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Antitumour Effect of Valproic Acid Against Salivary Gland Cancer in Vitro and in Vivo

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Antitumour Effect of Valproic Acid Against Salivary Gland Cancer in Vitro and in Vivo ONCOLOGY REPORTS 31: 1453-1458, 2014 Antitumour effect of valproic acid against salivary gland cancer in vitro and in vivo HIROKAZU NAGAI, MASAKO FUJIOKA-KOBAYASHI, GO OHE, KANAE HARA, NATSUMI TAKAMARU, DAISUKE UCHIDA, TETSUYA TAMATANI, KENJI FUJISAWA and YOUJI MIYAMOTO Department of Oral Surgery, Subdivision of Molecular Oral Medicine, Division of Integrated Sciences of Translational Research, Institute of Health Biosciences, The University of Tokushima Graduate School, Tokushima 770-8504, Japan Received November 18, 2013; Accepted December 16, 2013 DOI: 10.3892/or.2013.2959 Abstract. Salivary gland cancer (SGC) has a comparatively Introduction poor prognosis and is prone to frequent recurrence and metastases. Therefore, the development of more effective Salivary gland cancer (SGC) is a rare cancer type of the head chemotherapy against SGC is desirable. The aim of the and neck region where cancer cells form in major or minor sali- present study was to investigate the antitumour effects of vary glands (1-3). Generally, surgical resection is considered to valproic acid (VPA) against SGC in vitro and in vivo. Two be the most common and successful therapeutic approach for human SGC cell lines (HSY and HSG cells) were used in SGC performed today (1,4); however, SGC frequently recurs the present study. The effects of VPA on the proliferation of locally and metastasises to the regional lymph nodes and SGC cells in vitro were assessed by MTT assay. Cancer cells distant organs, which results in poor prognosis (4-6). Although treated with VPA were subjected to cell cycle analysis by flow other treatment approaches for SGC may include radiation cytometry. In addition, the expression levels of p21 and p27 therapy and chemotherapy, SGC exhibits low sensitivity to were examined by real-time RT-PCR to identify the mecha- irradiation and chemotherapy. Therefore, the development of nisms of the antitumour effect of VPA on SGC. The effects more effective chemotherapeutic drugs and strategies against of VPA on cancer growth in vivo were evaluated in a xeno- SGC are desirable. graft model. VPA inhibited the proliferation of SGC cells in Cancer has long been known to be a primarily genetic a dose-dependent manner in vitro. Degenerated cancer cells disease initiated and progressed by alterations in genes, such were observed at high concentrations of VPA. In the cell cycle as oncogenes and tumour suppressor genes. However, recent analysis, VPA induced cell-growth inhibition and G1 arrest reports indicate that various types of cancers are caused by of cell cycle progression in both cancer cell lines in a time- epigenetic changes, which are heritable changes in gene and dose-dependent manner. VPA markedly upregulated the expression that occur without alteration in DNA sequences mRNA expression levels of both p21 and p27 in both SGC (7-9). These epigenetic changes, including DNA methylation cell lines in a time-dependent manner. In the xenograft model and histone modifications, modify the structure of chromatin experiment, VPA treatment markedly inhibited the growth of and affect the accessibility of regulatory proteins to DNA salivary gland tumours when compared with the growth of (10,11). Histone acetylation is one such epigenetic change and the untreated controls. VPA may be a valuable drug in the has been reported to play important roles in the initiation and development of better therapeutic regimens for SGC. progression of cancers (12,13). Histone deacetylation can cause the tightening of chromatin and can block transcriptional acti- vation. Moreover, it is reversible and is regulated by a balance between the opposing activities of histone acetyltransferase (HAT) and histone deacetylase (HDAC). HAT is an enzyme Correspondence to: Dr Hirokazu Nagai, Department of Oral Surgery, Subdivision of Molecular Oral Medicine, Institute of that catalyses the acetylation of N-terminal lysine residues Health Biosciences, The University of Tokushima Graduate School, in histone proteins, which reduces the affinity of histone for 3-18-15 Kuramoto-cho, Tokushima 770-8504, Japan DNA and increases the accessibility of transcriptional regula- E-mail: [email protected] tory protein to chromatin (10). On the other hand, HDAC is an enzyme that catalyses the removal of acetyl groups from Abbreviations: VPA, valproic acid; SGC, salivary gland cancer; histones, and increased HDAC activities are usually associ- HDAC, histone deacetylase ated with transcriptional repression (10). Recently, altered HDAC activities have been shown to Key words: valproic acid, salivary gland cancer, antitumour be present in many types of cancers, possibly representing activity, epigenetics, histone deacetylase inhibitor an attractive target for cancer therapy (7-9,12,13). HDAC inhibitors induce cell cycle arrest and apoptosis of cancer cells by blocking deacetylases leading to the accumulation of 1454 NAGAI et al: ANTITUMOUR EFFECT OF VALPROIC ACID AGAINST SALIVARY GLAND CANCER hyperacetylated histones and alteration of gene transcription subcutaneously into the backs of mice through 26G needles. (7,9,11,14,15,17,18). Various classes of HDAC inhibitors have Once palpable tumours were established at 1 week after the been identified and are currently being tested in phase I/II inoculation, VPA treatment was started by administering VPA clinical trials (12,13). Valproic acid (VPA), which is widely (0, 0.2 and 0.4% w/v) in drinking water. The tumour volume used for epilepsy and manic-depressive psychosis, has also and body weight of the mice were measured twice a week. recently garnered attention as a specific inhibitor of HDAC Tumour volumes were calculated using the following formula: activity (7,19). It is known that chromatin with hyperacety- Tumour volume = 0.5 x L x W2, where L and W represent the lated core histones adopts a relaxed conformation with the largest diameter and the smallest diameter, respectively. For unfolding of the associated DNA and chromatin remodelling each treatment, six mice were used. during the nucleosome packing of DNA, which are key steps in the regulation of many genes that play crucial roles in cell Cell cycle analysis. The cell cycle distribution was analysed growth and differentiation (10). VPA has been reported to using a fluorescence-activated cell sorter (FACS) as previously show antitumour effects against many types of cancers such described (23,24). Cells grown under subconfluent conditions as acute myeloid leukaemia, breast and prostate cancers and were treated with VPA (0, 2 and 5mM). After 12 or 24 head and neck squamous cell carcinomas. The objective of the present study was to define the biological and therapeutic effects of VPA in treating SGC. Materials and methods Valproic acid. Valproic acid sodium salt (VPA; Sigma Aldrich Co., St. Louis, MO, USA) was dissolved in Dulbecco's phosphate-buffered saline (PBS) without Ca2+ or Mg2+ (DPBS; Sigma Aldrich) as a stock solution. For in vitro experiments, the VPA stock solution was diluted with the complete culture medium. For in vivo experiments, the VPA stock solution was supplemented in drinking water. Cell lines and cell culture. Two human SGC cell lines, HSY and HSG cells, were used in the present study. They are adenocarcinoma cell lines derived from the parotid gland and submandibular gland, respectively (20,21). These two cell lines produce tumours when subcutaneously inoculated into nude mice. They were maintained in Dulbecco's modified Eagle's medium (DMEM; Sigma Aldrich) supplemented with 10% fetal calf serum (FCS), 100 µg/ml streptomycin and 100 U/ml penicillin in a humidified atmosphere composed of 95% air and 5% CO2 at 37˚C. In vitro cell proliferation assay. The proliferation of SGC cells treated with VPA was assessed by MTT assay. Cells were seeded on 96-well plates (Falcon, Franklin Lakes, NJ, USA) at 2x103 cells/well in DMEM containing 10% FCS. Twenty-four hours later, cells were treated with various concentrations (0, 1, 2, 5 and 10 mM) of VPA for 2 and 4 days. After VPA treatment, a 10 µl aliquot of 5 mg/ml 3-(4,5-dimethylthiazol-2-yl)-2,5-di- phenyltetrazolium bromide (MTT) (Sigma Aldrich) was added to each well, and the cells were incubated for 4 h. The blue dye taken up by cells was dissolved in dimethyl sulphoxide, and the absorbance was measured with a microplate reader (Bio-Rad Laboratories, Hercules, CA, USA) at 540 nm. All assays were run in triplicate. Mice and in vivo study. BALB/c nude mice were purchased from Japan CLEA Inc. (Osaka, Japan). The mice were main- tained under pathogen-free conditions and were handled in accordance with the Guidelines for Animal Experimentation of Tokushima University. The experiments were initiated when the mice were 8 weeks of age and were performed as previ- ously described (23). Five million HSY cells were inoculated ONCOLOGY REPORTS 31: 1453-1458, 2014 1455 Figure 1. Phase-contrast micrographs of HSY cells treated with VPA. HSY cells were treated with 0, 2 and 5 mM of VPA for 24 h. The morphology of HSY cells was transformed from being cuboidal to being spindle-shaped in a dose-dependent manner. Original magnification, x40. A B Figure 2. Effects of VPA on SGC cell proliferation. Salivary gland cancer (SGC) cells were seeded at a concentration of 2x103 cells/well on 96-well plates. Twenty-four hours later, the cells were treated with various concentrations (0, 1, 2, 5 and 10 mM) of VPA for 2 and 4 days. In vitro cell proliferation was evaluated by the MTT assay. VPA inhibited the proliferation of SGC cells in a dose-dependent manner (A, HSY cells; B, HSG cells). Degenerated cancer cells were observed at a high concentration (10 mM) of VPA. *P<0.05, significant difference from the untreated control group. concentration (10 mM) of VPA. In particular, the HSY cells were most sensitive to the inhibitory effects of VPA on cell proliferation.
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