Article pubs.acs.org/Langmuir
Inhibition Assay of Yeast Cell Walls by Plasmon Resonance Rayleigh Scattering and Surface-Enhanced Raman Scattering Imaging Kiran Manikantan Syamala,† Hiroko Abe,† Yasuko Fujita,† Kazuya Tomimoto,† Vasudevanpillai Biju,† Mitsuru Ishikawa,† Yukihiro Ozaki,‡ and Tamitake Itoh*,† †
Health Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Takamatsu, Kagawa 761-0395, Japan ‡ Department of Chemistry, School of Science and Technology, Kwansei Gakuin University, Sanda, Hyogo 669-1337, Japan S Supporting Information *
ABSTRACT: We report on plasmon resonance Rayleigh scattering (PRRS) and surface enhanced Raman scattering (SERS) imaging for inhibition assay of yeast cell walls. This assay reveals that the proteins having alkali sensitive linkage bound to β1,3 glucan frameworks in cell walls are involved in SERS activity. The result is further confirmed by comparison of genetically modified cells and wild type cells. Finally, we find that PRRS and SERS spots do not appear on cell walls when daughter cells are enough smaller than parent ones, but appear when size of daughter cells are comparable to parent cells. This finding indicates the relationship between expression of the proteins that generate SERS spots and cell division. These results demonstrate that PRRS and SERS imaging can be a convenient and sensitive method for analysis of cell walls.
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INTRODUCTION For the analysis of cell surface molecules, fluorescent labels, such as dye molecules or quantum dots, have been well developed.1 However, photobleaching or pH-dependence of such labels still prevents us from stable and long-time observations. As an alternative for them, Ag or Au NPs, which have strong plasmon resonance in visible to near infrared (NIR) region, have been expected because they are free from photobleaching.2 Furthermore, plasmon resonance Rayleigh scattering (PRRS) imaging is easily carried out under single NP level by white light dark-field illumination.3 The problem of PRRS imaging is that we cannot intrinsically differentiate Rayleigh scattering of Ag NPs from that of other components on the cells. Thus, simultaneous use of PRRS with surface enhanced Raman scattering (SERS) is helpful for the differentiation. SERS is enhanced Raman scattering by plasmon resonance by a factor of ∼108−14 for the molecules located in gaps inside dimers of NPs.4−10 Raman spectra have distinct vibrational bands known as “molecular fingerprints”.11 Thus, the large enhancement factors of SERS enable us multiplexed detections of molecules with weak excitation power compared with the conventional Raman one.12−17 Combination of PRRS and SERS may improve molecular imaging and spectral analysis for monitoring of biological structures.16,17 The other advantages of PRRS and SERS are robustness against laser excitation, biocompatibility, straightforward sample preparation, and timeefficient analysis.12−17 We consider that PRRS and SERS analysis using known proteins expressed in model cells may be a key to the extension of the analysis to a practical method. Yeast cells are potential © 2012 American Chemical Society
candidates for the analysis because proteins expressed in yeast cells have been well attributed.18−21 Thus, several research groups have applied PRRS and SERS spectral analysis for detections of yeast cell (Saccharomyces cerevisiae) wall molecules.16 However, attribution of the molecules generating PRRS and SERS spectral signals are quite difficult because of inhomogeneity in the molecular distributions, nontargeted delivery of Ag NPs, and huge SERS spectral variations.16 Such difficulty has limited the extension of PRRS and SERS spectral analysis to a practical method. In the current work, instead of previous spectral analysis,16 we applied inhibition assay to yeast cells using PRRS and SERS imaging. By combining the imaging with biochemical treatments, we revealed that the appearance of PRRS and SERS spots was due to the expression of alkali-sensitive mannoprotein that is covalently bound to β1,3 glucan frameworks on cell walls. By comparison of modified and wild type cells we confirmed that one kind of the proteins (Pir1) exhibited PRRS and SERS signals. The analysis of PRRS and SERS images of many cells suggested that the expression of the proteins may be related to cell division cycle. The current investigations indicated that PRRS and SERS imaging can be a powerful method for sensitive noninvasive analysis of cell surfaces. Special Issue: Colloidal Nanoplasmonics Received: January 30, 2012 Revised: March 26, 2012 Published: March 28, 2012 8952
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SERS images were monitored using a digital camera (Nikkon, COOLPIX5000, Tokyo). SERS light from cells was collected with a common objective lens and sent to the polychromator (Pro-275, Acton, Tokyo) equipped with a charge-coupled device (CCD, DV434FI, Andor, Tokyo) for spectral measurements. The spectral resolution of the measurements was 15 cm−1. Figure 1c, d shows typical PRRS and SERS images before and after adsorption of Ag NPs on yeast cells. The adsorption of Ag NPs is clearly identified by the difference in the images. Note that adsorption of Ag NPs on yeast cell walls was also confirmed by atomic force microscope (AFM) and scanning electron microscope (SEM) imaging.16 The details of the spectroscopic system is described elsewhere.22,23 The experiment to understand the SERS activity during the cell division was performed as described here. The experiments were performed after isolating the cells from different stages of cell cycle stages and treating them with a colloidal solution of Ag NPs. It should be noted here that the cells were not cultured along with a colloidal solution of Ag NPs to monitor the SERS activity, since the colloidal solution aggregates and precipitates in the presence of culture broth. Details of materials and chemicals, sample preparations, differential treatment for removing components of yeast cell walls, construction of Pir1 overexpressing yeast cells, and construction of PIR1 gene disrupted yeast cells are provided in the Supporting Information.
EXPERIMENTAL SECTION
The experimental setup for PRRS and SERS imaging is briefly illustrated in Figure 1a, b. To simplify the notations, “PRRS images”
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RESULTS AND DISCUSSION
Inhomogeneity in SERS Spectra from Yeast Cell Walls. We checked inhomogeneity in SERS spectra from many spots on yeast cells. Figure 2 shows the selected six spectra from them. SERS spectra mainly exhibit bands in the 1218− 1717 cm−1 region. Several reports tentatively attribute the bands around the region to vibrational modes of protein molecules based on several reports.16,24−28 SERS bands 1218−1289 cm−1 are likely assigned to Amide III of protein, 1321−1335 cm−1 to protein γT (CH2−CH3), 1353−1367 cm−1 to alanine and tyrosine, 1437 cm−1 to δCH2 and COO−, 1534−1567 cm−1 to protein Amide II, and 1621 cm−1 to δNH2.16,24−28 However, SERS spectral shapes and intensities are largely different from each other, and we cannot find any correlation between SERS spectra and cell division. There are several candidates of the origin of spectral inhomogeneity in SERS, for example, chemical interactions, molecular orientation, molecular segments interacting with local fields in the hot spots, and so on.10,17,29−32 We consider that the spectral
Figure 1. (a) Optical setup for measurement of PRRS images and (b) SERS images. (c) Typical PRRS images of yeast cells before (left panel) and after (right panel) adsorption of Ag NPs. (d) Typical SERS images of yeast before (left panel) and after (right panel) adsorption of Ag NPs. Each scale bar denotes 10 μm. means both dark-field imaging with and without adsorption of Ag NPs, and the notation of “SERS imaging” means conventional fluorescence underlining as background of SERS spectra. PRRS imaging of the yeast cell wall was carried out by introducing white light from a 50 W halogen lamp into the sample through a dark-field condenser lens in an inverted optical microscope (Olympus IX70, Tokyo). A cw diode laser (Coherent DPSS 532, Palo Alto, CA; 532 nm, 2.0 W/cm2) was used as the excitation light source for SERS imaging. A holographic notch filter was placed behind an objective lens (Olympus LCPlanF1, 60×, N.A. 0.7, Tokyo) to block Rayleigh scattering laser light from the cells.
Figure 2. SERS spectra randomly selected from single SERS spots on yeast cell walls. 8953
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Figure 3. (a) PRRS (left panel) and SERS (right panel) images of untreated control cells. (b, c) PRRS and SERS images of the cells boiled with SDS (0.1% w/v) for 5 and 10 min, respectively. (d, e) PRRS and SERS images of the cells treated with 2.5 and 5.0% hydrofluoric acid, respectively. (f) PRRS and SERS images of the cell treated with β1,6 glucanase. (g) PRRS and SERS images of the cells treated with β1,3 glucanase. Each scale bar denotes 10 μm.
was examined by treating cells with hydrofluoric acid (HF) (2.5 and 5% v/v) and β1,6 glucanase, respectively. HF specifically removes GPI anchored proteins and β1,6 glucanase breaks linkages of β1,6 glucan. Figure 3d−f shows PRRS and SERS spots, indicating that GPI anchored proteins and β1,6 glucan were not involved in the adsorption of Ag NPs on the mannoproteins. Finally, contribution of β 1,3 glucan to PRRS and SERS spots was examined by treating cells with β 1,3 glucanase, which specifically breaks β1,3 linkages on cell walls. Interestingly, Figure 3g shows that PRRS and SERS spots disappeared after β1,3 glucanase treatments. This disappearance indicates involvement of β1,3 glucan in PRRS and SERS spots and thus adsorption of Ag NPs on this type of mannoproteins. Form the inhibition assay of yeast cell walls, we identified that proteins linked to β1,3 glucan are specifically responsible for the PRRS and SERS spots. The details of each procedure of chemical treatments are provided in the Supporting Information. The identified protein has alkali sensitive linkage bound to β1,3 glucan in cell walls.37−39 Thus, we checked the effect of pH on PRRS and SERS spots on cell walls. We measured PRRS and SERS images of cells at different pH values. Figure 4a−c shows typical images of cells treated by acidic (pH 1.5), neutral (pH 7.0), and alkaline (pH 12) aqueous solutions. PRRS and SERS spots were not observed on the cells at pH 12, but observed on the cells maintained at pH 7.0 and 1.5. The effect of pH indicates that the components involving PRRS and SERS spots are removed or altered at alkaline pH. This observation supports the contribution of proteins with β1,3 glucan to PRRS and SERS spots. Additionally, we examined PRRS and SERS images of an extracted solution after the alkaline treatment,
inhomogeneity in the SERS spectra are due to chemical interaction between SERS active molecules and surfaces of Ag NPs.17,29−32 Indeed, SERS spectra of biomolecules are sensitive to the chemical interaction between Ag surfaces and lone pair electrons in N atoms of molecules forming charge transfer state.29−32 However, the large inhomogeneity in the SERS spectra indicates that direct attribution of molecules which adsorb on Ag NPs and generate SERS is very difficult for us exclusively by SERS spectral analysis. Inhibition Assay of Yeast Cell by Various Chemical Treatments. From the previous report, we identified that mannoproteins are involved in SERS spots on yeast cells.16 Mannoproteins are broadly classified into two types: O-glycosylated mannoproteins linked to β1,3 glucan;33−35 and glycosylphosphatidylinositol (GPI) linked mannoproteins which are linked to β1,6 glucan, that are bound to β1,3 glucan.33−35 Mannoproteins are localized on the outer layer of cell walls, which are exposed to the external environment. To identify the mannoproteins involved in PRRS and SERS spots, we examined PRRS and SERS images after specifically removing each component linked to mannoproteins from cell walls by chemical and enzymatic methods. Figure 3a shows control experiments of PRRS and SERS images. First, contribution of noncovalently attached proteins to PRRS and SERS spots was examined by boiling the cells with 0.1% dodecyl sodium sulfate (SDS), which specifically removes noncovalently attached proteins from cell walls.36 Figure 3b, c shows that PRRS and SERS spots were observed like in Figure 3a after the boiling for 10 min, indicating adsorption of Ag NPs on the mannoproteins. Thus, we excluded the contribution of the proteins noncovalently attached on cell walls. Second, the contribution of the proteins anchored by GPI and β1,6 glucan 8954
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Figure 5. (A) PRRS (left panel) and SERS (right panel) images of the yeast cells overexpressing Pir1 protein. (B) PRRS and SERS images of the control yeast cell. Each scale bar denotes 10 μm.
overexpression. Note that this result does not mean that Pir1 proteins dominate generation of PRRS and SERS spots of wild type of yeast cells, because Pir1 proteins are localized at bud scars.40 We tentatively consider that overflow of overexpressed Pir1 proteins from bud scars results in the increase in the number of PRRS and SERS spots on total cell surfaces. Indeed, we confirmed that Pir1 proteins totally covered cell wall surfaces by an antigen−antibody reaction method (data not shown). To further examine the contribution of Pir1 proteins to PRRS and SERS spots, we compared disruptant yeast cells lacking Pir1 proteins with control ones. The details of the construction of PIR1 gene disrupted cells are provided in the Supporting Information. Figure 6 shows that PRRS and SERS spots were not observed from mutant cells. However, the dark field image may show very little PRRS spots on cell walls as shown in Figure 6, indicating poor adsorption of Ag NPs on the cell walls. Note that this result also does not mean that Pir1 proteins, which are localized at bud scars, dominate generation of PRRS and SERS spots in the case of wild type of yeast cells.40 We tentatively consider that disruption of the PIR1 gene may results in the decreasing in the number of protein involved in PRRS and SERS spots. One of the possibility for specificity of Ag NPs interaction with the β1,3 glucan mannoprotein may be due to the electrostatic interaction between the Ag NPs and Pir 1,3 β glucan complexes. The Ag NPs are negatively charged and the Pir-1,3 β glucan complexes may provide surface polarity enhancing the electrostatic interactions leading to the binding of Ag NPs to the cell wall. Further it is also not clear whether the binding of Ag NPs to the Pir-1,3 β glucan complexes may be due to the affinity of Ag NPs for O-glycosylated mannoproteins, because Pir proteins are heavily O-glycosylated. We further analyzed the affinity of Pir1 proteins for Ag NPs by in vitro affinity assay, where the isolated Pir1 proteins was incubated with Ag NPs and the amount of Pir1 proteins bound with Ag NPs was analyzed by Western blotting. The results implied that Pir1 protein has affinity for Ag NPs indicating that Pir protein chemically interact with Ag NPs (data not shown). PRRS and SERS Imaging for Cell Division. The composition of cell walls is drastically modified during the cell division.18−21,40 To examine whether it is possible to characterize
Figure 4. PRRS (left panel) and SERS (right panel) images of yeast cells maintained at pH (a) 1.5, (b) 7.0, and (c) 12. (d) PRRS and SERS images of alkali extract of the cells neutralized with HCl. Each scale bar denotes 10 μm.
because the proteins are expected to be resolved into the solution. Figure 4d shows SERS light spots from the solutions, indicating we measured the proteins resolved into the solution. Thus, we consider that the proteins bound to β1,3 glucan through alkaline labile linkage are likely involved in PRRS and SERS spots. The details of each procedure pH treatments are provided in the Supporting Information. PRRS and SERS Imaging for Yeast Cells after Overexpression of Pir Proteins. There are several kinds of proteins linked to β1,3 glucan.40 Thus, Pir protein is one of the candidates of the protein involved in PRRS and SERS spots.40 We selected Pir1 protein and investigate its contribution to PRRS and SERS spots by compared yeast cells which overexpress Pir1 proteins with control ones. The details of the construction of Pir1 overexpressing yeast cells are provided in the Supporting Information. Figure 5 shows that PRRS and SERS spots of overexpressing cells were much clearer than those of the control cells, indicating that the contribution of Pir1 proteins to PRRS and SERS spots is enlarged by the 8955
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Figure 6. (a) PRRS (left panel) and SERS (right panel) images of the control yeast cell. (b) PRRS and SERS images of Pir1 disrupted cells. (c) Magnified view of the PRRS image of the Pir1 disrupted cells showing only a small number of Ag NPs on the cell walls. Arrowhead points toward Ag NPs. Each scale bar denotes 10 μm.
the modification during division by PRRS and SERS imaging, we measured their images of cells undergoing division. Figure 7a
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CONCLUSIONS
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ASSOCIATED CONTENT
In the present work, we examined contribution of mannoproteins on yeast cell wall surfaces to PRRS and SERS spots by inhibition assay. Disappearance of PRRS and SERS spots on cells after β1,3 glucanase treatment indicated that proteins linked to β1,3 glucan specifically contributed to PRRS and SERS spots. Furthermore, the proteins extracted from the cell wall showed SERS spots, indicating affinity of the proteins to Ag NPs. Comparison of control cells with modified cells overexpressing or lacking Pir1 protein, which is one of the mannoprotein linked to β1,3 glucan, showed the contribution of Pir1 protein to PRRS and SERS spots. Furthermore, we found the correlation between size of daughter cells and appearance of PRRS and SERS spots, indicating that PRRS and SERS imaging will be valuable for an ultrasensitive noninvasive tool for analysis of cell wall changes. Finally, we pointed out the difficulty to obtain reproducible SERS spectra in the work. The reproducible SERS spectra have time dependence for an effective interaction.41 The proteins are dynamic systems with various factors that affect the unique interaction with Ag NPs, that is, flexibility/mobility, accessibility, polarity, exposed surface, and turns. We consider better reproducible SERS spectra will be obtained by improving the spectral and temporal resolution.
Figure 7. RRS images (right panels) and SERS ones (left panels) of yeast cells for different size of daughter cells. Each scale bar denotes 10 μm.
shows that PRRS and SERS spots do not appear on cell walls when daughter cells are enough smaller than parent cells, indicating lack of adsorption of Ag NPs on cell walls. Figure 7b, c shows that PRRS and SERS spots appear on cell walls possibly prior to cytokinesis and septum formation when the size of daughter cells is rather comparable to that of parent cells, indicating adsorption of Ag NPs on cell walls. The differential adsorption of Ag NPs on the cell wall of parent and daughter cells may be due to the differential expression of Pir proteins, indicating the possibility to characterize cells at different stages of cell division by PRRS and SERS imaging. The details of the description of the correlation between PRRS and SERS imaging and size of daughter cells are provided in the Supporting Information. Note that the detailed examination of correlation between cell wall dynamics during cell cycle and PRRS and SERS spots should be also checked by flow cytometric analysis of cellular DNA contents.
S Supporting Information *
Details of materials and chemicals, sample preparations, differential chemical and pH treatment for removing components of yeast cell walls, construction of Pir1 overexpressing yeast cells, construction of PIR1 gene disrupted yeast cells, and the description of correlation between PRRS and SERS imaging and size of daughter cells. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest. 8956
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ACKNOWLEDGMENTS The current study was supported by Priority Area (19049013) “Strong Photon-Molecule Coupling Fields (No. 470)” from Ministry of Education, Culture, Sports, Science and Technology, Japan, Grant-in-Aid for Scientific Research B 20510111, C 21310071, C 21550168, and C 23560049 from Japan Society for the Promotion of Science (JSPS), through its Funding Program for World-Leading Innovative R&D on Science and Technology (FIRST Program), Japan, and Industrial Technology Research Grant Program in 2009 (09A08011a) from New Energy and Industrial Technology Development Organization (NEDO), Japan. We thank to Dr. H. Hirayama and Dr. T Suzuki (Glycometabolome Team, Systems Glycobiology Research Group, RIKEN, Advanced Science Institute, 2-1 Hirosawa, Wako Saitama 351-0198, Japan) for the endo-1,6β-glucanase expressing plasmid (pET28a(+)-NcNEG1) and Dr. Y. Nakajima and Dr. Y. Yoshida (Health Research Institute, AIST) for useful discussions.
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