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Specificity of Pseudopodium Induction by the Action of Cations on Amoeba Proteus

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Specificity of Pseudopodium Induction by the Action of Cations on Amoeba Proteus J. Cell Sci. 7, 549-555 097°) 549 Printed in Great Britain SPECIFICITY OF PSEUDOPODIUM INDUCTION BY THE ACTION OF CATIONS ON AMOEBA PROTEUS J. E. BREWER AND L. G. E. BELL Department of Zoology, University of Southampton, Southampton, England SUMMARY Some substituted cholines, long-chain aliphatic substituted amines and simple inorganic salts have been tested at different concentrations for their ability to induce pseudopodia from Amoeba proteus. The ability of substituted amines to induce pseudopodia is inversely related to their ability to bind to acid polysaccharides. The reaction of compounds with the surface polysaccharide is probably not in itself the only requirement for pseudopodium induction. A mechanism is proposed in which the properties of the cell membrane are altered by the reaction of compounds with bulky cationic groups with the membrane lipid. The formation of new pseudopodia is not the direct result of a local reduction in the surface charge density or in surface potential. INTRODUCTION Previous work has shown that local concentrations of organic cations, both complex proteins and simple detergents, will induce pseudopodia from Amoeba proteus (Jeon & Bell, 1965; Seravin, 1968; Brewer & Bell, 1969a). The mechanism of action proposed (Jeon & Bell, 1965; Brewer & Bell, 1969a) involves the reaction of the cations with acidic polysaccharides at the cell surface followed by the passage of the signal so produced across the cell membrane to the cytoplasm. The importance of charge- dependent interactions in the reaction of detergents with A. proteus has been shown by Brewer & Bell (19696), but the results described in the present communication suggest that pseudopodium induction involves greater specificity in the inducing cation. The role of the concentration of the inducing cation has also been investigated. METHODS Culture methods A. proteus, strain X65 (Ord, 1968), was grown in mass culture in Chalkley's solution by the method of Griffin (i960). Tetrahymena pyriformis was the food organism. Cells were starved (24 h) before use and washed at least 5 times in Chalkley's solution to remove contaminants. Chalkley's solution was of the following final composition: NaCl, 1-37 mM; NaHCO3, 2 2 3 3 4-76 x io~ mM; KC1, 2-68 x io~ mM; Na.2HPO4, 279 x io" mM; CaHPO4, 7-35 x io" mM; MgCl», 4-92 x io~3 mM. 35-2 550 J. E. Brewer and L. G. E. Bell Chemicals All chemicals were of the best grade available. Succinyl choline (SuccCh), succinyl dicholine (SuccDich), dodecyltrimethylammonium bromide (C]2quat) and dodecyldimethylamine (C12NMe2) were obtained from K and K Laboratories Inc.; dodecanoic acid (CuC00H) and sodium dodecyl sulphate (C12SO4Na) were obtained from BDH Ltd.; phosphoryl choline (PhosCh) was obtained from Koch-Light Laboratories Ltd. and dodecylamine (C]2NH2) was obtained from RN Emanual Ltd. C12NMe2 and C12NH2 were used as the hydrochlorides and C^COOH was used as the sodium salt. Technique for the demonstration of pseudopodium induction The method of Jeon & Bell (1965) was used. Amoebae were observed in a chamber, depth 1 mm, constructed of pieces of glass slide cemented to a large slide with Araldite. Sufficient Chalkley's solution was present to provide a flat upper surface. Micropipettes, 10 /«n tip diameter, were filled with a solution of the compound to be tested in Agarose (05 %) by compressed air. The tip of the pipette was placed near an amoeba and the reaction of the amoeba was observed and filmed. Induction of pseudopodia, food-cup formation, inhibition of pseudopodium formation and indifference could be clearly distinguished. Com- pounds were retested on at least 2 occasions using at least 10 pipettes. Cinematography at 1 frame/s was used to record the experiments and closed circuit television enabled unhindered observations to be made by persons other than the experimenter. RESULTS The main groups of compounds investigated were a group of cholines of approxi- mately the same chain length but of different charge ratios, a number of simple inorganic salts and detergents of the general form C12H25R where R was a charged group. The compounds were tested at different concentrations over parts of the range io~4 M-I M. Very high concentrations, e.g. io-1 M, caused non-specific effects irrespective of the pseudopodium-inducing ability of the compounds at lower concentrations. The concentration of cations at the cell surface may be expected to be 2-3 orders of magni- tude lower than the concentration in the pipette (Brewer & Bell, 1969a). The first stage in pseudopodium induction was the cessation of streaming immediately below the cell envelope at a point nearest to the pipette tip (Jeon & Bell, 1965; Brewer & Bell, 1969 a). Further stimulation led to the formation of a pseudopodium in the direction of the pipette. Pipettes containing compounds which did not induce pseudo- podia generally had no effect on the direction of formation of pseudopodia by the cell. However, high concentrations of many compounds caused a characteristic non- specific reaction. This took the form of inhibition of streaming in the direction of the pipette and in some cases complete reversal of cytoplasmic streaming occurred and the cell moved rapidly away from the stimulus. Thus, pipettes containing NaCl (1 M in 0-5 % Agarose) positioned in front of an advancing pseudopodium caused a rapid and powerful contraction in the pseudopodium and immediate reversal of the direction of cytoplasmic streaming. Similar effects were obtained with pipettes containing KC1, 1 CaCl2 or MgCl2 at 1 M or C12SO4Na at io" M. This effect is completely non-specific when compared with the effects of these compounds at lower concentrations; NaCl, 3 KC1, CaCl2, MgCl2 and C12SO4Na have no effect in pipettes at io~ M whereas Specificity of pseudopodium induction 551 C12quat induces pseudopodia at this concentration. Similarly the effects of the above concentrations of these compounds on amoebae immersed in them are quite different; at 1 M NaCl and KC1 induce pinocytosis, CaCl2 and MgCl2 are poor inducers of pino- cytosis and C12quat and C12SO4Na are lytic. The effect of increasing the concentration of the test compound in the pipettes takes 2 forms depending on whether or not there is a concentration which is effective 4 in inducing pseudopodia. Pipettes containing C12quat at IO~ M and below have no effect on amoebae, which continue to move to extend pseudopodia in directions unrelated to the position of the pipette. At 3 x io~4 M, pseudopodia are induced in nearly all cases but food-cups develop only occasionally. At io~3 M, several pseudopodia are induced and large food-cups are produced about the tip of the pipette. At IO~2M extreme reactions occur in which nearly the whole of the amoeba is engaged in forming an enormous food-cup by the projection of a continuous sheet of the cell towards the pipette. In some cases the cell may be immobilized. At icr1 M immediate reversal of streaming takes place in that part of the cell closest to the pipette and the cell moves away from the stimulus. Pipettes containing NaCl never induce pseudopodia and the change in reaction with increase in NaCl concentration is a change from indifference to avoidance without an intervening attractive concentration. Thus, cells are indifferent to pipettes con- taining NaCl at io~2 M or below; at io"1 M the reaction is one of avoidance by the inhibition of pseudopodium formation in the general direction of the pipette. Pipettes containing NaCl at 1 M produce a dramatic contraction in approaching pseudopodia followed by the rapid reversal of streaming away from the stimulus. Pipettes containing the following compounds were found to induce pseudopodia in the following order of effectiveness at some appropriate concentration: C12quat > SuccDich > PhosCh > SuccCh > C12NMe2. C12NH2, C12SO4Na, C^COC-H, NaCl, KC1, CaCl2 and MgCl2 were completely ineffective at any concentration. These results are summarized in Table 1 together with some physical properties of the compounds. The lengths of the unhydrated organic ions were estimated from Courtauld space-filling models; the sizes of the inorganic ions are given in terms of the radii of the hydrated ions. The activity of the compounds was assessed both in terms of the concentrations which elicited pseudo- podia and the position along the length of the amoeba from which pseudopodia could be formed (Jeon & Bell, 1965). The change in the activity of the substituted amines with the degree of substitution was striking. The fully substituted compound induced pseudopodia from about two-thirds the length of the cell from the front at io~3 M in the pipette, the rear part of the cell being insensitive, but theunsubstituted primary amine was completely inactive at any concentration. The tertiary amine was only weakly active in the anterior, most sensitive part of the cell and was less active than any of the quaternary amines tested. SuccDich with 2 quaternary amine groups was of about the same activity as C12quat with only one such group but much more active than either PhosCh or SuccCh, which have one quaternary ammonium group together with a negatively charged group (phosphoryl or carboxyl). On t-ri Table i. Reaction of Amoeba proteus to compounds diffusing from micropipettes Charge Ionic Size, ratio species 1-1 ' M 3 X IO~4M IO"1 M ^ fcq C12quat i-88 1 :o SuccDich i-8 2:0 - + "T CNMejH i-9 1 :o ° 8 SuccCh i"3 1:1 -I- + PhosCh 1:1 a C12SO4 0:1 CnCOO 1-84 0:1 C12NH2H 177 1 :o Na 0-183 1 :o tq K 0-125 1 :o Mg O-345 2:0 o Ca 0-308 2:0 o + + + +, Extreme food-cup formation; + + +, food-cup formation; ++, pseudopodium induction; +, weak pseudopodium induction; o, no effect; , cytoplasmic contraction; —, inhibition of pseudopodium formation.
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