Abstract
Dynamic characterizations of intracellular variations and cell-substrate interactions under different external environments are critical to study cell behaviors and exploring biological applications. However, techniques that are capable of dynamically and simultaneously measuring multiple parameters of living cells in a wide-field manner have rarely been reported. Here, we present a wavelength-multiplexing surface plasmon resonance holographic microscopy which allows wide-field, simultaneous, and dynamic measurements of cell parameters, including cell-substrate distance and cytoplasm refractive index (RI). We use two lasers of 632.8 nm and 690 nm as light sources. Two beam splitters are employed in the optical setup to separately adjust the incident angle of two light beams. Then, surface plasmon resonance (SPR) can be excited for each wavelength under SPR angles. We demonstrate the advances of the proposed apparatus by systematically studying the cell responses to osmotic pressure stimuli from the environmental medium at the cell-substrate interface. The SPR phase distributions of the cell are firstly mapped at two wavelengths, then the cell-substrate distance and cytoplasm RI are retrieved using a demodulation method. Based on phase response differences between two wavelengths and monotonic changes of SPR phase with cell parameters, cell-substrate distance, and cytoplasm RI can be determined simultaneously using an inverse algorithm. This work affords a new optical measurement technique to dynamically characterize cell evolutions and investigate cell properties in various cellular activities. It may become a useful tool in the bio-medical and bio-monitoring areas.
© 2023 Optica Publishing Group under the terms of the Optica Open Access Publishing Agreement
1. Introduction
Cell activities at the bio-interface including adhesion, movement, replication, apoptosis, etc. play an essential role in the development and maintenance of tissue, organs and biological bodies [1–4]. Therefore, measuring cell-substrate interactions and intracellular variations to environmental factors is of great importance in the biological field [5]. A technique that can quantitatively characterize cell evolutions in a dynamic manner is highly desired.
Surface plasmon resonance (SPR), also known as collective oscillations of free electrons on metal surface (i.e., surface plasmon polaritons, SPPs), can be excited by light wave at metal-dielectric interface [6]. The wavevector of the SPPs kspp is calculated by
Taking advantages of high sensitivity from SPR-based techniques and complex amplitude measurement by digital holographic microscopy (DHM), surface plasmon resonance holographic microscopy (SPRHM) has become an emerging technique in the last decade which can reconstruct both the amplitude- and phase-based SPR images at the same time [21–28]. In the biological application field, SPRHM was used to map the cell adhesion gap and its evolution during cell activities [26]. Combined with optical tweezers (OT), OT-SPRHM system was proposed to characterize cell-substrate interactions when cell individuals were stimulated with optical force [27]. Recently, a dual-wavelength SPRHM was reported to simultaneously measure cell-substrate distance and cytoplasm RI of living cells [28]. However, in that work, incident angle of light beam at two wavelengths is adjusted sequentially to excite SPR, making dynamic monitoring of cell parameters hard to realize.
In this work, we propose a wavelength-multiplexing SPRHM to dynamically monitor cell-substrate distance and cytoplasm RI evolutions at the same time. Two beam splitters are employed to tune the incident angle of lasers at wavelengths of 632.8 nm and 690 nm to excite SPR. Then, phase-contrast SPR images of living cells are reconstructed by double-exposure DHM. The cell-substrate distance and cytoplasm RI are demodulated from reflection phase shift difference of the two wavelengths. Using the proposed technique, we carry out a series of measurements of cell parameters when osmotic pressure of extracellular environment is changed from isotonic, hypertonic to hypotonic conditions. The time traces of cell-substrate distance and cytoplasm RI in these processes clearly reveal cellular states under different external stimulations, which could provide useful information of cell properties for biological studies. Compared to previous work which also measured the cell-substrate distance and cytoplasm RI using scanning surface plasmon resonance microscopy [29], our method can realize higher temporal resolution, which is very useful for detections of ultrafast biological processes thanks to the wide-field detection capabilities. The proposed wavelength-multiplexing SPRHM is a promising tool to quantitatively detect living-cell with high throughput in a non-invasion fashion, and can be useful in various biological applications.
2. Materials and methods
2.1 Materials
The isotonic fluid is Dulbecco’s modified eagle medium (DMEM), which is supplemented with high glucose medium (gibco) contained 4.5 g/L D-Glucose, L-Glutamine and 110 mg/L Sodium Pyruvate. We prepared the hypertonic medium by adding a certain amount of sorbitol to DMEM. The hypotonic medium was made by diluting DMEM with deionized water.
2.2 Establishment of the SPR model
Based on the cell components, a six-layer SPR model consisting of the coverslip, Cr layer (adhesion layer), gold layer, culture medium, membrane and cytoplasm is built [26]. The phase interrogation of reflection light wave was employed to measure SPR signals. The reflection coefficient of reflection light wave in the six-layer SPR model r1,6 can be calculated by the Fresnel formulas, which are expressed as
To eliminate the environmental disturbances, a background hologram is recorded. Then, the reflection phase shift difference Δφ is calculated by subtracting the reflection phase shift with pure background from that with the cell specimen. Practically, we can obtain the reflection phase shift difference in SPR from phase difference of the object wave (i.e., the reflected light wave), which is reconstructed with the numerical reconstruction algorithm in DHM [24]. Four-layer SPR model (coverslip-Cr layer-gold layer-culture medium) is used when there is no cell specimen in order to record the background. The parameters of the six-layer SPR model are shown in Table 1. The dispersion is considered between the wavelengths of 632.8 nm and 690 nm [28].
We determined the cell-substrate distance and cytoplasm RI using a demodulation method (Supplement 1). Briefly, given a specific phase value for one wavelength, one can obtain a monotonical curve of cell-substrate distance versus cytoplasm RI. Then, two curves can be obtained from two wavelengths (632.8 nm and 690 nm). Since the phase responses for two wavelengths are different, there will be an intersection point from the two curves. The cell-substrate distance and cytoplasm RI can then be extracted from this intersection point. It should be note that the penetration depths for 632.8 nm and 690 nm are ∼170 nm and ∼220 nm, respectively [19]. Considering the thickness of the cell cytoplasm layer is at the scale of several micrometers, the difference of the penetration depth between two wavelengths is quite small. Moreover, since the penetration depth of evanescent wave only covers a very thin slice of the cell near the cell bottom membrane, we assume that the cytoplasm RI is homogeneous along the z direction of the evanescent wave area (the direction perpendicular to gold surface). Thus, the difference in the penetration depth of the evanescent field between two wavelengths can be neglected in our measurement.
2.3 Experiment setup
Figure 1 shows the optical setup of the proposed wavelength-multiplexing SPRHM. Laser beams with the wavelengths of 632.8 nm and 690 nm pass through the collimating lenses CL1, 2 and halfwave plates HP1, 2 to be shaped as collimated light beams with the polarization direction of 45°, respectively. Then, the two light beams go through the focal lenses FL1, 2 (f1 = 150 mm, f2 = 250 mm) and are focused at the back focal plane BFP of the microscope objective (MO, APON100×HOTIRF, NA = 1.70, Olympus, Japan). The light beams are further incident onto the gold layer after passing the MO. The cell chip is coupled with MO via the matching oil. Here, the incident angle of the light beams at the wavelengths of 632.8 nm and 690 nm are adjusted by horizontally moving the beam splitters BS1, 2, respectively. The incident angles are set as 55.4° @632.8 nm and 53.7° @690 nm. In this way, SPR can be excited by the two wavelengths simultaneously. The light beams reflected from the gold layer go through the imaging lens IL, Wollaston prism WP and polarizer P to realize the off-axis hologram recording. As show in the inset on the right side, a linearly-polarized light wave will be split into the p- and s-polarized light waves by WP. Since only the p-polarized light wave can excite SPR and carry the specimen information, it acts as the object light wave in DHM. And the s-polarized light wave has no SPR response and acts as the reference wave. After the modulation by the linear polarizer P, the two light waves have the same polarization direction and interfere with each other. Finally, the light beams of 632.8 nm and 690 nm are separated by the dichroic mirror DM and recorded by the CCD1 and CCD2, respectively. The right bottom inset shows the recorded light beam area at the CCD targets. The reason of using two CCDs for hologram recording is to maintain the sample information in frequency filtering (Supplement 1).
2.4 Sample preparation
RAW264.7 cells were cultured in a humidified atmosphere at 37 °C with 5% CO2. Cells were fed in the DMEM supplemented with high glucose medium (gibco), 10000 U/ml penicillin, 10 mg/ml streptomycin (BI) and 10% fetal bovine serum (BI). The RAW264.7 cell seeding density on the gold surface is 1 × 105 cells/cm2.
3. Results and discussions
3.1 Wide-field mapping of cell parameters under different environmental mediums
Using wavelength-multiplexing SPRHM, we firstly measured cell-substrate distance and cytoplasm RI when the cell is in an isotonic fluid. Initially, background holograms of two wavelengths were captured to extract image background. Then, digital holograms containing cell specimen were recorded successively for 169 s at 1 frame per second (fps). High-quality phase-contrast SPR images of the cell at wavelengths of 632.8 nm and 690 nm were reconstructed from digital holograms using numerical reconstruction algorithm in DHM. Figures 2(a1–a3) and 2(b1–b3) present the reconstructed phase-contrast SPR images at the timepoints of 0, 84 and 169 s at the wavelengths of 632.8 nm and 690 nm, respectively. The SPR phase value varies from location to location over cellular area. The phase response presents differences between two wavelengths, revealing that the SPR signal is sensitive to the wavelength. It is worthy to mention that the wavelengths of 632.8 nm and 690 nm are sufficient to measure the cell and background separately in our system. Since the bulk solution may also lead to the SPR phase changes and influence the measurement accuracy [36], we averaged the phase of the background and subtracted it from the whole region of interest (ROI) to remove the noises from the cell culture medium in every frame. Moreover, our method does not require a designed pattern on the sensor surface as the plasmonic-based impedance microspectroscopy [37], so the local RI variation of sensor material is circumvented in our system. Since the SPR phase is inhomogeneous in the cellular area, the cell-substrate distance and cytoplasm RI also distribute unevenly in lateral direction. Figures 2(c1–c3) and 2(d1–d3) present the wide-field distributions of cell-substrate distance and cytoplasm RI at t = 0, 84 and 169 s when the cell is in the isotonic medium, respectively. Note that the signal difference at the cell edges in Fig. 2(c1–c3) and 2(d1–d3) results from the SPW propagation [38]. Additionally, at some sites within the cell, the cell-substrate distance approaches to zero. It is because of the focal contacts where cell adhesion proteins bind to integrins [39].
Then, we explored the cell response to a high osmotic pressure condition by replacing the isotonic culture medium with hypertonic fluid. The cell-substrate interactions under the high osmotic pressure stimulations were monitored by recording digital holograms of two wavelengths with a period of 169 s. We reconstructed the phase-contrast SPR images of two wavelengths and obtained the distributions of cell-substrate distance and cytoplasm RI (Supplementary Fig. S3). Finally, we removed the hypertonic solution and added hypotonic fluid in the cell culture chamber to follow the cell behaviors at the cell-substrate interface. On the contrary to the hypertonic fluid, the hypotonic medium has a low osmotic pressure. The cell was monitored with the same period of 169 s with the above experiments. The phase-contrast SPR images, cell-substrate distance and cytoplasm RI distributions in this process can be found in Supplementary Fig. S4.
3.2 Dual parameter evolutions of a living cell under different environmental mediums
In addition to wide-field characterization of cell-substrate distance and cytoplasm RI, the dynamic evolutions of cell parameters under different external environments were also studied. Specifically, four cellular regions (70 × 70 pixels) were randomly selected, as shown in the inset of Fig. 3(a1). Then, the average values of cell parameters in these ROIs are calculated and the time traces are plotted. The measurement results of cell parameters in the isotonic fluid are depicted in Figs. 3 (a1) and 3(a2). When the cell is in the isotonic medium, the cell keeps normal morphology, as shown in the inset of first row in Fig. 3. The values of cell-substrate distance and cytoplasm RI in the four ROIs vary in the range of 55–105 nm and 1.35–1.37 RIU, respectively. The cell-substrate distance quantitatively reveals the cell-substrate interactions of the measured cell. There exist close contacts and extracellular matrix contacts in the bottom membrane of the cell [39]. Furthermore, one can note that the values of cell parameters remain steady with small fluctuations over time, indicating a stable intracellular environment.
Furthermore, Figs. 3(b1) and 3(b2) plot the temporal evolutions of cell-substrate distance and cytoplasm RI in the same ROIs after the hypertonic fluid was pumped in the cell chamber, respectively. Clearly, all the ROIs exhibit an increasing trend in cell parameters during the monitoring period. Larger fluctuations of the signals are observed, which indicates a dynamically-changing intracellular environment induced by the external stimulations. Moreover, the temporal changes of cell parameters are not homogeneous across the cell area. The cell-substrate distance increasing from initial to final moments in ROIs 1–4 (marked by grey, red, blue and green colors, respectively in Fig. 3(a1)) are 3.3, 9.6, 13.3, and 26.2 nm, respectively. As for cytoplasm RI, it displays an increase of 0.002, 0.004, 0.006, 0.012 RIU in ROIs 1–4, respectively. Actually, the signal changes are in good agreement of cell response in the high osmotic pressure condition. As illustrated in the inset of the second row in Fig. 3, when the cell is surrounded by hypertonic medium, cell morphology shrinks because of the higher osmotic pressure in extracellular environment. The cell bottom membrane moves upward, leading to a larger cell-substrate distance. Meanwhile, since the water flows out of the cell, the intracellular concentration will be higher, which results in an increased cytoplasm RI [40].
Moreover, the time traces of cell-substrate distance and cytoplasm RI under the low osmotic pressure stimulus are plotted in Figs. 3(c1) and 3(c2), respectively. This time we observe a decreasing trend in the cell parameters under the hypotonic environment. The changing amplitude of cell-substrate distance and cytoplasm RI is not spatially homogeneous. Specifically, ROI4 (marked in green color) has the most prominent variations with cell-substrate distance descending of 13.7 nm and cytoplasm RI dropping of 0.006 RIU. The most moderate changes of cell parameters are identified in ROI1 (marked in grey color) with cell-substrate distance decreasing from 98 nm to 95 nm and cytoplasm RI descending from 1.369 RIU to 1.368 RIU. The measurement results of cell dual parameters can also be interpreted by the cell behavior in the hypotonic condition, as shown in the inset of the third row in Fig. 3. With the decreased osmotic pressure in extracellular environment, the cell will swell with water flowing into the cell. This leads to an increased cell volume. The cell bottom membrane is pushed to the substrate with a decreased cell-substrate distance. Meanwhile, the medium flowing into the cell dilutes intracellular fluids with lower concentration, leading to a reduced cytoplasm RI.
In order to further compare the cell-substrate distance and cytoplasm RI changes under the isotonic, hypertonic and hypotonic mediums, we performed statistical analysis by obtaining histograms of cell parameters in three conditions. The results are shown in Fig. 4. Specifically, Figs. 4(a1), 4(a2) and Figs. 4(a3), 4(a4) present the histograms of cell-substrate distance and cytoplasm RI when the cell was exposed to an isotonic fluid at the initial and final moments, respectively. The Gaussian fitting was employed and Gaussian average values of cell dual parameters were determined. It can be seen that the average values of cell-substrate distance and cytoplasm RI remain stable in the normal environment. Moreover, Figs. 4(b1–b4) and 4(c1–c4) exhibit the results after the hypertonic and hypotonic solutions were injected, respectively. When the cell is in a hypertonic medium, the average values of cell dual parameters increase and the histograms move rightward to a higher value. The contrary behaviors of these two parameters are observed when the cell is stimulated by low osmotic pressure environment. Therefore, the statistical analysis here is consistent with the results in Fig. 3. Compared to the work which only reveals either cytoplasm RI or cell bottom membrane displacement under osmotic pressure stimulations [40,41], our approach realizes simultaneous measurement of cell dual parameters, providing more insights of cell behavior to biological studies. Moreover, one can notice that the cytoplasm RI before hypertonic medium is below that under the isotonic and hypotonic mediums. This is because of the cell variations during the transitional period of three treatments. In our experiment, after the old medium was gently replaced by a new one and fluidic environment was stabilized, the measurement was resumed. Therefore, time interval exists between measurements of three conditions, leading to a discontinuous RI change in Fig. 4. The cell parameter measurement results under hypertonic and hypotonic conditions from another cell were also provided, showing the similar changes to the results in Fig. 4 (Supplement 1).
3.3 Discussions
Since the cell dual parameters in our work are determined from the reflection phase shift difference of SPR, we characterized the system stability by monitoring the phase fluctuations of the system. The temporal fluctuations of the SPR phase could originate from several possible factors including the temperature variations, mechanical vibrations and electronic noise from the CCD camera in the system. In the experiment, we successively recorded the digital holograms without cell specimens for 500 s at the rate of 1 fps. Using the double-exposure DHM and numerical reconstruction algorithm, the reflection phase shift difference of each frame was obtained at the wavelengths of 632.8 nm and 690 nm. Then, an area containing 100 × 100 pixels was chosen at random and the standard deviation of the reflection phase shift difference in each pixel was calculated. The histograms of the standard deviation of the phase values at the wavelengths of 632.8 nm and 690 nm were further obtained, as shown in Figs. 5(a) and 5(b), respectively. The average value of the standard deviation of the reflection phase shift difference is 2.7° and 3.8° in 500 s at the wavelengths of 632.8 nm and 690 nm, respectively, reflecting a high temporal stability of the setup. The phase fluctuations in our setup at both wavelengths are very small and consistent with our previous work [30]. As a matter of fact, the high temporal stability is due to the holographic recording structure in our setup, in which the object and reference waves transmit in the common optical path to resist environmental disturbances [42]. The measurement uncertainties of cell-substrate distance and cytoplasm RI caused by the phase fluctuations of two wavelengths were analyzed in Supplement 1. Additionally, in order to assess the contributions of experiment noise to the inhomogeneous distribution of cell parameter, we simplified the SPR model with a fixed cytoplasm RI to study the cell-substrate distance. It shows that the measurement error of cell-substrate distance is small and the error at the cell edge is larger than that in the central area (Supplement 1). We also analyzed the measurement uncertainty of cell parameters caused by the possible deviations of parameter values in SPR model (Supplement 1).
4. Conclusions
In conclusion, a wavelength-multiplexing SPRHM was demonstrated to dynamically measure the cell-substrate distance and cytoplasm RI at the same time. By independently adjusting the incident angle of 632.8 nm and 690 nm with two separated BS, SPR can be excited at two wavelengths simultaneously. Therefore, compared to the previously-reported setup in Ref. 28 which requires sequential excitation of SPR for two wavelengths, the proposed setup possesses the advanced functionality of real-time tracking of cell parameters. Experimentally, we revealed the cell responses at the cell-substrate interface to external stimuli including high- and low-osmotic pressure conditions by tracking the dynamic changes of cell parameters. The cell shrinkage and swelling under hypertonic and hypotonic solutions were detected from the evolutions of cell-substate distance and cytoplasm RI thanks to the high sensitivity of SPR. We believe the proposed optical sensing tool opens up new perspectives for interfacial phenomenon detection of living cells.
Funding
National Natural Science Foundation of China (61927810, 62005219); Fundamental Research Funds for the Central Universities (310202011qd004).
Disclosures
The authors declare no conflicts of interest regarding this article.
Data availability
Data underlying the results presented in this paper are not publicly available at this time but may be obtained from the authors upon reasonable request.
Supplemental document
See Supplement 1 for supporting content.
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