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Increase in Osmiophilia of Axonal Membranes of Crayfish As a Result of Electrical Stimulation, Asphyxia, Or Treatment with Reducing Agents

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Increase in Osmiophilia of Axonal Membranes of Crayfish As a Result of Electrical Stimulation, Asphyxia, Or Treatment with Reducing Agents INCREASE IN OSMIOPHILIA OF AXONAL MEMBRANES OF CRAYFISH AS A RESULT OF ELECTRICAL STIMULATION, ASPHYXIA, OR TREATMENT WITH REDUCING AGENTS CAMILLO PERACCHIA and J . DAVID ROBERTSON From the Department of Anatomy, Duke University Medical Center, Durham, North Carolina 27706. Dr. Peracchia's present address is the Department of Physiology, University of Rochester Medical Center, Rochester, New York 14642 ABSTRACT Certain axonal membranes of crayfish abdominal nerve cord display ultrastructural changes if the axons are fixed, during electrical stimulation, by aldehydes followed by osmium . Such changes are characterized by an increase in electron opacity and thickness of the unit membranes' dense strata in the axon surface, endoplasmic reticulum, and outer mitochon- drial membranes . The electron opacity completely disappears if the sections are treated with hydrogen peroxide solutions . This suggests that the changes represent an increase in the membranes' reactivity for osmium . An unmasking of SH groups could explain such increased osmiophilia, since SH groups are very reactive with osmium, while disulfide bonds are considerably less reactive . This hypothesis was tested by treating control, glutaraldehyde- fixed nerve cords with disulfide reducing agents . In these preparations an increase in electron opacity and thickness was observed to be localized in the same axonal membranes which reacted as a result of electrical stimulation . The phenomenon did not appear if the SH groups were blocked by maleimide or N-ethylmaleimide before treatment with osmium . These findings seem to suggest that certain axonal membranes of crayfish contain proteins rich in sulfur whose SH groups are unmasked as a result of electrical stimulation. In pre- liminary experiments an increase in osmiophilia localized in the same membranes with the same characteristics and distribution was observed also in axons from nerve cords asphyxi- ated either in vitro or in the living animal . INTRODUCTION Most of the information concerning changes in from axons stimulated in vitro and were inter- nerve fibers as a result of activity comes from elec- preted in relation to changes in volume of the ex- trophysiological studies . Nevertheless, some studies amined axons (3-7) . Recently, however, changes on morphological modifications are also available . Occurring at the speed of the action potential have Early in this century changes in the histological also been recorded, suggesting that rapid modifica- staining of neurofibrils were seen in nerve fibers tions, possibly associated with excitation, take place subjected to polarizing current (1), and such ob- (8, 9, 10) . servations were later confirmed and found to Changes in birefringence were recorded in stim- appear only in live, unanesthetized nerves (2) . ulated axons also synchronously with the action Slow changes in light scattering were recorded potential (9, 10), as well as an increase in fluores- THE JOURNAL OF CELL BIOLOGY . VOLUME 51, 1971 . pages 2 2 3-239 223 cence in axons treated with 8-anilinonaphthalene- Fixation was performed during the stimulation, 1-sulfonic acid (ANS) (10) . ANS seems to bind to perfusing by syringe, through the sternal artery, the hydrophobic groups of macromolecules (11) 40-60 cc of 3-6°ßc glutaraldehyde solution buffered and to change the fluorescence properties in rela- with 0.1 M (Na, K) phosphate to pH 7 .4 at room tion to conformational modifications in various temperature . The electrical activity, recorded on the oscilloscope screen, disappeared after 30-35 sec of macromolecules (12) . It was suggested, therefore, perfusion with the fixative, corresponding to 15-20 that these changes could be related to conforma- cc of injected fixative . tional modifications occurring in membrane mac- The chain of abdominal ganglia was then dis- romolecules during excitation . sected from the animal and kept for 2 hr in the same In previous reports we have briefly described fixative at room temperature . It was washed for 15 ultrastructural modifications occurring in crayfish min in 0 .2 M phosphate (pH 7 .4) and postfixed for nerve fibers as a result of electrical stimulation, 2 hr in 2% osmium tetroxide buffered by 0 .1 M which are characterized by an increase in electron phosphate to pH 7 .4 at room temperature . The dehy- opacity and thickness of certain axonal membranes dration was carried out in graded alcohol or acetone (13) . These changes were interpreted as caused by and the embedding was made in Epon or Araldite . In control experiments, the animals were pre- an unmasking of SH groups in membrane proteins pared in the same manner, in the sense that the (14) . sternal artery was dissected, cannulated, and per- Modifications that could be of the same nature fused with heparin followed by Van Harreveld were described in stimulated frog sciatic nerves saline, and the electrodes were placed in contact with (15) . In this case a deposition of electron-opaque the nerve cord but the stimulator was left off . The granules was observed on axonal as well as fixative was perfused after lapses of time correspond- Schwann cell membranes . The dense granules were ing to those of different stimulations, and the experi- absent in the anodic segment of nerves submitted ment was carried on as described above . to polarizing current . Sections (500 A thick) were cut on an LKB Ultratome microtome, collected on uncoated 400 METHODS mesh grids, and observed either unstained or stained by a 3 min immersion in a 3% solution of lead salts Crayfish (Procambarus clarkii), 10-15 cm long, were (17) . On certain occasions, before lead staining, the obtained from Carolina Biological Supply Co., Bur- sections were stained by a 10 min immersion in a lington, N. C., and kept in well oxygenated aquaria saturated solution of uranyl acetate in 50 0/0 alcohol. at about 20 °C. The crayfish were anesthetized for In some experiments unstained sections from stimu- about 10 min by cooling in crushed ice and water . lated nerve cords were collected on uncoated grids The sternal artery was dissected, cannulated with a and immersed in a 370 solution of hydrogen peroxide polyethylene tubing (outer diameter, 0 .038 inches) in order to remove the osmium (18) . The specimens and perfused, by syringe, with 50-100 U .S.P. units were observed with an AEI EM 6B electron micro- of heparin (Liquaemin Sodium "10") (Organon scope . For examination at magnifications higher Inc., West Orange, N . J .) in 10 cc of Van Harre- than 20,000, the sections were coated with a thin veld's salt solution (16) . During the subsequent dis- carbon film. section and stimulation the crayfish were perfused Experiments were performed using sulfhydryl with the salt solution using an intravenous system at reagents as follows : chains of unstimulated ganglia the rate of 20-30 drops per minute at room tempera- were dissected from the animals and fixed for 2 hr ture . In some experiments the perfusion with heparin by immersion in a 670 solution of glutaraldehyde was not performed. Oxygen was bubbled continu- buffered by 0.1 M (Na, K) phosphate to pH 7 .4 at ously through the salt solution . room temperature . After a 15 min wash in 0 .2 M The cephalic carapace was then dissected out, the phosphate, the chains were cut into two portions . green glands were carefully removed, and the cir- One was immersed for 1 hr in 0.4 M sodium thio- cumoesophageal connectives with the supraoesopha- ., Plainview, geal ganglion were exposed . One of the two circum- glycolate (K & K Laboratories Inc oesophageal connectives was isolated and placed in N. Y.) (19, 20) or 5 mm DTE (Dithioerythritol) M contact with a pair of platinum electrodes for the (Sigma Chemical Co., St. Louis, Mo.), both in 0.1 stimulation . The abdominal chain was exposed phosphate buffer (pH 7) at room temperature . The between the fifth and the sixth ganglion and placed other was placed in 0.2 M phosphate (pH 7) as a in contact with a similar pair of electrodes for exter- control. After a 30 min wash in 0 .2 M phosphate nal recording . Square pulses (1-5 v) (0 .1-0 .5 msec) buffer (pH 7), the specimens were postfixed, dehy- repeated at frequencies of 2-60 cps were applied for drated, and embedded as described above . In certain various lengths of time (from 30 sec to 30 min) . experiments ganglia treated with the reducing agents 224 THE JOURNAL OF CELL BIOLOGY • VOLUME 51, 1971 were washed for 15 min in phosphate buffer (pH 7), The axoplasm is rich in microtubules but contains and were treated for 30 min-1 hr with a 0 .1 M solu- little endoplasmic reticulum . The matrix is denser tion of maleimide (K & K Laboratories Inc.) or than in giant axons and is frequently occupied by N-ethyl-maleimide (NEM) (Mann Research Labs fuzzy, unoriented filaments which sometimes seem Inc., New York) (19, 20, 21) in 0 .1 M phosphate to bridge adjacent microtubules. Medium-sized buffer (pH 7 .6) at room temperature and postfixed, axons are surrounded by few Schwann cells, while dehydrated, and embedded as described above . Preliminary experiments were performed on as- small axons are generally enveloped by just one phyxiated nerve cords. Chains of abdominal ganglia, cell. Tubular lattices are also sometimes seen in dissected from the animals, were kept for 30 min in these Schwann cells, but with a smaller extension . closed bottles filled with Van Harreveld's saline, In Fig. 3 a portion of a medium-sized axon at through which nitrogen or carbon dioxide was higher magnification is seen . In this axon, as well bubbled . Control chains were kept for the same as in control axons of different size (Figs . 1, 2), all length of time in Van Harreveld's saline through of the membranes display the same electron opac- which oxygen was bubbled. The saline solutions ity.
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