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Mechanosensitive Ca2+ Release from Intracellular Stores in Nitella Flexilis

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Mechanosensitive Ca2+ Release from Intracellular Stores in Nitella Flexilis Plant Cell Physiol. 42(4): 358–365 (2001) JSPP © 2001 Mechanosensitive Ca2+ Release from Intracellular Stores in Nitella flexilis Munehiro Kikuyama 1, 3 and Masashi Tazawa 2, 4 1 Biological Laboratory, The University of the Air, 2-11 Wakaba, Mihama-ku, Chiba, 261-8586 Japan 2 Department of Applied Physics and Chemistry, Fukui University of Technology, Gakuen, Fukui, 910-8505 Japan ; We found previously that the cytoplasmic drop isolated cytoplasm that had been squeezed out from an internodal cell from internodal cells of Nitella flexilis releases Ca2+ in of N. flexilis was mixed with a hypotonic solution (Kikuyama response to hypotonic treatment and named the phenome- et al. 1995). Since HICR in the cytoplasmic drop was greatly 2+ non hydration-induced Ca release (HICR). The HICR is inhibited by a water channel inhibitor HgCl2, water channels in assumed to be a result of activation of Ca2+ permeable chan- the membrane of Ca2+ stores are assumed to be involved in nels in the membrane of Ca2+ stores in a stretch-activated HICR (Kikuyama and Tazawa 1998). Thus, a possible mecha- manner. To prove this idea, mechanical stimulus was nism of HICR may be as follows. Rapid hydration of the cyto- applied to the drop by means of shooting isotonic/hypnotic plasm lowers the osmotic pressure of the cytoplasm, which medium or silicon oil into the drop, or compressing the then results in osmotic expansion of putative Ca2+ stores. drop. All these mechanical stimuli induced a rapid increase Osmotic expansion of the stores necessarily stretches the mem- in the Ca2+ concentration of the drop. The chloroplast frac- brane and causes efflux of Ca2+ from the stores. If this is the tion isolated from the cytoplasmic drop released Ca2+ on case, the ion channel in the membrane of the stores would be a compression, while the chloroplast-free cytoplasm did not. stretch-activated one. Suppression of HICR by HgCl2 can be In Chara corallina, the cytoplasmic drop, which shows a accounted for in terms of inhibition of osmotic expansion of very weak HICR, also responded weakly to the mechanical the store membrane (Kikuyama and Tazawa 1998). stimulus, but the chloroplast fraction was inert. When chlo- The present study was undertaken to confirm the above roplasts from Chara were added to the chloroplast-free assumption that mechanical stimulation of the cytoplasmic 2+ cytoplasm of N. flexilis, the cytoplasm recovered the mecha- drop induces Ca release from the stores through activation of noresponse.Starchgrainswereaseffectiveaschloroplasts. mechanosensitive ion channels. The data indicate that Ca2+ permeable channels in the membrane of Ca2+ stores in N. flexilis are really mechano- Materials and Methods sensitive. Plant materials 2+ The materials, N. flexilis and Chara corallina, were cultured in Key words: Aequorin — Ca store — Chloroplast — Hydra- an aquarium filled with tap water under 12 h illumination a day with 2+ tion induced Ca release (HICR) — Nitella flexilis —Mech- two 20 W fluorescent lamps placed about 10 cm above the water sur- anosensitive ion channel. face. Temperature was kept at about 25°C with a thermostat. Abbreviations: ER, endoplasmic reticulum; EGTA, ethylenegly- Isolation of cytoplasm from internodal cells col bis(2-aminoethylether)-N,N,N¢,N¢-tetraacetic acid; D[Ca2+], increase Isolation of the cytoplasm was carried out in the same manner as in Ca2+ concentration; HICR, hydration-induced calcium release; Osm, described in the previous paper (Kikuyama and Tazawa 1998). Briefly, osmolar; PM, photomultiplier. internodal cells, isolated from neighboring internodal and leaf cells, were kept in an artificial pond water (APW; 0.1 mM each of KCl, NaCl and CaCl2) for a day, then immersed in 10 mM KCl for several hours or more to make cells inexcitable to mechanical stimulation. The D 2+ KCl treatment was essential to avoid excitation-induced [Ca ]c that D 2+ Introduction interferes with measurement of [Ca ]c caused by HICR (Hayama and Tazawa 1978, Hayama et al. 1979). In order to remove Ca2+ from the vacuole, the vacuolar sap was In internodal cells of Nitella flexilis, transcellular osmosis replaced with the isotonic perfusion medium composed of 5 mM induces a transient increase in the concentration of cytoplas- EGTA, 10 mM PIPES (pH 7 with KOH), 6 mM MgCl2 and 300 mM 2+ 2+ 2+ mic free Ca ([Ca ]c) on the endosmosis side (Tazawa et al. sorbitol (345 mOsm). With this procedure, possible release of Ca 2+ D 2+ from fragments of the central vacuole is completely neglected, even if 1994, Tazawa et al. 1995). The increase in [Ca ]c ( [Ca ]c) was assumed to be a result of Ca2+ release from intracellular they were formed during the isolating procedure and remained in the cytoplasmic drop. Then the cell content was squeezed out onto a sheet stores that is evoked by a rapid hydration of the cytoplasm on of Parafilm (American National Can, Greenwich, CT, U.S.A.) by using the endosmosis side (Tazawa et al. 1995). The hydration- forceps (Fig. 1). The isolated drop will be called simply cytoplasmic induced calcium release (HICR) was also observed when the drop hereafter. 3 Present address: Department of Biology, Faculty of Science, Niigata University, Niigata, 950-2181 Japan. 4 Corresponding author: E-mail, [email protected]; Fax, +81-77-524-9221. 358 Mechanosensitive Ca2+ Release in Nitella 359 Fig. 1 Method for isolating cytoplasmic drop. (1) Vacuolar per- fusion. An internodal cell (cell) was placed on a Plexiglas bench (B) Fig. 2 A method for inducing HICR and/or mechanosensitive and the vacuolar sap was removed and replaced with isotonic per- response in cytoplasmic drop (Drop) placed in silicone oil (oil). (a) fusion medium (PM) by vacuolar perfusion. (2) Squeeze out. Cyto- Injection of perfusion medium. (b) Shooting of a drop of silicone oil. plasm concomitant with the perfusion medium was squeezed out onto A silicone oil dorp was shot into the cytoplasmic drop using a pump a sheet of Parafilm (PF) using forceps (F). (3) Put in silicone oil and (Piezo pump). (c) Compression of cytoplasmic drop. Compression and add aequorin. Two ml of the cytoplasmic drop (drop) was placed in sil- decompression were performed by horizontal movements of a Plex- icone oil and added with aequorin by using a glass micropipette (p). iglas rod connected to a piezoelectric device (Piezo Actuator). The specimen containing aequorin was placed just over the photomul- tiplier tube, and light emission from aequorin was measured. fch-aequorin, 150 mM KCl, 6 mM MgCl2, 0.15 mM EGTA, 0.5 mM PIPES (pH 7.0 with KOH) was added to the specimen (Fig. 1). Preparation of chloroplast fraction and chloroplast-free fraction Although the amount of the aequorin solution added was in the order The isolated cytoplasmic drop from two internodal cells was cen- of 100 pl, the actual amount was significantly changed in each meas- trifuged at 125´g for 5 s using a centrifuge (5415C, Eppendorf, Ham- urement partly because we had an impression that the cellular sensitiv- burg, Germany). The supernatant was isolated from the precipitate. ity of Ca2+ release fluctuated seasonally. This is a major reason why The supernatant was a mixture of cytoplasm and the isotonic per- the measured photomultiplier current are largely different in each fig- fusion medium and contained no chloroplast. It will be named simply ure. as chloroplast-free fraction hereafter. The precipitate (about 2 ml) containing mostly chloroplasts was Measurement of ,[Ca2+] upon hypotonic treatment and mechanical resuspended in 20 ml perfusion medium, centrifuged (125´g,30s)and stimuli the supernatant was discarded. After two rinses, precipitated chloro- The cuvette with specimen was placed in a dark box equipped plasts were dispersed in 4 ml perfusion medium. The suspension will with a photomultiplier tube (PM) (R1924P, Hamamatsu Photonics, be named simply as chloroplast fraction. Hamamatsu, Japan) in the same manner as described in the previous Increase in the Ca2+ concentration (D[Ca2+]) in response to vari- paper (Kikuyama and Tazawa 1998). ous stimuli was measured in isolated cytoplasmic drops, chloroplast- The HICR of each specimen was induced by applying a hypot- free fractions and chloroplast fractions as increases in light emission onic medium (the same ionic composition as the isotonic perfusion from aequorin added in each fraction. Two ml of specimen was placed medium but lacking sorbitol; about 45 mOsm) from a microsyringe in a cuvette and covered with silicone oil (10 cs; KF-96-10CS, Shin- (1705, Hamilton, U.S.A.) which was driven by a motor (CYLINOID, Etsu Chemical, Tokyo, Japan). Then aequorin solution (0.5 mg ml–1 CA-2, Kamaden, Tokyo) (Fig. 2a). 360 Mechanosensitive Ca2+ Release in Nitella Fig. 4 Transient increase in PM current of aequorin light emission in Fig. 3 Transient increase in PM current of aequorin light emission in response to a shot of silicone oil. (a) A silicone oil drop was shot at response to a jet of isotonic (a) or hypotonic medium (b). In (b) the time zero. The resulted PM current shows a single peak. (b) First, a sil- first spike is followed by a slower and long-lasting one. icone oil drop was shot at time zero and then a jet of hypotonic medium was applied at a time of 8.3 s (arrow). The increase in PM current is composed of two processes, the first rapid increase and the second slower one. Three types of mechanical stimuli were used. (1) Injection of perfusion medium. About 4 ml of either isotonic or hypotonic per- fusion medium was injected into the cytoplasmic drop within 2 s from Results a microsyringe (Fig. 2a). (2) Shooting of a drop of silicone oil. A drop m of silicone oil (about 0.3 l) was shot into the cytoplasmic drop by Injection of perfusion medium into cytoplasmic drop using a pump (Piezo pump; NS-02D, Nippon Keiki Works Ltd., Tokyo, Japan) driven by a piezoelectric device (Fig.
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