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Potent Inhibitory Effects of D-Tagatose on the Acid Production and Water-Insoluble Glucan Synthesis of Streptococcus Mutans GS5 in the Presence of Sucrose

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Potent Inhibitory Effects of D-Tagatose on the Acid Production and Water-Insoluble Glucan Synthesis of Streptococcus Mutans GS5 in the Presence of Sucrose View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Okayama University Scientific Achievement Repository Acta Med. Okayama, 2015 Vol. 69, No. 2, pp. 105ﾝ111 CopyrightⒸ 2015 by Okayama University Medical School. Original Article http ://escholarship.lib.okayama-u.ac.jp/amo/ Potent Inhibitory Effects of D-tagatose on the Acid Production and Water-insoluble Glucan Synthesis of Streptococcus mutans GS5 in the Presence of Sucrose Daijo Sawadaa,b＊, Takaaki Ogawaa, Minoru Miyakea, Yoshinori Hasuib, Fuminori Yamaguchic, Ken Izumorid, and Masaaki Tokudac,d Departments of aOral and Maxillofacial Surgery and cCell Physiology, Faculty of Medicine, Kagawa University, Miki, Kagawa 761-0793, Japan, bHasui Dental Family Clinic, Kagawa 761-0704, Japan, dRare Sugar Research Center, Miki, Kagawa 761-0793, Japan We examined and compared the inhibitory effects of D-tagatose on the growth, acid production, and water-insoluble glucan synthesis of GS5, a bacterial strain of Streptococcus mutans, with those of xylitol, D-psicose, L-psicose and L-tagatose. GS5 was cultured for 12h in a medium containing 10ｵ (w/v) of xylitol, D-psicose, L-psicose, D-tagatose or L-tagatose, and the inhibitory effect of GS5 growth was assessed. Each sugar showed different inhibitory effects on GS5. Both D-tagatose and xylitol significantly inhibited the acid production and water-insoluble glucan synthesis of GS5 in the presence of 1ｵ (w/v) sucrose. However, the inhibitory effect of acid production by D-tagatose was significantly stronger than that of xylitol in presence of sucrose. Key words: Streptococcus mutans, D-tagatose, xylitol, acid production, water-insoluble glucan he definition of ʻrare sugarsʼ is monosaccha- the most extensively examined rare sugar, including T raides and their derivatives that are not com- anti-diabetes and anti-obesity effects [4-7]. monly found in nature. The biological effects of rare The Gram-positive bacterium Streptococcus mutans sugars have not been investigated in detail, partly plays one of the most important roles in the develop- because they are difficult to obtain and partly because ment of dental caries, which is the most common oral their synthesis is laborious, time-consuming and inef- infectious disease in the world [8]. As part of the ficient [1, 2]. Kagawa University Rare Sugar mechanism of dental caries, S. mutans adheres to an Research Center established a simple method to pro- acquired pellicle formed on the tooth surface, synthe- duce rare sugars in large amounts from inexpensive sizes glucan by the action of glucosyltransferases (gtf), D-glucose and D-fructose [3]. Most types of rare and promotes the formation of dental plaque [9]. In hexoses are now available for experiments to deter- the dental plaque, S. mutans produces organic acids as mine their functional characteristics. For example, a result of carbohydrate metabolism. These organic various favorable effects on human health have been acids induce demineralization of the tooth surface, reported for D-psicose, a non-calorie sweetener and resulting in dental caries [10]. Xylitol is a well-known sugar that prevents dental Received August 5, 2014 ; accepted November 27, 2014. ＊Corresponding author. Phone : ＋81ﾝ87ﾝ891ﾝ2227; Fax : ＋81ﾝ87ﾝ891ﾝ2228 Conflict of Interest Disclosures: No potential conflict of interest relevant E-mail : [email protected] (D. Sawada) to this article was reported. 106 Sawada et al. Acta Med. Okayama Vol. 69, No. 2 caries [11]. However, the preventive effect of xylitol Rare Sugar Research Center of Kagawa University has been shown to be remarkably inhibited by the (Kagawa, Japan). The TY medium was prepared from existence of another monosaccharide that can be 1.4ｵ tryptone and 0.8ｵ yeast extract. Tryptone, metabolized by S. mutans [12]. In the present study, yeast extract and other chemicals were purchased we examined the effects of 4 rare ketohexoses from Wako Pure Chemical Industries (Tokyo, Japan). (D-psicose, L-psicose, D-tagatose, and L-tagatose) on We found that it was difficult to reveal the different the growth, acid production and water-insoluble effects of each rare sugar with a rich-sugar medium, glucan synthesis of S. mutans. We used xylitol, a and thus we use a low-sugar TY medium. 5-carbon polyalcohol, as a control monosaccharide Bacterial strains and culture conditions. S. since xylitol is known to have inhibitory effects on the mutans GS5, a clinically isolated strain commonly growth, acid production and water-insoluble glucan used in dental research [13], was kept at －80℃ synthesis of S. mutans. The applications of xylitol until use. GS5 was grown in TY medium at 37℃ in includes hygiene, nutraceutical formulations and static culture in air-sealed tubes for 24h, and it was products such as anti-cariogenic gums. It is roughly as diluted with TY medium at an optical density of sweet as sucrose with 33ｵ lower calories. OD600 ＝0.3. Based on the results of previous studies, Fig. 1 shows the structural differences of four we selected the static culture because there was no rare sugars including D-fructose and xylitol. D-psicose difference between the static culture and the anaerobic and D-tagatose are C-3 and C-4 epimers of D-fructose, culture and because a caries induction test was possi- respectively (Fig. 1). L-psicose and L-tagatose are ble with the static culture [14]. Two mL of TY the optical isomers of D-psicose and D-tagatose, medium containing 200mg (10ｵw/v) xylitol, D-psicose, respectively. All of these rare monosaccharides can L-psicose, D-tagatose or L-tagatose was prepared and be synthesized according to the production strategy of divided into two 1-mL solutions in the tubes. Izumoring, and D-psicose can be produced from Some of the rare sugars show insolubility when the D-fructose by the enzymatic reaction of D-tagatose 3 concentration is greater than 15ｵ. In addition, most epimerase [3]. D-tagatose is very similar in texture of the soft drinks available to the public contain less to sucrose and is 92ｵ as sweet, but with only 38ｵ of than 10ｵ (10g/100mL solution) sugar [15]. We the calories and with a very low glycemic index. The therefore decided to use various sugars at 10ｵ con- properties and functions of L-psicose and L-tagatose centration in the present experiment. Ten mg of have hardly been researched because of their limited sucrose (1ｵw/v) was added to one 1-mL solution, and availability. The present study is the first to examine no sucrose was added to the other 1-mL solution. the effects of these rare monosaccharides on a typical To start the growth of GS5, 50µL of the bacterial bacterial strain of S. mutans, GS5. solution was inoculated into the TY medium, and the tubes were sealed by Parafilm (Pechiney Plastic Materials and Methods Packaging Co., Batavia, IL, USA) for culture at 37℃. The optical density at 600nm was measured at Reagents. Rare sugars were supplied by the 4, 8, 12, and 20h after inoculation. The pH and the CH2OH CH2OH CH2OH CH2OH CH2OH C=O C=O C=O C=O C=O CH2OH OH C H H C OH OH C H OH C H H C OH H C OH H C OH H C OH OH C H OH C H H C OH OH C H H C OH H C OH OH C H H C OH OH C H H C OH CH2OH CH2OH CH2OH CH2OH CH2OH CH2OH D-fructose D-psicose L-psicose D-tagatose L-tagatose xylitol Fig. 1 Chemical structures of the monosaccharides used in this study. April 2015 Inhibitory Effects of D-tagatose on Streptococcus mutans GS5 107 water-insoluble glucan production were measured at the 20th hour. The turbidity in D-tagatose was the 12h. least among the sugars and also lower than xylitol Bacterial growth assay. Bacterial growth throughout the experiment, to the 20th hour. was assessed by measuring the turbidity of the solu- GS5 grew rapidly in the control TY medium, tion. In the presence of sucrose, GS5 formed many which contained no monosaccharide. The inhibition of bacterial aggregates containing insoluble glucan that GS5 growth by xylitol, D-psicose, L-psicose, D-tagatose were difficult to homogenously dissolve. Thus, turbid- and L-tagatose groups was significant (p＜0.05) com- ity measurement was performed only for the groups pared to the control group. Only D-tagatose had a without sucrose supplementation at 4, 8, 12 and 20h significantly stronger inhibition of bacterial growth after inoculation. To determine the solution turbidity, than xylitol (p＜0.05). optical density was measured using spectrophotometry Decrement of pH. The decrease in pH along at 600nm (Gene Quant Pro, Amersham, Tokyo, with bacterial growth in the control medium and in the Japan). xylitol-, D-psicose-, L-psicose-, D-tagatose- and L- Measurement of pH. The ability of GS5 to tagatose-containing media was measured in the absence produce acid at 12h after inoculation was evaluated by and presence of 1ｵ sucrose (Fig. 3). In the absence measuring the pH of the solution using the CHECKER of sucrose, only xylitol significantly inhibited the pH pH tester (Hanna Instruments, Tokyo, Japan). The decrement. It the others showed only a tendency to initial pH of the TY medium in the presence of various inhibit the pH decrement. sugars was 7.4. In the presence of sucrose, all of the sugars sig- Measurement of water-insoluble glucan. nificantly inhibited the pH decrement compared to the The production of water-insoluble glucan was mea- change in the control group pH (p＜0.05). Interestingly, sured at 12h after inoculation. Water-insoluble glucan both D-tagatose and D-psicose showed significantly and bacteria lumps were collected by centrifugation at stronger inhibition of pH reduction compared to xyli- 3,500×g for 10min.
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