Localisation of intracellular calcium stores in the striated muscles of the jellyfish Polyorchis penicillatus: possible involvement in excitationcontraction coupling
Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9 and Bamfield Marine Station, Bamfield, British Columbia, Canada V1R 1B
*Author for correspondence (e-mail: aspencer{at}bms.bc.ca)
Accepted July 31, 2001
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Summary |
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Key words: calcium stores, excitationcontraction coupling, jellyfish, Polyorchis penicillatus, caffeine, CaATPase.
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Introduction |
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The sarcoplasmic reticulum of striated muscle is an intracellular tubular network with functionally discrete units that respond differently to various types of cellular stimulation (Golovina and Blanstein, 1997). The terminal cisternae of the sarcoplasmic reticulum have been identified as the likely calcium release and storage sites, and contain the calcium release channels, ryanodine receptors (Winegrad, 1965; Inui et al., 1987a; Inui et al., 1987b; Lai et al., 1988) and high-capacity and low-affinity calcium-binding proteins such as calsequestrin (Meissner et al., 1973; Jorgensen et al., 1983). Calcium uptake by the sarcoplasmic reticulum is mediated by Ca2+/Mg2+-ATPase pumps, which are a family of transmembrane proteins (Carafoli, 1991) with each pump molecule transporting two calcium ions from the cytoplasm into the lumen of the SR during each catalytic cycle at the expense of a single molecule of ATP (Tada et al., 1982; Inesi, 1987).
Myoepithelial cells in cnidarians represent some of the most primitive types of muscle (Prosser, 1982), and are formed by an apical soma attached by a narrow neck to several contractile feet which are aligned in parallel arrays. Myoepithelial cells of polyps and most postural muscles in medusae are non-striated, while the subumbrellar myoepithelial cells of medusae have striated myonemes (Chapman et al., 1962; Fautin and Mariscal, 1991; Thomas and Edwards, 1991). The myofibrils of Polyorchis penicillatus, like other hydromedusae (Spencer and Satterlie, 1981) contain thick and thin myofilaments arranged in a hexagonal array of one thick filament surrounded by six thin filaments (Singla, 1978a; Singla, 1978b), and are joined end-on by desmosomes and laterally by gap junctions (Spencer, 1979). Despite their structural similarity to other striated muscles, little is known about the mechanism of excitationcontraction coupling in cnidarian striated muscle. In this study, we present data on muscle contraction to show that calcium released from intracellular calcium stores plays a role in the contraction of jellyfish swimming muscle and we also localise putative calcium stores by cytochemical labelling of Ca2+-ATPase and calcium.
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Materials and methods |
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Field stimulation of muscle strips
Preliminary studies indicated that muscle strips from the subumbrella (bell lining) and velum had similar pharmacologies. Due to the thickness and elastic property of mesoglea in the bell region, recordings from muscle strips obtained from this region were extremely variable and it was difficult to measure contractile amplitude. Therefore, only muscle strips from vela were used in this study. The velum consists of a thin lamina of mesoglea covered on the subumbrella side by a single layer of striated muscle cells, while the epithelium on the opposite surface has occasional strands of smooth muscle that are incapable of repetitive phasic contraction. The vela of medusae, anaesthetized in 1:1 isotonic MgCl2 (0.33 mol l1) and artificial sea water (ASW; NaCl 376 mmol l1, Na2(SO4) 26 mmol l1, MgCl2 41.4 mmol l1, CaCl2 10 mmol l1, KCl 8.5 mmol l1 and N-2-hydroxy-ethylpiperazine-N'-2-ethanesulphonic acid (Hepes) hemisodium salt 10 mmol l1; pH 7.5), were excised so as to provide continuous strips of maximal width. Greater width ensured that tension was easily measured; however this did not compromise aerobic contraction as the tissue thickness was constant. To avoid any contamination by nervous tissue, each velar strip was bisected lengthwise into two strips and only strips free from nerve-ring tissue were used in the study. Muscle fibres ran parallel to the long axis of the velar strips. Vela with widths between 23 mm and lengths between 2 and 2.5 cm were used in this study. The free ends of each velar strip were pinned to the Sylgard base of a 35 mm Petri dish containing a pair of embedded Ag/AgCl2 stimulating electrodes connected to a Grass S44 stimulator. The velar strip ran between the two stimulating electrodes and around a small hook attached to an isometric force transducer (Kent Scientific Corporation). The stimulation voltage was determined by increasing the voltage until there was no increase in the amplitude of contraction at the stimulation frequency of 0.1 Hz. The voltages used usually were between 30 and 40 V. The frequency of stimulation varied from 0.1 to 0.8 Hz, with each square pulse having a duration of 30 ms. The rate of perifusion was controlled by a peristaltic pump at 1.5 ml min1 and the perifusate was removed by a vacuum pump. All perifusion solutions were kept at 1214°C during experiments by running the perifusion tubing through an ice bucket. The transduced tension was recorded on a digital Dash-IV pen-recorder (Astro-Med Inc.). The amplitude of contractile tension for each condition (control, drug effect and washed) was calculated by averaging ten contractions when the contraction was stabilised from each preparation. Caffeine was dissolved in the ASW to a final concentration of 10 mmol l1.
Localisation of Ca2+-ATPase
Strips of the subumbrellar muscle sheet were removed from jellyfish by a pair of forceps and cut into pieces approximately 2 mmx3 mm. The muscle pieces were washed and relaxed in Ca2+-free ASW and then fixed with 2 % paraformaldehyde and 0.25 % glutaraldehyde in cacodylate-buffered saline at pH 7.8 (sodium cacodylate/HCl 100 mmol l1, NaCl 300 mmol l1, KCl 10 mmol l1) for 30 min on ice. Glutaraldehyde was added to provide better preservation of the ultrastructure (Ueno and Mizuhira, 1984). After three washes (30 min each) in ice-cold cacodylate-buffered saline and two brief rinses in glycine/NaOH buffer (250 mmol l1, pH 9.0), tissues were incubated at either 12°C or 37°C for 45 min in a solution containing glycine/NaOH buffer 250 mmol l1, pH 9.0, ATP-Na 3 mmol l1, CaCl2 10 mmol l1, MgCl2 5 mmol l1, lead citrate 4 mmol l1 (Ando et al., 1981). Levamisole was added to a final concentration of 8 mmol l1 to exclude any contribution of non-specific alkaline phosphatase to ATP hydrolysis (Van-Noorden and Jonges, 1987). Ouabain (final concentration 10 mmol l1) was added to the incubation medium to inhibit Na+-K+-ATPase (Maggio et al., 1991). To examine ATP-, calcium- and substrate-dependence of the cytochemical reaction, the following controls were performed, with incubation in ATP-free medium, Ca2+-free medium with 10 mmol l1 EGTA, or lead citrate-free medium. After incubation, samples were rinsed sequentially in glycine buffer and cacodylate-buffered saline, post-fixed in 1 % osmium tetroxide in cacodylate-buffered saline for 1 h, and then processed for conventional TEM examination. Sections of 7090 nm thickness were collected on nickel grids and examined without staining.
Ultrastructural localisation of calcium
Calcium stores were localised using the method of Probst, 1986. Tissue samples were fixed with 4 % paraformaldehyde and 2 % glutaraldehyde in 0.1 mol l1 phosphate buffer (pH 7.4) for 2 h at 4°C and post-fixed in 1 % osmium tetroxide and 2.5 % potassium dichromate in 0.1 mol l1 phosphate buffer at 4°C for 24 h. After incubation, samples were rinsed in phosphate-buffered saline then processed for conventional TEM examination. Sections of 7090 nm thickness were examined without staining.
Electron energy-loss spectroscopy
Unstained, ultrathin sections 3050 nm thick from tissues prepared for calcium localisation (see above) were used for electron energy-loss spectroscopy (EELS) using an energy-filtering transmission electron microscope (EM 902, Zeiss, Germany) and examined at an accelerating voltage of 80 kV. The inelastically scattered electrons with element-specific energy losses were used to obtain high-resolution imaging of calcium distribution in the sections. For calcium element mapping, energy-filtered images (energy width 20 eV) were recorded above and below the edge of electron absorption specific for calcium (CaL2,3 edge 346 eV) at 355 eV and 330 eV, respectively. The image taken at 330 eV served as a reference image for background levels. Net calcium distribution images were obtained by computer-assisted image processing of the difference between images taken at 355 and 330 eV.
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Results |
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Ultrastructural localisation of Ca2+-ATPase
Fig. 2 shows the ultrastructure of the swimming muscle where each cell is separated into a somal region and a myofibrillar region attached to the mesoglea. As previously reported (Singla, 1978b; Spencer, 1979), no T-tubular structures have been observed in P. penicillatus myofibrils; however, several membrane-bound vesicles in the sub-sarcolemmal cytoplasm were found close to contractile filaments. The distribution of these vesicles did not show any specific pattern. To establish if these sub-sarcolemmal vesicles are indeed sarcoplasmic reticulum and possibly involved in excitationcontraction coupling in swimming muscle cells, we used a cytochemical method (Ando et al., 1981) to test the presence of Ca2+-ATPase activity in these vesicles. When tissue was incubated in medium containing calcium, magnesium ions and ATP, an electron-dense precipitate of lead phosphate indicated the presence of Ca2+-ATPase activity. We found labelling in somal regions, such as the nucleus (Fig. 3A), the Golgi apparatus (Fig. 3B), vesicles of the endoplasmic reticulum and the lateral and apical plasma membranes (Fig. 3C). Precipitates on the outer side of these latter membranes presumably arose from non-specific ecto-ATPase activity (Ogawa et al., 1986: Nasu and Inomata, 1990).
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Ultrastructural localisation of calcium using dichromate precipitation andelectron energy loss spectroscopy
We also used potassium dichromate precipitation to indicate the presence of calcium stores (Probst, 1986). This histochemical method localizes loosely bound calcium and hence indicates calcium-binding sites. In somata, electron dense precipitates (EDPs) were found in the nucleus, mitochondria, the inner surface of the plasma membrane and sarcoplasmic reticulum-like vesicles (Fig. 4A,B). EDPs were also found in sub-sarcolemmal vesicles (Fig. 4C,D), and lining the inner side of the sarcolemma (Fig. 4D). Fine EDPs were also found in the mesoglea adjacent to myofibrils.
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Discussion |
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The sarcoplasmic reticulum in striated muscle can be elaborate, as in vertebrate skeletal muscle, where SR and T-tubules form triads that are precisely positioned above the Z line in each sarcomere (Fawcett, 1986). In cases like this, muscle contraction is completely dependent on calcium released from sarcoplasmic reticulum. At the other extreme, where a sarcoplasmic reticulum is absent, such as the striated muscles of the tunicate Doliolum nationalis, muscle contraction depends on calcium influx through the sarcolemma (Bone, 1997). In other striated muscles showing varying degrees of development of the sarcoplasmic reticulum, including vertebrate cardiac and invertebrate muscles, calcium influx is essential for muscle contraction and triggering the release of calcium from sarcoplasmic reticulum. Thus, it appears that the requirement for extracellular calcium influx for muscle contraction is inversely correlated with the development of the sarcoplasmic reticulum (Bers, 1991; Ashley et al., 1993; Palade and Györke, 1993; Paniagua et al., 1996).
Caffeine was applied to determine whether calcium stores were directly involved in mediating contraction and in producing the forcefrequency relationship. In most tissues, caffeine empties intracellular stores by making the store leaky to calcium or increasing the open probability of calcium releasing channels (Weber and Herz, 1968; Rousseau et al., 1988). In our experiments, caffeine increased the amplitude of the first few contractions (Fig. 1C). This could be due to caffeine sensitising myofilaments to calcium (Wendt and Stephenson, 1983), or to the sensitisation of calcium releasing channels treated with caffeine (Herrmann-Frank et al., 1999). After the initial facilitated contractions, caffeine produced a reversible inhibitory effect; it reduced the steady-state peak tension by 75 % at 0.1 Hz and 50 % at 0.8 Hz, and abolished the progressive tension increase that normally accompanies increased stimulation frequency (Fig. 1) (Lin and Spencer, 2001). These results indicate the presence of caffeine-sensitive calcium stores. However, caffeine did not evoke any contraction or contractures when applied alone without field stimulation. One possible explanation could be that the amount calcium released from the calcium stores alone was not enough to induce contraction or the tension developed was below threshold for the transducer. Ryanodine is known to be an effective channel blocker for caffeine-sensitive calcium stores (Winegrad, 1965; Inui et al., 1987a; Inui et al., 1987b; Lai et al., 1988); however, no inhibitory effects of ryanodine at 100 µmol l1 were observed during field stimulation of jellyfish striated muscles (data not shown). This raised the possibility that the inhibitory effects of caffeine we observed were non-specific blocking of voltage-gated calcium channels due to the high concentration of caffeine (10 mmol l1). Alternatively, the calcium releasing channels on caffeine-sensitive stores in jellyfish muscles could not be blocked by ryanodine.
In vertebrate striated muscles a substantial portion of stored calcium resides in the sarcoplasmic reticulum (Bers, 1991). In large diameter muscle cells, however, these stores may be distant from the external plasma membrane, which provides the initial influx of external Ca2+ to trigger calcium release. To ensure efficient triggering of calcium-induced calcium release, larger muscle cells have T-tubules that are invaginations of the plasma membrane, to bring this triggering signal rapidly to Ca2+ stores deep within the muscle. T-tubules are specialized to provide the external Ca2+ signal since their membranes have a high density of voltage-gated calcium channels (Carl et al., 1995). Small muscle cells, such as those in frog and lizard hearts, however, do not posses T-tubules and all compartments of the sarcoplasmic reticulum are relatively close to the external plasma membrane (Fabiato, 1982; Anderson et al., 1989; McLeod et al., 1991). T-tubules have never been observed in electron micrographs of P. penicillatus swimming muscle, presumably because there is only one layer of myofibrils, and each is about 2 µm in diameter, thereby positioning the contractile apparatus close to the triggering calcium signal from the plasma membrane (Singla, 1978b; Spencer, 1979) (this study).
At least three characteristics are necessary for an intracellular compartment to act as a calcium store involved in muscle contraction: (1) the presence of membrane pumps to replenish Ca2+ in the store; (2) calcium-release channels, which release calcium into the cytoplasmic space; and (3) calcium-binding proteins, which bind calcium in the store. As the nature of calcium-releasing channels in jellyfish is not known, we chose to map Ca2+-ATPase activity and demonstrate the presence of calcium by using histocytochemical methods to identify possible calcium stores. We used an enzyme cytochemical method to map the activity of Ca2+-ATPase ultrastructurally, since this method has been used to demonstrate Ca2+-ATPase activity in a wide variety of animal tissues, including marine invertebrates (Maggio et al., 1991; Cario et al., 1996). Ca2+-ATPase is known to participate in sequestering calcium into stores as well as pumping calcium into extracellular space (Carafoli, 1991). At least two types of Ca2+-ATPase have been identified; one is located on the sarcolemma or plasmalemma and the other type is located on sarcoplasmic reticulum (Carafoli, 1991). The method used in this study does not distinguish between these two types of Ca2+-ATPases, nor any non-specific ecto-ATPase activity (Ogawa et al., 1986; Nasu and Inomata, 1990). This latter activity is characterised by its location, which is at the outer surface of the plasma membrane (Ando et al., 1981).
The plasmalemmal Ca2+-ATPase functions to remove calcium from intracellular spaces during the relaxation phase of the muscle contraction cycle (Carafoli, 1991). The sarcolemmal region of P. penicillatus swimming muscle is more heavily labelled by Ca2+-ATPase specific precipitates than the apical region. This polarized distribution of Ca2+-ATPase activity is to be expected and parallels the functional polarization of the cells into somal and contractile compartments. A polarised distribution of Ca2+-ATPase has been reported for vertebrate epithelium, pancreatic and salivary gland cells, photoreceptors (Seguchi et al., 1982; Lee et al., 1997; Krizaj and Copenhagen, 1998) and crustacean posterior caecal epithelium (Meyran and Graf, 1986). Plasmalemmal Ca2+-ATPase has been localised to the caveolae or uncoated plasma membrane invaginations in mouse endothelial cells, smooth muscle cells, cardiac muscle cells, epidermal keratocytes and mesothelial cells by using a specific antibody generated against erythrocyte membrane Ca2+-ATPase (Fujimoto, 1993). Although we did not see caveolae-like structures in the sarcolemma, the plasma membrane surrounding myofibrils is heavily invaginated and ruffled, especially at the junctions between adjacent myofibrils where Ca2+-ATPase activity is very high.
Another type of Ca2+-ATPase is located on the sarcoplasmic reticulum membrane and pumps calcium into the sarcoplasmic reticulum during the relaxation phase of muscle contraction (Lytton and Nigam, 1992), and is considered to be an indicator protein for calcium stores. In P. penicillatus muscle, the presence of Ca2+-ATPase activity in sub-sarcolemmal vesicles close to myofilaments indicates these these vesicles perform the function of sarcoplasmic reticulum.
The calcium precipitation method revealed a similar distribution pattern to that for Ca2+-ATPase localisation; however, it should be noted that although calcium precipitates were present in mitochondria there was no associated Ca2+-ATPase activity. This is to be expected as mitochondria can act as calcium sinks, with calcium ion influx via a calcium uniporter rather than a Ca2+-ATPase pump (Crompton et al., 1983; Kessar and Crompton, 1983). Calcium precipitates also outlined the inner leaflet of the sarcolemma of P. penicillatus swimming muscle, which has been reported for a variety of cell types where calcium ions are probably bound by negatively charged glycoproteins (Carafoli, 1987). Lullman and Peters (Lullman and Peters, 1977; Lullman and Peters, 1979) proposed that these membrane-bound calcium ions could be released during depolarisation of the sarcolemma and participate in cardiac myocyte contraction. However, further studies showed that neither the intracellular calcium concentration, nor muscle contractile force increases during depolarisation without calcium influx (Rich et al., 1988; Nabauer et al., 1989). Thus the inner leaflet of the sarcolemma might simply serve as a calcium-buffering site.
Calcium precipitates were also found in similar vesicular structures in the soma and beneath the sarcolemma of myofibrils. As is implied by the Ca2+-ATPase activity, these vesicles underneath the sarcolemma may function as calcium stores during excitationcontraction coupling, since they are adjacent to the myofibrils. Calcium channels are more abundant on the sarcolemma of myofibrils than on the somal plasmalemma (Lin and Spencer, 2001) to ensure rapid excitationcontraction coupling. Thus cytochemical localisation of Ca2+-ATPase and calcium indicates the presence of a relatively poorly organized sarcoplasmic reticulum and the physiological actions of caffeine on muscle contraction indicate that calcium influx through voltage-gated calcium channels is sufficient to cause muscle contraction. Thus the sarcoplasmic reticulum may play a regulatory role in muscle contraction. For example, the normal swimming pattern for P. penicillatus is a series of bouts. Spencer and Satterlie (Spencer and Satterlie, 1981) noted that there is a stepwise increase in the tension of the first four or so contractions in each bout as well as a decrease in duration. The facilitation in the amplitude of contractile tension is likely to be the result of refilling calcium stores after a period of rest and may represent a case of post-rest potentiation. Together these frequency-dependent changes in contraction dynamics are presumably an adaptation for overcoming the inertia of an animal at rest.
The presence of Ca2+-ATPase activity and calcium precipitates in the mesoglea close to myofibrils is intriguing. One possible function for calcium and Ca2+-ATPase in mesoglea could be similar to opacification (blanching) of the mesoglea in the siphonophore Hippopodius hippopus, which is a calcium dependent process (Bassot et al., 1979). Blanching is due to temporary formation of light-scattering granules in response to the propagation of action potentials in overlying epithelia. Thus in both cases the mesoglea may act as a long-term store for calcium, with dynamic exchange between the epithelium and mesoglea.
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Acknowledgments |
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