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Climacostol Inhibits Tetrahymena Motility and Mitochondrial Respiration

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Climacostol Inhibits Tetrahymena Motility and Mitochondrial Respiration Cent. Eur. J. Biol. • 6(1) • 2011 • 99–104 DOI: 10.2478/s11535-010-0100-7 Central European Journal of Biology Climacostol inhibits Tetrahymena motility and mitochondrial respiration Research Article Yoshinori Muto1,*, Yumiko Tanabe2, Kiyoshi Kawai2, Yukio Okano3, Hideo Iio4 1Department of Functional Bioscience, Gifu University School of Medicine, 501-1193 Gifu, Japan 2Department of Nutrition, Faculty of Wellness, Chukyo Women’s University, 474-0011 Ohbu, Japan 3Department of Molecular Pathobiochemistry, Gifu University Graduate School of Medicine, 501-1194 Gifu, Japan 4Department of Material Science, Graduate School of Science, Osaka City University, 558-8585 Osaka, Japan Received 08 July 2010; Accepted 01 October 2010 Abstract: Climacostol is a resorcinol derivative that is produced by the ciliate Climacostomum virens. Exposure to purified climacostol results in lethal damage to the predatory ciliate Dileptus margaritifer and several other ciliates. To elucidate the mechanism of climacostol toxic action, we have investigated the effects of this compound on the swimming behavior of Tetrahymena thermophila and the respiratory system of isolated rat liver mitochondria. When added to living T. thermophila cells, climacostol markedly increased the turning frequency that was accompanied by a decrease in swimming velocity and subsequently by cell death. Observations by DIC and fluorescence microscopy showed morphological alterations in climacostol treated T. thermophila, indicating that climacostol might exert cytotoxic action on this organism. In the experiment with isolated rat liver mitochondria, climacostol was found to inhibit the NAD-linked respiration, but had no apparent effect on succinate-linked respiration. This finding indicates that climacostol specifically inhibits respiratory chain complex I in mitochondria. The combination of results suggest that the inhibition of mitochondrial respiration may be the cytotoxic mechanism of climacostol’s defenses against predatory protozoa. Keywords: Climacostol • Apoptosis • Complex I • Mitochondria • Reactive oxygen species • Tetrahymena © Versita Sp. z o.o. 1. Introduction correlated to the unsaturation level of its aliphatic chain [3]. The complete molecular structure of climacostol was The heterotrich ciliate, Climacostomum virens, has determined as 1,3-dihydroxy-5-[(Z)-2’-nonenyl]benzene numerous cortical granules containing a cytotoxic and it was chemically synthesized [1,4]. On the basis compound called climacostol [1]. This compound is of its chemical structure, climacostol is classified as used for chemical defense against predators such as a resorcinolic lipid, and is widely detected in plants, the raptorial ciliate Dileptus margaritifer and its cytotoxic fungi, algae, and bacteria [5,6], but only in one animal activity has been assessed on several species of ciliates species (a marine sponge) and in a ciliated protozoan such as Didinium nasutum, Paramecium caudatum, [7]. Some observations clearly suggested participation and Blepharisma japonicum [2]. Recent observations of resorcinolic lipids in the modulation of the host- on various ciliated protozoa further revealed that the pathogen relationship in plants [5]. Until now, however, cytotoxicity level of climacostol appears to be inversely the physiological role of the resorcinolic lipids has not * E-mail: [email protected] 99 Climacostol inhibits Tetrahymena motility and mitochondrial respiration been fully clarified and little is known about the cytotoxic (25 mm × 50 mm) and a smaller coverslip (18 mm ×18 mm) mechanisms of climacostol on the target organisms. by introducing 10 μm diameter polystyrene beads into the Among the ciliates, Tetrahymena has been medium. This assembly was then mounted on an Olympus convenient for cell biology studies because several IX70 inverted microscope equipped with high-resolution species are easily grown axenically [8]. They possess DIC and epifluorescence optics. highly evolved cytoarchitecture as well as an intracellular messenger system regulating various cell functions 2.4 Digital image processing [9,10]. Its ultrastructure, cell physiology, development, Measurement of the motility pattern was initiated biochemistry, genetics and molecular biology have by transferring 50 μl aliquot of the cell suspension been extensively studied [11-15]. Moreover, the motile into a plastic petri dish (φ33mm) containing 0.4 ml behavior of Tetrahymena in response to external of 10 mM Mops/Tris (pH 7.2) inorganic saline chemical stimuli is easily assessed and has been solution with and without a test substance (the used as a measure of the biological activity of various final cell density, approximately 1×105 cells/ml). chemicals [16-18], making it a suitable model cell After rapid mixing of the medium, time-lapse images system for analysis of the cytotoxic mechanisms of were obtained with a C5985 video camera (Hamamatsu climacostol. In the present study, we have undertaken Photonics, Japan) in darkfield illumination using an a series of investigations into the mode of action of inverted microscope with a ×4 objective lens [18,20]. climacostol on Tetrahymena thermophila cells and its Video signals were digitized by a personal computer with effects on the respiratory chain of rat liver mitochondria. an LG-3 frame grabber (Scion, USA) and then converted Our results show that climacostol inhibits the motility of to TIFF format. The images were recorded every 0.1 s T. thermophila remarkably and induces morphological for 1 min after the cell suspension was added. For changes of the cell, being dependent at least in part quantitative analysis of the swimming pattern, sequential on mitochondrial function. A part of this work has been cell video images were subjected to image processing published in the Proceedings of the annual meeting of including filtering as well as binary (i.e. black and white the Japan Society of Protozoology [19]. only) transformation. Ten successive images of the same field were then added and converted to one fused image to show the swimming tracks of T. thermophila. All image 2. Experimental Procedures processing was performed using the public domain NIH Image program (developed at the U.S. National 2.1 Cell culture Institutes of Health and available on the Internet at Tetrahymena thermophila B1868(mating type II) was http://rsb.info.nih.gov/nih-image/). grown axenically at 25°C in 1% (w/v) proteose peptone containing 1% (w/v) yeast extract and 0.87% (w/v) 2.5 Mitochondrial preparation and glucose without shaking. Cells were harvested during the measurement of respiration mid-log phase of growth (5×105 cells/ml) by centrifugation, Rat liver mitochondria were prepared by the method of washed and resuspended to 1×106 cells/ml in 10 mM Schneider [21] using 0.25 M sucrose solution containing Mops/Tris (pH 7.2) containing 1 mM KCl, 1 mM NaCl and 0.5 mM EDTA and 10 mM Tris-HCl (pH 7.4). The 1 mM CaCl2 (inorganic saline solution). Cells were then mitochondrial respiration was measured using a Galvani- equilibrated for more than 30 min prior to measurement. type oxygen electrode. The reaction medium was essentially composed of 0.15 M KCl, 5 mM MgCl2, 1 mM EDTA and 2.2 Climacostol 20 mM Tris-HCl in a final volume of 2 ml (pH 7.4). Reaction Chemically-synthesized climacostol [1] was dissolved was initiated after saturating O2 in the reaction medium in ethanol (5 mg/ml) and stored protected from light at 30°C and was carried out at the same temperature. at −20°C until use. The solution was diluted with an Submitochondrial particles (SMP) were prepared from rat appropriate experimental medium at the time of the liver mitochondria according to the procedure of Ruzicka experiment. For each experiment, corresponding volume [22]. The oxygen uptake of SMP was measured by the of the vehicle ethanol was added and measurement was same method used for mitochondria. Reaction medium performed as control. was essentially composed of 0.15 M KCl, 5 mM MgCl2, 5 mM inorganic phosphate, 0.5 mM EDTA, and 20 mM 2.3 Differential interference contrast (DIC) and Tris-HCl in a final volume of 1.9 ml (pH 7.4). The reaction fluorescence microscopy was performed at 30°C. The protein concentration was T. thermophila cells equilibrated in inorganic saline solution determined by the method of Lowry et al. [23], using bovine were slightly compressed between a large coverslip serum albumin as the standard protein. 100 Y. Muto et al. 3. Results of incubation in a solution of climacostol with a final concentration of 21 μM, T. thermophila cells initially 3.1 Motility changes of Tetrahymena lost their shape and became spherical (Figure 2A, thermophila induced by climacostol part b). Some cells were highly abnormal, exhibiting By regulating the frequency and direction of ciliary beat, cell lysis in which pellicle membranes were ruptured T. thermophila changes swimming patterns in response (Figure 2A, part c). Since almost all the cells became to various environmental stimuli. When observing the immobilized and spherical after exposure to 21 μM motility pattern of T. thermophila in darkfield illumination climacostol for 5 minutes, there might be no surviving with a microscope, it consists of smooth tracks (runs) cells in this condition. In Tetrahymena and related interrupted randomly by a turn which alters the direction ciliates, many of the mitochondria are located in the of motion (Figure 1A, part a). Incubating T. thermophila in cortex and are lined up parallel to the ciliary rows [13]. climacostol (21 μM) immediately increased
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