Hydrogen bonds of interfacial water in human breast cancer tissue compared to lipid and DNA interfaces

Halina Abramczyk, Beata Brozek-Pluska, Jakub Surmacki, Joanna Jablonska-Gajewicz, Radzislaw Kordek

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Technical University of Lodz, Institute of Applied Radiation Chemistry, Laboratory of Laser Molecular Spectroscopy, Lodz, Poland.

DOI: 10.4236/jbpc.2011.22020                

Abstract

The paper presents the results for water confined in a human breast cancerous tissue, a single stranded DNA, a double stranded DNA and in phospholipids (DPPC - D-a-Phosphati dylcholine, dipalmitoyl). The interfacial water in DNA and lipids is represented by a double band in the region of the OH stretching mode of water corresponding to the symmetric and asymmetric vibrational modes, in contrast to water confined in the cancerous breast tissue where only one band at 3311 cm-1 has been recorded. The marked red-shift of the maximum peak position of the OH stretching mode confirms that the vibrational properties of the interfacial water observed in restricted biological environment differ drastically from those in bulk water. The change of vibrational pattern of behavior may be due to the decoupling of the vibrations of the OH bonds in water molecule or change of the vibrational selection rules at biological interfaces. According to our knowledge Raman vibrational properties of water confined in the normal and cancerous breast tissue of the same patient have not been reported in literature yet. Here we have also presented the first Raman ‘optical biopsy’ images of the non-cancerous and cancerous (infiltrating ductal cancer) human breast tissues.

Keywords

H-Bond; Lipids; Breast Cancer; Raman Imaging; Interfacial Water; Vibrational Spectroscopy

1. INTRODUCTION

The properties of water have always been a central subject of investigation. The basic motivation behind such studies is the role of water in biological activity of most molecular processes such as protein-DNA interactions or activity of biological lipid membranes [1-4]. The biological activity depends on stability, structure, and dynamics of water at biological interfaces. The molecular processes in the restricted environments are largely dominated by interactions, vibrational energy transfer, orientation of water molecules, which differ drastically from those of bulk water properties. The confinement of water in biological structures does not represent a single pattern of behavior. For example, water confined in reverse micelles [5-9] differs from water confined in phospholipid membranes [10] or in DNA interfaces [3].

The biological interfaces play an important role in a variety of vital reactions involved in protein interactions, enzyme catalysis, molecular recognition, and various steps of proton and electron transfer pathways. The interactions with water modify static and dynamical properties of lipid bilayers. Moreover, the interactions lead to modification of the diffusion barrier across the membrane to ions and oxygen for example [11]. The modification of the interfaces by water may play an important role in energy dissipation in lipids, which is a key mechanism in maintaining photostability of the biological tissue. Unraveling the role of interfacial water in biological systems has required the application of a number of different techniques. The electron and neutron diffraction, X-ray absorption and diffraction, NMR and electron microscopy have enabled the direct probing of the static structure of hydration patterns. There is a large body of literature that review different aspects of static structure of interfacial water [2,12-17].

Recent developments of time-resolved electron and X-ray methods [18] have enabled the direct probing of the ultrafast structural dynamics. Several reviews have appeared in literature on various aspects of dynamics of interfacial water [1,19-33].

The biological tissue contains both the bulk and the confined water. With the advent of clinical imaging (X-ray mammography, magnetic resonance imaging (MRI), ultrasounds (US)) and novel promising methods (near infrared imaging, Raman imaging) valuable tools have been added to extend diagnostic applications such as screening of the breast cancer, which is the most common form of cancer in women. The bulk and the confined water as well as the other significant tissue components (deoxyhemoglobin (Hb), oxyhemoglobin (HbO₂), adipose) may impede the efficacy of screening in some methods (X-ray mammography, MRI, US). On the other side, information about interfacial water may establish better basis to characterize tissue quantitatively in terms of its optical parameters, such as the scattering and absorption coefficients by optical imaging (Raman, IR, fluorescence) [34,35].

One of the most direct probes to elucidate the structure and dynamics of confined water are the infrared and Raman spectroscopies [1,36-41]. The stationary and time resolved vibrational spectra modified by interaction with biological interfaces are valuable sources of information to extract microscopic picture of the hydration layer. Vibrational properties of the confined water may provide an understanding of interactions with the tissue environment that reflects changes in tissue cellularity, metabolic activity, physiology, and response to cancer. The recent availability of extremely high spatial resolution of optical spectroscopy has led to development of the new techniques such as Raman scanning, which is capable of providing structural information on the nanometer level. As a basic principle of the method is that the specimen is scanned across a laser beam which has a diameter of 200 nm. Measuring the Raman scattering (RS) intensity at each position provides an image of the specimen with a resolution similar to light microscopy. Among the optical methods of diagnostics RS seems to be potentially the most powerful because it provides direct biochemical information from vibrational fingerprint spectra.

In this paper we present our results on vibrational properties of water confined in the non-cancerous and cancerous human breast tissue and compare them with the properties of water confined at the interfaces for selected components of the biological tissue such as DNA (single stranded DNA and a double stranded DNA), phospholipids (DPPC—D-α-Phosphatidylcholine, dipalmitoyl). According to our knowledge Raman vibrational properties of water confined in the normal and cancerous breast tissue of the same patient have not been reported in literature yet. The results presented in the paper provide a basis for a substantial revision for interpretation of the origin of the IR and Raman bands observed in the region of the OH stretching mode of the interfacial water.

2. EXPERIMENTAL METHODS

DPPC (D-α-Phosphatidylcholine, dipalmitoyl) was purchased from Aldrich (product number: P1652). The double stranded DNA was purchased from Thermo Scientific, Ulm, Germany and was composed of 5’-AAT ATA TAT ATA TAT ATA TAT AA-3’ and 5’-TTA TAT ATA TAT ATA TAT ATA TT-3’ strands. The single stranded DNA was purchased from Institute of Biochemistry and Biophysics Polish Academy of Science, Warsaw, Poland and had a following sequence: 5’-TTA TAT ATA TAT ATA TAT ATA TT-3’. Scheme 1 presents the systems studied in the paper.

The breast tissue samples were prepared from the material removed in a surgical operation of a patient suffering from an infiltrating ductal breast cancer. The breast tissue samples taken for research did not affect the course of the operation or treatment of the patients. All procedures were conducted under a protocol approved by the institutional Bioethics Committee at the Medical University of Lodz, Poland (RNN/29/11/KE, RNN/30/11/KE, RNN/31/11/KE). As physiology of the health and diseased tissues are complex and influenced by multiple internal and external factors, we have limited our comparison of the cancerous and non-cancerous samples to the same patient. The total number of patients was 146 [34-35].The histological analysis has been performed by the pathologists from the Medical University of Lodz, Department of Pathology, Chair of Oncology. After general description of the tumor mass, the surgical margins were marked with ink and the material was dissected. The specimens were cut longitudinally into slices about 2 cm thick and the features of the cross-sections were described. In the next step the appropriate tissue samples from the tumor mass and from the tumor margin, where no carcinoma was detected by the pathologists, were taken for histopathological and Raman analysis. Two types of the breast tissues have been examined by Raman spectroscopy: bulk tissue, and thin sections of 2 cm. The thin sections were obtained by cryosectioning of the bulk tissue with a microtome. The bulk tissue samples require no processing. The samples for histopathological analysis were fixed in 10% buffered formalin, embedded in paraffin, put on microscopic glasses and stained with hematoxylin and eosin. The adjacent sections of the samples for Raman measurements were not stained. After Raman measurements the thin sections were stained and underwent the histopathological examination.

Our experimental approach employed IR, Raman spectroscopy and Raman imaging. The home made stainless steel cell was constructed to control the water content of the film for IR measurements. The cell was connected to the reservoir where various salt aqueous solutions were placed to maintain the controlled humidity. The controlled constant humidity has been maintained by compounds in contact with the film within an enclosed space around it. P₂O₅, saturated salt aqueous solutions of CH₃COOK, NaCl, NaBrO₃ and pure water have been used to maintain humidities of 0, 23, 75, 92, 100%, respectively.

All Raman images and spectra reported here were acquired using a Raman spectrometer Ramanor U1000 (Jobin Yvon) excited with the ion Ar laser (514 nm) and alpha 500 RA (WITec, Ulm, Germany) model. The alpha 500 system consists of an Olympus microscope, coupled with an UHTS spectrometer and a Newton-CCD camera (operating in standard mode with 1024 × 127 pixels at –64˚C with full vertical binning. The laser beam doubled SHG of the Nd : YAG laser (532 nm) is focused on the sample with a numerical aperture NA of 0.50 to the laser spot of 200 nm. The average laser excitation power was 10 mW. Before recording the Raman image, the fluorescence in the sample was quenched by illumination with the excitation light during 500 ms at each point. The quenching of the fluorescence was very effective due to the high optical density provided by the light focusing. IR spectra were recorded using Specord M80, Zeiss. IR-ATR spectra were collected using Nicolet Avatar 330 FT-IR Thermo spectrometer.

The 2D arrays images of ten-thousands of individual Raman spectra were evaluated by the basis analysis method. In this data analysis method each measured spectrum of the 2D spectral array is compared to basis spectra using a least square fit. Such basis spectra are created by from the average spectra from three different areas in the sample. The weight factor in each point is represented as 2D image of the corresponding color and mixed coloring component. The Raman spectra have been analyzed using the principal component analysis (PCA) and MATHLAB least-squares fitting algorithm. The PCA score plots (model—SNV, mean center, first derivative) for all the recorded Raman spectra and all the samples have been obtained [35].

3. RESULTS

Our recent papers [34,35,42] on cancer diagnostics by Raman spectroscopy and Raman imaging demonstrate their power as diagnostic tools with the key advantage for breast cancer pathology. The results demonstrate the ability of Raman spectroscopy to accurately characterize cancer tissue and provide evidence that lipids and carotenoids of the tissue may play an essential role as Raman biomarkers that are able to distinguish between normal, malignant and benign types.

The biological tissue represents a very complex system from the chemical, physical, and biological point of view. Each of the basic components of tissue—lipids, fat, collagen, epithelial cell cytoplasm, cell nucleus with complex DNA structure, calcium oxalate dihydrate, calcium hydroxyapatite, β-carotene, cholesterol, water—represents a complex chemical composition and structure. It is therefore essential to characterize the structure and composition at all levels to understand the complex behavior of such tissues. The detailed Raman spectra analysis of the normal and cancerous breast human tissue has been discussed in our recent papers [34,35,42]. This paper concentrates on the vibrational properties of water confined in the non-cancerous and cancerous human breast tissue and compares the results with the properties of water confined at interfaces for the major components of the biological tissue such as DNA (single stranded DNA and a double stranded DNA), and phospholipids (DPPC—D-α-Phosphatidylcholine, dipalmitoyl).

Figure 1(a) shows typical Raman spectra of the OH stretching vibration of water in the normal (non-cancerous), and cancerous bulk breast tissue (infiltrating ductal cancer) compared to bulk neat water. The maximum band positions at 3258 cm^–1 and 3410 cm^–1 and the band shape in the bulk breast cancerous tissue are identical to those in the neat bulk water.

We could expect that the characteristic features of water molecules near a biological interface, where H-bond network gets locally disrupted, differ significantly from those of bulk due to interactions with lipids, DNA and proteins. Unfortunately, the result from Figure 1(a) indicates simply that there is limited access to the interfacial, confined water by Raman probing in the bulk tissue, which is dominated by the properties of the bulk water.

To check if the way of the sample preparation induces any changes in the Raman features, we have recorded the Raman spectra and images for the thin sections of 2 cm of the human breast cancer tissue (infiltrating ductal cancer) of the same patient as in Figure 1(a). Detailed inspection into the OH stretching band (Figure 1(b)) for the thin section of tissue shows markedly different picture—instead of the two bands at 3258 cm^–1 and 3410 cm^–1 observed in the bulk tissue one can see only an apparently single band with a maximum at 3311 cm^–1 which does not reveal any additional bands when analyzed by deconvolution. It indicates that in the thin sections the laser beam is capable to interrogate deeper into hydration layer, which is usually a few (2-3) water molecular diameters thick and Raman scattering becomes sensitive to the characteristic features of water molecules confined near biological interfaces, which differ drastically from those of the bulk water.

To obtain a more illuminating picture of vibrational behavior of water in human breast tissue we have moni-

(a)(b)(c)

Figure 1. Raman spectra of the OH stretching vibration of water in normal (non-cancerous), and cancerous breast tissue (infiltrating ductal cancer) compared to the bulk neat water, (a) bulk tissue; (b) thin layer of 2 mm of tissue; (c) Raman images of the normal (non-cancerous)—left and cancerous breast tissue (infiltrating ductal cancer)—right.

tored the Raman spectra in selected constituents of the biological tissue: phospholipids and DNA.

Figure 2 presents the IR spectra of the OH stretching vibration of water at DPPC surface, which is one of the dominant constituents of epithelium, for various amounts of water. One can see that both the intensities of the bands at 3232 cm^–1 and 3379 cm^–1 and the maximum peak positions decrease gradually with water content lowering. At the 0% of humidity the OH vibrations of the interfacial water have been observed.

Conflicts of Interest

The authors declare no conflicts of interest.

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