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Squid Giant Axon (Glia/Neurons/Secretion) Proc. Nat. Acad. Sci. USA Vol. 71, No. 4, pp. 1188-1192, April 1974 Transfer of Newly Synthesized Proteins from Schwann Cells to the Squid Giant Axon (glia/neurons/secretion) R. J. LASEK*, H. GAINERt, AND R. J. PRZYBYLSKI* Marine Biological Laboratory, Woods Hole, Massachusetts 02543 Communicated by Walle J. H. Nauta, November 28, 1973 ABSTRACT The squid giant axon is presented as a teins synthesized in the Schwann cells surrounding the axon model for the study of macromolecular interaction be- tween cells in the nervous system. When the isolated giant are subsequently transferred into the axoplasm. axon was incubated in sea water containing [3Hjleucine MATERIALS AND METHODS for 0.5-5 hr, newly synthesized proteins appeared in the sheath and axoplasm as demonstrated by: (i) radioautogra- Protein synthesis was studied in squid giant axons obtained phy, (ii) separation of the -sheath and axoplasm by extru- from live squid which were kept in a sea tank and used within sion, and (iii) perfusion of electrically excitable axons. hr of obtained The absence of ribosomal RNA in the axoplasm [Lasek, 48 capture. The giant axons were by decapitat- R. J. et al. (1973) Nature 244, 162-165] coupled with other ing the squid and dissecting the axons under a stream of run- evidence indicates that the labeled proteins that are found ning sea water. The axons, 4-6 cm long, were tied with thread in the axoplasm originate in the Schwann cells surrounding at both ends, removed from the mantle, and cleaned of ad- the axon. Approximately 50%70 of the newly synthesized hering connective tissue in a petri dish filled with sea water Schwann cell proteins are transferred to the giant axon. These transferred proteins are soluble for the most part under observation with a binocular dissecting microscope. and range in molecular size from 12,000 to greater than Axons were incubated for 0-4 hr at 18-20° in 1 ml of Milli- 200,000 daltons. It is suggested that proteins transferred pore-filtered (MPF) sea water containing either 10 or 100 from the Schwann cell to the axon have a regulatory role 1,Ci of L-[4,5-3H]leucine. The incubation was terminated by in neuronal function. rinsing the axon in a large volume of MIPF sea water at 40 for min. The was extruded from The supply of macromolecules from the neuron cell body to 5-10 axoplasm immediately the sheath a method described except that the axon is well established (1). However, some proteins by previously (8) a of was substituted for the rub- may be supplied to the axon by synthetic mechanisms which length polyethylene tubing ber roller. All of the data below were obtained exist at the level of the axon. Two possible sites have been presented by this method. alternate methods of the suggested for the local synthesis of axonal proteins: (i) pro- However, extruding with a roller or with fine teins are synthesized in the axoplasm (2), and (ii)- proteins axoplasm by compression forceps produced comparable results. The sheath and axoplasm were are synthesized in the Schwann cells surrounding the axon homogenized in 50 mM Tris- HCL buffer, pH 7.4. Aliquots and subsequently transferred to the axon (3). Singer has been the strongest proponent of the Schwann-cell-to-axon transfer of the homogenate were taken for the following analysis: hypothesis and has reviewed the literature regarding this total radioactivity; hot (950 for 30 min) trichloroacetic acid question (4). precipitable radioactivity measured on filters; protein mea- sured the method of et al. and in some cases The squid giant axon represents an ideal model for the study by Lowry (9); of axonal macromolecular synthesis because the axoplasm sodium dodecyl sulfate, gel electrophoresis (10) or isoelec- tric on In other experi- can readily be separated from the sheath by simple extrusion focusing (11) polyacrylamide gels. (5). Amino-acid incorporation into protein has been demon- ments the giant axons were prepared for radioautography at the end of the incubation. strated in the isolated giant axon (6, 7). Furthermore, Lasek et al. (8) have recently characterized the RNA which is present RESULTS AND DISCUSSION in the axoplasm of the squid giant axon and have found little Table 1 compares the amount of trichloroacetic acid-precipit- if any ribosomal RNA. Ninety-five percent or more of the found in and sheath after 120 RNA in the axoplasm is 4 S in size, apparently transfer RNA. able radioactivity axoplasm min of incubation. The axoplasm contains 5-24% of the These results appear to rule out protein synthesis in the axo- labeled proteins. The variation in the relative labeling of the plasm by generally accepted mechanisms, and an alternate axoplasm is not completely understood; however, it may be source of the labeled proteins seems probable. The findings a result of variations in the amount of connective tissue presented below are consistent with the hypothesis that pro- which remained attached to the sheath after dissection. Abbreviations: MPF, Millipore-filtered; AXM, acetoxycyclo- Puromycin and acetoxycycloheximide (AXM) inhibited heximide. the incorporation into both axoplasm and sheath by 80% * Present address: Department of Anatomy, Case Western Re- or more, whereas chloramphenicol had little effect on in- serve University, Cleveland, Ohio 44106. corporation. The inhibition produced by puromycin and AXM t Present address: Behavioral Biology Branch, National Institutes did not result from reduced precursor entry into the axon of Health, N.I.C.H.D., Bethesda, Md. 20014. because these drugs had no demonstrable effect upon the solu- 1188 Downloaded by guest on October 1, 2021 Proc. Nat. Acad. Sci. USA 71 (1974) Transfer of Proteins from Glia to Neurons 1189 TABLE 1. Incorporation of [3H]leucine into proteins in the axoplasm (A) and sheath (S) of the squid giant axon after 120 min of incubation cpm/jig of protein Chloram- Control AXM t Puromycin phenicol A S A S A S A S 122 (5.3 %)* 4490 2 123 2 201 158 2013 42 (6.6%) 1853 6 241 8 69 48 1340 130 (12%) 2170 24 1148 138 (24%) 1409 20(7.9%) 503 26 (4.7%) 1036 Mean 79 (10%) 1910 4 182 5 135 76 1500 * In the control column, the figures in parentheses represent the amount of total hot trichloroacetic acid-precipitable radioactivity found in the axoplasm and are expressed as a percentage of the total found in the sheath. The protein content of the axoplasm (A) and sheath (S) obtained from each giant axon is on the order FIG. 1. Radioautographs of squid giant axons incubated in I of 100 jig and 40 jig, respectively. ml of MPF sea water containing [Htlleucine (100 jiCi/ml). r'he t AXM (Acetoxycycloheximide) = 50 jg/ml; puromycin = 50 emulsion is saturated in some regions of the sheath because of the jig/ml; and chloramphenicol = 100 or 200 jig/ml. exposure time of 3 weeks. Marker bar equals 50 jim. (A) Portion of a control giant axon with smaller axons left attached (top of ble radioactivity in either the sheath or axon. These results figure). The axon was incubated for 120 min in [3Hlleucine plus suggest that the incorporation of radioactivity into proteins 50 jg/ml of acetoxycycloheximide and 50 jig/ml of puromycin to in the axon and sheath represents translation on cellular ribo- inhibit protein synthesis. (B) Giant axon treated-the same as in somes and that relatively little incorporation occurred in A except that AXM and puromycin were omitted. Note the mitochondria or bacteria. presence of silver grains over the axoplasm. (C) Giant axon with Radioautographs verify that the labeled proteins extruded smaller axons attached incubated for 180 min. Note that the with the axoplasm represent labeled proteins present in the smaller axons also have grains over the axoplasm. (D) Higher magnification of the axon shown in B. Note the concentration of TABLE 2. Comparison of radioautographic grain counts in the grains in the region of the Schwann cell layer (arrows) and in axoplasm and sheath of squid giant axions scattered cells in the outer layer of the sheath. Minutes of incubation axoplasm, rather than a contaminant from the sheath (Fig. Section 60 120 180 1). Grain counts of labeled axons incubated for 60, 120, and 180 min indicate that the axoplasm contains 12-28% of the A Axoplasm 406 (28%) 398 (28%) 760 (18%) of Sheath 1434 1398 4290 counts in the sheath (Table 2). The percentage radioactivity B Axoplasm 202 (26%) 556 (12%) 2722 (23%) in the axoplasm was higher in the radioautographic analysis Sheath 768 4507 11621 (Table 2) than in the analysis of extruded axoplasm (Table 1). This difference probably results from the inclusion of A and B represent two different- sections from the same axon. connective tissue elements and some small axons which adhere Giant axons were isolated and incubated as described in the text. to the sheath in the extrusion experiments; in the radio- The incubation was terminated by immersion in 5% trichloro- autographic estimates these elements were systematically acetic acid containing excess unlabeled leucine (4°). The solu- disregarded when the grains were counted. Axons incubated tion was changed five times over a period of 6 hr, the axon ex- for 120 min with 50 /Ag/ml of AXM and 50 jg/ml of puro- tracted with two changes of ethanol at room temperature over- no grains above the background level night and imbedded in Epon by standard methods. All of the mycin contained grains in the axoplasm were counted at X 1000 magnification. (Fig. 1A). Grains in the sheath were estimated by counting the grains in a Local differences in incorporation were found when two 25-jim2 ocular micrometer which was moved around the sheath levels of the same axon were compared (compare A and B twice so that every seventh 25-jim2 field was counted.
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