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Association of Calcium with Membranes of Squid Giant Axon

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Association of Calcium with Membranes of Squid Giant Axon ASSOCIATION OF CALCIUM WITH MEMBRANES OF SQUID GIANT AXON Ultrastructure and Microprobe Analysis J. L. OSCHMAN, T. A. HALL, P. D. PETERS, and B. J. WALL From the Cavendish Laboratory and Department of Zoology, Cambridge, England, and Downloaded from http://rupress.org/jcb/article-pdf/61/1/156/1070906/156.pdf by guest on 28 September 2021 the Marine Biological Laboratory, Woods Hole, Massachusetts 0254~. The present ad- dress of Dr. Osehman and Dr. Wall is Department of Biological Sciences, Northwestern University, Evanston, Illinois 60201. ABSTRACT Giant axons from the squid, Loligo pealei, were fixed in glutaraldehyde and posttixed in osmium tetroxide. Calcium chloride (5 mM/liter) was added to all aqueous solutions used for tissue processing. Electron-opaque deposits were found along the axonal plasma membranes, within mitochondria, and along the basal plasma membranes of Schwann ceils. X-ray microprobe analysis (EMMA-4) yielded signals for calcium and phosphorus when deposits were probed, whereas these elements were not detected in the axoplasm. INTRODUCTION Many cellular processes appear to be mediated by served readily in the past because of the wide- reversible interactions of ionized calcium with the spread use of osmium, which decalcifies tissues plasma membrane. We have been interested in unless excess calcium is present in the fixative. using the electron microscope to locate membrane To assess the significance of the deposits ad- areas with high affinity for calcium. Addition of jacent to the membranes, one must know their calcium ions to the solutions used for fixing and composition and how they form. The present processing tissues for the electron microscope study was undertaken to utilize the rapidly de- causes opaque deposits to be formed along the veloping technique of electron-probe X-ray micro- plasma membranes of a variety of ceils (I). In analysis (3, 4) to study the composition of the de- insect intestine, for example, deposits occur on posits. The analytical electron microscope is a apical membranes (microvilli) and along septate transmission electron microscope fitted with X-ray but not along gap junctions (2). Apparently, spectrometers that analyze X rays generated particular regions of the plasma membrane, or when a micro-area of the specimen is bombarded some structure closely associated with the mem- by the electron beam. Since each element pro- brane, can sequester enough calcium to make the duces X rays of characteristic energy and wave- region adjacent to the membrane opaque to elec- length, information is obtained about the composi- trons. Although we do not know precisely how the tion of the specimen. Microprobe analysis is well deposits form, we suspect that the presence of cal- suited for analyzing bound ions, since conventional cium ions during processing keeps intraceUular fixation and embedding techniques can be used. binding sites saturated. The deposits were not ob- Our initial attempts were made on intestinal 156 THe. JOU~AL OF CEIL BIOLOGY • VOL~B 61, 1974 • pages 156-105 tissue, the subject of our previous studies. The de- stained with uranyl acetate and lead citrate, and posits in intestine proved too small to produce an examined either with a JEOL EM6B or with a Philips adequate signal. In the meantime, HiUman and EM 300. Measurements of size and frequency of de- posits on membranes were made after calibration Llin~s (personal communication) had observed with a carbon replica of a diffraction grating, 28,800 similar but larger deposits in squid axon, and pre- lines per inch. viously Villegas and Villegas in 1968 (5) had also observed deposits in squid axon. We found that the X-Ray Microprobe Analysis deposits in squid axon were too small to be ana- lyzed individually (spot size in the microprobe is Specimens for microprobe study were fixed and about 0.2 /~m), but groups of several deposits embedded as described above. Thick sections (blue along the membranes and within mitochondria or green interference colors, ca. 1,900-2,800 .~ thick) could be probed. Deposits yielded good signals (9) were placed on nickel grids, and a layer of carbon was evaporated upon them. To minimize fourth-order when the spectrometers were set at the Bragg copper interference with the phosphorus K~ line, a angles for calcium and phosphorus. When the titanium specimen holder was used. Specimens were spectrometers were offset slightly from these angles, examined without staining in the EMMA-4 micro- the signals were much smaller. When the probe probe analyzer. Column voltage was set at 40 kV. A was moved to the axoplasm, the count rate also dentine standard was used to calibrate the spectrom- Downloaded from http://rupress.org/jcb/article-pdf/61/1/156/1070906/156.pdf by guest on 28 September 2021 dropped sharply. Energy analyses of the X rays eters for calcium and phosphorus. One spectrometer yielded sharp spectral peaks for Ca and P which was set for the calcium I~, radiation, using a lithium could be compared with those from a dentine fluoride diffracting crystal. The other spectrometer standard. was set for the phosphorus K~ radiation, using a The results confirm that the deposits contain penta-erythritol (PET) crystal. The regions of in- terest were probed for intervals of 20, 40, or 100 s. calcium as well as phosphorus, suggesting that Background counts were determined by probing the phosphate may be the anion. The results obtained same areas with the spectrometers offset by 0.080 by probing mitochondria, while preliminary, con- inch. In some instances a length of membrane was firm that mitochondria of squid axon, like probed with an astigmatic elliptical spot. After micro- mitochondria from many other tissues (6, 7), probe analysis the areas probed were photographed sequester calcium. with the EM 300 to provide a record of the precise A preliminary report of this work has been pub- location of the probe spot, which could be recognized lished (8). Some aspects of this study were inde- because of the beam damage done to the specimen. pendently demonstrated by Hillman and Llinfis. 1 The results of probing different areas were com- pared by computing the values for R, given by : MATERIALS AND METHODS P--b R Electron Microscopy W-- W~ Axons were taken from living squids (Loligo pealei) where P is the peak count; b is the count obtained at Woods Hole. Axons were fixed overnight in from the spectrometer offset by 0.080 inch; W is the s-collidine-buffered 2.4% glutaraldehyde containing 5 "white 'p count obtained from a third, nondispersive raM/liter CaC12 and 25.5% sucrose. Axons were detector receiving radiation directly from the speci- then washed thoroughly in buffered sucrose and post- men; and Wb is the white count obtained by probing fixed in osmium tetroxide. Calcium chloride (5mM/ a specimen-free region of the grid. The latter value liter) was also added to the rinse and osmium solu- permits correction for extraneous X rays such as those tions. In some cases postfLxation in osmium was produced by backscattered electrons hitting parts of omitted. Glutaraldehyde and collidine buffer were the column. The value of R is a relative measure of obtained from Polysciences, Inc., Warrington, Pa., elemental concentration within an entire analyzed because we had found in our previous study (I) that microvolume. These volumes typically were larger these reagents have very low electrolyte content. than individual deposits and did not consist solely of Specimens were rapidly dehydrated in ethanol and deposits, embedded in Spnrr resin. Thin sections cut on a Separate analyses were done with a Kevex energy Huxley microtome were mounted on copper grids, dispersive X-ray spectrometer with a Si-(Li) detector attached to the EMMA-4. Specimens were prepared 1Hillman, D. E., and R. Llinks. 1974. Calcium-con- as described above except that osmium treatment taining electron-dense structures in the axons of the was omitted. This technique facilitated spectrum squid giant synapse. J. Cell Biol. 61:146. scans to determine if other elements were present in OSCnMAN, HALL, PETERS, AND WALL Association of Calcium with Membranes of Squid Giant Azon 157 Downloaded from http://rupress.org/jcb/article-pdf/61/1/156/1070906/156.pdf by guest on 28 September 2021 FmunE 1 Survey view of axon (az), Schwann cell sheath (Sc), and connective tissue (ct). Deposits occur at interface between axoplasm and Schwann cell. X 9,000. FmVRE ~ Detail of calcium deposits along axolemma. Sehwann cell cytoplasm shown at left. Glutaral- dehyde, osmium, stained section. Average size of deposits is about 0.05/zm. X 61,000. 158 TItE JOURNAL OF CELL BIOLOGY - VOLUME 61, 1974 the deposits, and provided data on the relative amounts of Ca and P. For quantitative estimation of Ca/P ratios, back- ground-corrected integral counts were obtained from quantum-energy bands around the calcium and phosphorus spectral peaks. RESULTS Electron Microscopy When calcium ions are present in the solutions used for processing squid axons for electron micros- copy, electron-opaque deposits occur along the interface between axoplasm and Schwann cell sheath. Figs. 1 and 2 illustrate these deposits at low and high magnifications, respectively. The deposits appear to have a globular shape and are most frequently associated with the axonal mem- Downloaded from http://rupress.org/jcb/article-pdf/61/1/156/1070906/156.pdf by guest on 28 September 2021 brane rather than with the nearby Schwann cell membrane. Some deposits appear to be located within the narrow interspace between axonal and Schwann cell membranes, but this could be due to curvature of the membrane within the thickness of the section. An unstained specimen that was fixed only in glutaraldehyde is illustrated in Fig. 3. Since no heavy metals were added to this specimen during preparation, the deposits must be due to calcium, the only cation present, along with tissue com- ponents with intrinsic electron-scattering power.
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