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Label-Free and Charge-Sensitive Dynamic Imaging of Lipid Membrane Hydration on Millisecond Time Scales

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Label-Free and Charge-Sensitive Dynamic Imaging of Lipid Membrane Hydration on Millisecond Time Scales Label-free and charge-sensitive dynamic imaging of lipid membrane hydration on millisecond time scales Orly B. Taruna,b,c, Christof Hannesschlägerd, Peter Pohld, and Sylvie Rokea,b,c,1 aLaboratory for Fundamental BioPhotonics, Institute of Bioengineering, School of Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland; bInstitute of Materials Science, School of Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland; cLausanne Centre for Ultrafast Science, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland; and dInstitute of Biophysics, Johannes Kepler University Linz, A-4020 Linz, Austria Edited by F. Fleming Crim, University of Wisconsin−Madison, Madison, WI, and approved March 1, 2018 (received for review November 7, 2017) Biological membranes are highly dynamic and complex lipid also employed in methods such as interferometric scattering mi- bilayers, responsible for the fate of living cells. To achieve this croscopy (13), ellipsometry (14), and atomic force microscopy (15, function, the hydrating environment is crucial. However, mem- 16). Second-harmonic (SH) and sum frequency (SF) generation brane imaging typically neglects water, focusing on the insertion have been recognized as powerful probes of membrane function: of probes, resonant responses of lipids, or the hydrophobic core. The intrinsic symmetry selection rule that applies to both methods Owing to a recent improvement of second-harmonic (SH) imaging ensures that centrosymmetric structures such as ideal single- throughput by three orders of magnitude, we show here that we component lipid bilayers do not emit SH or SF photons. With can use SH microscopy to follow membrane hydration of free- this in mind, the vibrational response of lipids in supported lipid standing lipid bilayers on millisecond time scales. Instead of using membranes was used to spectroscopically probe transmembrane the UV/VIS resonant response of specific membrane-inserted fluo- lipid motion (17) and lipid acyl chain conformation in monolayers rophores to record static SH images over time scales of >1,000 s, we on air/water interfaces (18). SH imaging studies have been per- SH imaged symmetric and asymmetric lipid membranes, while vary- formed on lipid bilayers deposited on a substrate in which the UV ing the ionic strength and pH of the adjacent solutions. We show resonance of specific drugs or chiral molecules was employed to that the nonresonant SH response of water molecules aligned by record static structural maps (19, 20). Another study employed − charge dipole interactions with charged lipids can be used as a static SH imaging to confirm single-component membrane sym- label-free probe of membrane structure and dynamics. Lipid domain metry and relate it to the stability of black lipid membranes diffusion is imaged label-free by means of the hydration of charged formed with different substrates (21). Due to the weak nonlinear domains. The orientational ordering of water is used to construct optical response in these experiments, recording times are more electrostatic membrane potential maps. The average membrane po- than 20 min per image. Since structural changes occur on much tential depends quadratically on an applied external bias, which is shorter time scales, no dynamic information has been obtained. modeled by nonlinear optical theory. Spatiotemporal fluctuations The above methods have greatly advanced membrane re- on the order of 100-mV changes in the membrane potential are search, but have so far ignored the hydrating water, without seen. These changes imply that membranes are very dynamic, not which membranes cannot exist (22, 23). Recently, we demon- only in their structure but also in their membrane potential land- strated high-throughput wide-field SH imaging (24, 25) where we scape. This may have important consequences for membrane func- tion, mechanical stability, and protein/pore distributions. Significance water | membranes | second-harmonic imaging | lipids | surface potential Lipid bilayer membranes are responsible for compartmentali- he properties of membranes around cells and organelles are zation, signaling, transport, and flow of charge in living cells. Tcritically determined by the structural and dynamical proper- Membranes self-assemble in aqueous solutions. Without a ties of lipid membranes (1, 2). The distribution of charge, chemical hydrating environment, membranes cannot exist. It is there- composition, and presence or absence of domains at membranes fore surprising to note that the hydrating water is neglected in determine the traffic in and out of cells, the structural integrity, most membrane-related studies. We imaged membrane-bound oriented water by means of label-free second harmonic mi- and the response of cells to their environment, even leading to cell CHEMISTRY croscopy. We tracked, on millisecond time scales, membrane death (3). In addition, the hydration of lipid membranes is key to domain diffusion of condensed charged lipid domains, domain their structural integrity: Without water, lipids will not self- structure, and the spatial distribution of charge. Real-time assemble into a membrane structure or remain stable. Imaging electrostatic membrane potential maps were constructed us- membrane hydration, the dynamics of charge, lipid domain for- ing nonlinear optical theory. The spatiotemporal fluctuation in mation, and diffusion is a formidable challenge relevant for un- the membrane potential is surprisingly large and reveals the derstanding membrane properties and utilizing them for treating importance of charge fluctuations on membranes. related diseases, such as neurodegenerative disorders (4). Owing to the importance of membranes, a wide variety of imaging Author contributions: O.B.T., P.P., and S.R. designed research; O.B.T. and C.H. performed BIOPHYSICS AND methods are used that are either geared toward measuring the fate research; O.B.T., C.H., P.P., and S.R. analyzed data; and O.B.T. and S.R. wrote the paper. COMPUTATIONAL BIOLOGY of membrane-inserted probes and their relation with the mem- The authors declare no conflict of interest. brane, such as confocal fluorescence microscopy (5, 6), stimulated This article is a PNAS Direct Submission. emission depletion far-field fluorescence nanoscopy (7), and This open access article is distributed under Creative Commons Attribution-NonCommercial- superresolution fluorescence imaging (8), or to probe the resonant NoDerivatives License 4.0 (CC BY-NC-ND). response, using coherent anti-Stokes Raman scattering micros- 1To whom correspondence should be addressed. Email: [email protected]. copy (9–11), or stimulated Raman scattering microscopy (12). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Refractive index contrast or the height difference of the hydro- 1073/pnas.1719347115/-/DCSupplemental. phobic core of the membrane that are substrate-dependent are Published online April 2, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1719347115 PNAS | April 17, 2018 | vol. 115 | no. 16 | 4081–4086 Downloaded by guest on September 28, 2021 improved the throughput of an SH microscope by a factor of microscopy. Finally, we use the second-order optical response of ∼5,000 compared with a confocal scanning microscope (25), water to measure the membrane potential and changes therein enabling the measurement of interfacial water that was oriented as a function of an external bias. While the average potential by the presence of surface charges inside a glass microcapillary. follows the quadratic dependence on an external bias, extract- If high-throughput wide-field SH imaging were to be applied to able from nonlinear optical theory, individual images show dy- lipid membrane research, it would be possible to image the namic spatiotemporal fluctuations on the order of 100 mV. molecular structure of membrane-interacting water that is in- terrelated with hydration, the presence of local charges, ioniza- Results and Discussion tion states, and membrane potentials. Such information, if SH Imaging of Membrane Hydration. Freestanding horizontal pla- obtained on a subsecond time scale, would provide a new nar lipid bilayers are formed in an aperture of a thin Teflon film pathway to image the dynamic molecular response of mem- by the apposition of lipid monolayers formed on two different branes and relate molecular structure to macroscopic function. air/water interfaces (20, 26, 27). The presence of a bilayer inside Here, we show that wide-field high-throughput SH imaging a ∼80- to 120-μm-sized circular aperture in a 25-μm-thick Teflon can indeed be used to label-free image the water molecules in film is confirmed with white-light imaging and electrical re- the hydration shells of charged membranes. As hydrating water cordings (Fig. 1A and Fig. S2). The appearance of Newton dif- molecules are oriented by the ionic groups in the lipid head fraction rings and the measured specific capacitance (Cm) and 2 groups of charged lipids through charge−dipole interactions, specific resistance (Rm) of the membrane (Cm > 0.7 μF/cm ,Rm ≈ they can emit SH photons. We use a series of experiments based 108 Ω·cm2,Fig.1A) agree well with literature values (26, 27). on changing the membrane composition, changing the ionic Compositional transleaflet asymmetry is confirmed by capacitance content of the aqueous phase adjacent to both membrane leaf- minimization measurements (28, 29) that are sensitive to differ- lets, and the pH
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