was immersed in the water trough; then a lipid monolayer at 34 mN/m surface pres-sure was spread on the water surface This surface prespres-sure was maintained, while the prism was being lifted out of the subphase at the rate of 1 mm/min The second lipid leaflet deposition was made by bringing the first deposited lipid layer into contact with a lipid monolayer at 34 mN/m surface pressure Once the lipid bilayer was formed, it was kept hydrated until the completion of the experiment The protein reservoir with a volume of 4 ml was placed below the lipid bilayer deposited CaF2prisms during the SFG measurement The peptide solution was stirred by a mag-netic micro-stirrer at a rate of 40 rpm during the peptide– lipid interaction The pH of the bulk was stabilized with
20 mM phosphate buffer saline (PBS) at 7.2 containing
20 mM NaCl All experiments were carried out at room temperature (*23C) The SFG spectra in the amide I frequency region were collected from the lipid-bound
Dynamic α/3-10helix
Fig 1 Two structures of
PAP248–286in SDS micelles
(PDB = 2L3H, right) and 50 %
TFE (PDB = 2L77, left)
Trang 3PAP248–286after the peptide solution had been in contact
with the lipid bilayers for at least 1 h (to equilibrate and
ensure that no further time-dependent changes occurred)
SFG Setup
In the SFG experiments, the visible and the tunable IR
beams were spatially and temporally overlapped on the
solution interface The visible beam was generated by
frequency-doubling the fundamental output pulses
(1064 nm, 10 Hz) of 36 ps pulse-width from an EKSPLA
solid state Nd:YAG laser (PL2241) The tunable IR beam
was generated by an EKSPLA optical parametric
genera-tion/amplification and difference frequency system based
on LBO and AgGaS2 crystals Fluctuations in the beam
energies were only 3 % standard deviation in the tunable
IR beam and 1.5 % in the visible beam In the current SFG
measurements, the incident angle for visible beam was
avis= 60 and for the IR beam it was aIR = 54 The
near-total-internal reflection experimental geometry was
adop-ted to collect the SFG signals from interfacial PAP248–286
using a right angle CaF2prism as the solid substrate In this
study, each presented data point was averaged over 100
acquisitions
The quantities vð2Þssp (s polarized SFG, s polarized visible
and p polarized infrared polarization combination) and vð2Þppp
(p polarized SFG, p polarized visible and p polarized
infrared polarization combination) reflect the observed
SFG intensities in the laboratory frame They are related to
vð2Þyyz and vð2Þzzz as follows:
vð2Þssp¼ LyyðxÞLyyðx1ÞLzzðx2Þ sin b2vð2Þyyz ð1Þ
vð2Þppp¼
LxxðxÞLxxðx1ÞLzzðx2Þ cos b cos b1sin b2vð2Þxxz
LxxðxÞLzzðx1ÞLxxðx2Þ cos b sin b1cos b2vð2Þxzx
þLzzðxÞLxxðx1ÞLxxðx2Þ sin b cos b1cos b2vð2Þzxx
þLzzðxÞLzzðx1ÞLzzðx2Þ sin b sin b1sin b2vð2Þzzz
ð2Þ where LiiðxÞ is a Fresnel coefficient corrected for local
fields; and b, b1and b2are the angles of the signal, visible
and IR beams with respect to the surface normal,
respec-tively For a C3v symmetry point group on an isotropic
surface, vð2Þxzx¼ vð2Þzxx The Fresnel coefficient LxxðxÞ can be
calculated as follows:
Lxx¼ 2n1cosðhtÞ
where aiand htare the incident and the transmitted angles
of the optical beam, respectively Because the
near-total-internal reflection geometry was used in this study, the
quantity LxxðxÞ in (3) will be close to zero since the angle
of the transmitted beam, ht; will approach 90 We thus have
vð2Þppp¼ LzzðxÞLzzðx1ÞLzzðx2Þ sin b sin b1sin b2vð2Þzzz ð4Þ The SFG signals are deconvoluted using the Lorentzian line shape function described as follows:
vð2Þeff ¼ vð2Þnr þX
q
Aq
xIR xqþ iCq
ð5Þ
where vð2Þnr is the nonresonating contribution; Aq is the amplitude of the vibrational mode q; xIR and xq are the input IR and the resonance IR of the vibrational q mode frequencies, respectively; and C denotes the damping coefficient of the SFG peak
Results and Discussions Interaction Between PAP248–286and 3:7 DPPG/ DPPC Lipid Bilayers
The interactions between PAP248–286 and DPPG:DPPC (3:7) lipid bilayers were studied at two peptide concen-trations of 200 nM and 1.0 lM This 3:7 lipid ratio is commonly used to simulate a mixed anionic/zwitterionic membrane system It is worth noting that both DPPC and DPPG are in the gel phase at 23C, which allows for the SFG spectral specificity of the distal and proximal leaflets using isotope labelling as previously demonstrated by Chen
et al (2007) In particular, deuterated 3:7 dDPPG/dDPPC was deposited on to the CaF2prism as the distal leaflet, and protonated 3:7 DPPG/DPPC was then deposited as the proximal leaflet.dDPPC and DPPC were used to reduce the density of negative charges in the lipid bilayer thus less-ening the electrostatic interaction between the model membrane and PAP248–286 Despite this lessening of elec-trostatic interaction, PAP248–286was bound strongly to the lipid bilayer, demonstrated by the strong SFG amide I band
at both peptide concentrations of 200 nM and 1.0 lM (Fig.2)
To verify that the interaction between PAP248–286 and DPPG/DPPC lipid bilayer was electrostatically driven, a pure DPPC lipid bilayer was used in place of the 3:7 DPPG/DPPC mixture Results showed that no discernible SFG amide I band was observed (Fig S1, ESI) in the absence of the electrostatic lipid–peptide attraction Despite its strong binding to the membrane, PAP248–286 did not exhibit any ability to penetrate the 3:7 DPPG/DPPC bilayer as demonstrated in Fig.3 Upon time-dependent translocation calibration, the SFG signals of the terminal methyl C–H and C–D stretches suggest that the 3:7 DPPG/
Trang 4DPPC remained almost unchanged upon the binding of
PAP248–286 (Fig.3) The minor spectral differences
observed in Fig.3were most likely due to the minor stress
caused by PAP248–286 when it was bound to the lipid bilayer Given the fact that PAP248–286is nondisruptive to the 3:7 DPPG/DPPC bilayer, the main helical segment (G261–I277) should adopt a more or less horizontal ori-entation at the lipid surface and the observed SFG amide I band should be contributed by the more vertically oriented helical segment K251–G260 This vertically oriented helical segment may play an important role in promoting the bridging interactions between membranes due to its positive charges Since horizontally oriented helical seg-ments were calculated to produce weaker SFG amide I band in both ppp and ssp polarization combinations (Nguyen et al 2009; Wang et al 2008), the strong SFG amide I signals (as compared to that of transmembrane peptide magainin II in POPG/POPC lipid bilayer, Fig S2, ESI) suggest a high helical content of lipid-bound PAP248–286, which is contradictory to the previously reported low value of 30 % suggested by Brender et al using circular dichroism However, the authors concluded that this low value of 30 % was probably an underestimate caused by the visible aggregation of the lipid vesicles (Brender et al 2009) We thus believe that SDS-bound PAP248–286was denatured by the anionic surfactant SDS as commonly reported in the community (Seddon et al.2004; Warschawski et al.2011) It is worth noting that SDS is a charged soluble detergent which interacts with both the polar and nonpolar regimes of the peptides/proteins Beyond its critical micellar concentration of around 7–8 mM, there coexist both SDS micelles and molecular SDS molecules in the bulk medium, which will at some degree affect the folding of the proteins/peptides in the solution
Interaction Between PAP248–286and 3:7 POPG/ POPC Lipid Bilayers
Since both DPPC and DPPG are in gel phase under the current experimental conditions (at room temperature), another set of experiments in which PAP248–286 interacts with lipid bilayers in fluid phase is desirable The 3:7 POPG/POPC bilayer system was chosen for the current study because its electrostatic attraction to PAP248–286 should be similar to that of 3:7 DPPG/DPPC presented in the previous section (Haro et al.2003) With this system, it
is impossible to spectrally distinguish the distal and prox-imal leaflets by the method of isotope labelling of the fluid-phase lipid bilayers The flip-flopping rate of fluid-fluid-phase lipid bilayers is so rapid [t1/2 can be as low as 1.3 min at room temperature (Liu and Conboy 2005)], which almost instantly causes the lipid bilayer to become entirely sym-metric, leading to no spectral features being observable by SFG However, being a symmetry-sensitive technique, SFG can probe the symmetry deviation of interfaces SFG
0.00
0.10
0.20
0.30
wavenumber (cm -1 )
200 nM ssp
200 nM ppp
0.00
0.10
0.20
0.30
wavenumber (cm -1 )
1 μM ssp
1 μM ppp
Fig 2 SFG amide I band of 3:7 DPPG/DPPC lipid-bound PAP248–286
at peptide concentration of 200 nM (top) and 1 lM (bottom) in ssp
and ppp polarization combinations
0.00
0.02
0.04
0.06
0.08
0.10
2800 2850 2900 2950 3000
wavenumber (cm -1 )
before PAP248-286 aer 1 μM PAP248-286
CH 3 sym
CH 3 FR
CH 3 asym
0.00
0.01
0.02
0.03
0.04
0.05
wavenumber (cm -1 )
before PAP248-286 aer 1 μM PAP248-286
CD 3 sym
CD 3 asym
CD 2 asym CD 3 FR
(a)
(b)
Fig 3 ssp SFG signals of the proximal (a) and distal (b) lipid leaflets
before and after peptide interaction
Trang 5data reveal that the fluid-phase 3:7 POPG/POPC lipid
bilayer exhibits a noticeable decrease in the degree of
symmetry upon interacting with PAP248–286, demonstrated
by the vibrational modes of the terminal methyl groups
starting to appear with the presence of the peptide (Fig.4)
This observation can be simply explained by the stresses
stemming from the lipid headgroup–PAP248–286binding
It is noted in Fig.4that the baseline of the SFG signal in
the 2800–3000 cm-1range of the 3:7 POPG/POPC bilayer
became weaker after the peptide interaction, which is due
in part to the peptide binding that reduces the number of
interfacial water molecules On the other hand, it is also
possible that the charge neutralization by the peptide
binding dictates the interfacial water orientation and leads
to the reduction in the SFG signal baseline (Fig S3, ESI) (Ding et al 2013) Further information about the binding behaviour of PAP248–286to POPG/POPC can be derived by analysing the SFG amide I band of the interfacial peptide molecules Interestingly, both the ssp and ppp SFG amide I signal intensities obtained were similar as occurred when 3:7 DPPG/DPPC was used at peptide concentrations of
200 nM and 1.0 lM PAP248–286 (Fig.5), indicative of a similar nondisruptive binding mode of PAP248–286 stem-ming from its low hydrophobicity and high positive net charge (?10)
Despite the above similarity in the PAP248–286 SFG amide I signal intensities, there were some minor spectral shifts observed that indicate secondary structure content shifts of PAP248–286upon interacting with the lipids High-resolution technique NMR suggested that PAP248–286 consists of mainly helical (a- or 310-) and random coil structures (PDB codes 2L77 and 2L3H, respectively Fig-ure1) (Nanga et al.2009) The structure of PAP248–286 in TFE suggested by Ayyalusamy et al (PDB code 2L77) contains significantly more helical content than when the peptide binds to SDS micelles (2L3H) In the current SFG measurements, since SFG is insensitive to unordered structures, random coil components would not make a substantial contribution to the strong amide I band shown
0.00
0.10
0.20
0.30
0.40
2800 2850 2900 2950 3000
wavenumber (cm -1 )
before PAP248-286 aer 1 μM PAP248-286
Fig 4 3:7 POPG/POPC lipid bilayer before and after interacting with
PAP248–286
0.00
0.10
0.20
0.30
wavenumber (cm -1 )
200 nM ppp
200 nM ssp
0.00
0.10
0.20
0.30
wavenumber (cm -1 )
1 μM ssp
1 μM ppp
Fig 5 SFG amide I band of 3:7 DPPG/DPPC lipid-bound PAP248–286
at peptide concentration of 200 nM (top) and 1 lM (bottom) in ssp
and ppp polarization combinations
0.00 0.10 0.20 0.30
wavenumber (cm -1 )
data fit
1605 cm-1
1630 cm-1
1650 cm-1
1685 cm-1
0.00 0.10 0.20 0.30
wavenumber (cm -1 )
data fit
1605 cm-1
1630 cm-1
1650 cm-1
1685 cm-1
(a)
(b)
Fig 6 ppp SFG amide I band fitting of lipid-bound PAP248–286 at peptide concentration of 1 lM: a with 3:7 DPPG/DPPC and b with 3:7 POPG/POPC The insets are the zoom-ins to show the smaller contribution peaks
Trang 6in Figs.2 and 5, as has previously been computationally
(by NLOPredict) and experimentally (by SFG)
demon-strated (Ding et al.2013; Nguyen et al.2010b; Wang et al
2008) Besides, random coil structure should give rise to
rather broad amide I bands (if observable) due to
unpre-dicted coupling among the backbone C=O units (Fu et al
2011) In this study, the strong SFG amide I bands of
PAP248–286possess well-defined spectral shape that can be
fit nicely using three or four component peaks as shown in
Fig.6and Table1 For these two main reasons, it is safe to
assume that the SFG amide I contribution of the random
structures of PAP248–286 was negligible in the illustrated
spectra
Although the amide I band of 3:7 POPG/POPC-bound
PAP248–286was well fit using three peaks featuring the
a-helical and b-sheet structures, we could not detect the
chiral SFG signal in either psp or spp polarization
combi-nation (Fig S1, ESI) Furthermore, our attempt to use the
interference method (Belkin et al 2000; Nguyen et al
their interference with the achiral components failed to
detect any chiral signal from the lipid-bound PAP248–286
Our inability to probe any chiral signal can be explained
either by the non-existence of the b-sheet structure or by
the b-sheet content being insufficient to produce any
detectable SFG chiral signal We believe the latter
expla-nation is more sensible because a small b-sheet
confor-mation does exist in the structure of PAP248–286 (residues
L283–Y286) and the two minor peaks used to fit the achiral
spectrum (Fig.6b; Table1) closely match the assignments
of the B2 and B1 vibrational modes previously reported
(Baio et al.2013; Nguyen et al.2010a)
Whilst the existence of a small and transient/dynamic
310-helical segment at the C terminus has been proposed in
an NMR study on SDS-bound PAP248–286 (Brender et al
2009), there was no 310-helical SFG signal detected in our
study The small peak at 1630 cm-1 could not have been
contributed by the 310-helical structure because this
struc-ture would also give rise to a peak at 1670 cm-1 when
coupled with the a-helical structures (Ye et al.2012,2010)
It is noted that the 310-helix was not observed in the
structure of PAP248–286, either (PDB code 2L77)
Since PAP248–286 does not penetrate into the hydrophobic core of lipid bilayers, its molecular orientation
at the lipid interface can be reasonably assumed to be independent of the phase of the lipid bilayers The higher SFG signal amplitudes of the 1630 and 1685 cm-1 peaks observed when PAP248–286 binds to fluid-phase lipids can
be attributed to the slight peptide conformational/orienta-tional alteration induced by the more intimate binding PAP248–286 causes to the lipid This peptide conforma-tional/orientational alteration demonstrates that the con-formational preferences of the monomeric PAP248–286 are rather sensitive to the peptide/lipid interaction, which may provide important insights into the aggregation pathways and the formation of the eventual amyloid fibre
Conclusion This study used sum frequency generation vibrational spectroscopy (SFG) to show that the molecular structure of the lipid-bound PAP248–286 may vary with the phase of lipid bilayer system Furthermore, PAP248–286 was observed to interact more intimately with the 3:7 POPG/ POPC lipid bilayer than with its gel-phase counterpart, causing the lipid bilayer to become asymmetric The dis-crepancies between our results and NMR measurements on SDS-bound PAP248–286might be due to the choice of 3:7 POPG/POPC lipid bilayer versus SDS micelles used to mimic the cell membranes, which brings into question whether SDS micelles are a good system for such studies The current study also suggests a potentially higher helical content of lipid-bound PAP248–286than the 30 % calculated using circular dichroism In addition, this study demon-strates the importance of the choice of lipid–bilayer system when conducting studies on the aggregation pathways and amyloid fibre formation of the SEVI precursor peptide PAP248–286
Acknowledgments This research is funded by the Vietnam National Foundation for Science and Technology Development (NAFOSTED) under Grant Number 106.16-2012.67 The author sincerely thanks Dr Gay Marsden for her generous assistance in the manuscript preparation.
Table 1 ppp SFG amide I band fitted amplitude/damping coefficient ratio (A/C) of PAP248–286peptide interacting with 3:7 DPPG/DPPC and 3:7 POPG/POPC
Secondary structure Peak centre (cm-1) 3:7 DPPG/DPPC A/C 3:7 POPG/POPC A/C
Trang 7Compliance with Ethical Standards
Conflict of interest The authors declare no competing financial
interests.
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