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The Oral Apparatus of Tetrahymena V

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The Oral Apparatus of Tetrahymena V J. Cell Set. 44, 317-333 (1980) 317 Printed in Great Britain © Company of Biologists Limited 1980 THE ORAL APPARATUS OF TETRAHYMENA V. ORAL APPARATUS POLYPEPTIDES AND THEIR DISTRIBUTION R. H. GAVIN Department of Biology, Brooklyn College of The City University of Neto York, Brooklyn, N.Y., U.S.A. SUMMARY Two-dimensional electrophoresis was used to resolve approximately 162 polypeptides from the isolated oral apparatus of Tetrahymena thermophila. The molecular weight range was between 110000 and 15000 Daltons. The polypeptides had apparent isoelectric points between pH 3-3 and pH 7-2. Electrophoretic analysis of isolated ciliary axonemes and fractionated oral ap- paratuses made possible the assignment of polypeptides to structures within the oral apparatus. Approximately 24 polypeptides, including a. and /? tubulins, are probable components of the basal body-basal plate complex. At least 5 of the oral apparatus polypeptides, including a and fl tubulin, are components of the oral apparatus ciliary axonemes. Approximately 138 poly- peptides are components of the oral apparatus framework. INTRODUCTION There is a continuing need for studies that refine our knowledge of the molecular structure of the ciliate cortex and its constituent organelles. The oral apparatus of Tetrahymena is a cortical feeding structure composed of ciliated and non-ciliated basal bodies interconnected by a framework of microtubules and filaments (Fig. 1). The ultrastructure (Nilsson & Williams, 1966; Forer, Nilsson & Zeuthen, 1970; Wolfe, 1970; Rannestad & Williams, 1971; Buhse, Stamler & Corliss, 1973; Gavin, 1977; Sattler & Staehelin, 1979), morphogenesis (Frankel & Williams, 1973) and genetics (Orias & Pollock, 1975; Kaczanowski, 1976; Frankel, Nelsen & Jenkins, 1977; Jerka-Dziadosz & Frankel, 1979; Frankel & Jenkins, 1979) of this cortical organelle complex have been extensively investigated. However, there have been relatively few studies devoted to the molecular composition of the oral apparatus (Rannestad & Williams, 1971; Gavin, 1974; Vaudaux, 1976). One report (Gavin, 1974) showed that in a one-dimensional urea-polyacrylamide system approximately 20 proteins could be resolved from isolated oral apparatuses. In the present paper we report the use of a technique for the separation of poly- peptides in 2 dimensions (O'Farrell, 1975) to resolve approximately 162 polypeptides from the isolated oral apparatus of Tetrahymena. In addition, by making use of a fractionation procedure (Wolfe, 1970) that solubilizes oral apparatus basal bodies while leaving intact a framework of microtubules and filaments (Gavin, 1977), we have shown that about 138 oral apparatus polypeptides are constituents of the frame- work, whereas only 24 polypeptides are basal body fraction components. 3i8 R. H. Gavin urn- - PC -df Fig. i. Diagram of the oral apparatus showing the relationship between oral apparatus basal bodies (open circles) and the fibrillar framework (solid lines). Each membranelle (m) consists of 3 rows of hexagonally arranged ciliated basal bodies. The undulating membrane (ura) consists of 2 rows of basal bodies, of which only the outer row is ciliated. Membranellar connectives (me) interconnect the 3 membranelles. The anterior end of each membranelle is connected to the undulating membrane by cross connectives (cc). The posterior end of each membranelle is connected to the undulating membrane by peripheral connectives (pc). The oral ribs (or) originate at the undulating membrane and join with fibres from the third membranelle to form the deep fibre (df). MATERIALS AND METHODS Culture methods Tetrahymena thermophila (Nanney & McCoy, 1976) was grown at 35 °C in a medium consisting of 1-5 % bacropeptone (Difco) and 0-4% yeast extract (Difco). Oral apparatus isolation The procedures for isolating oral apparatuses were basically those described by Wolfe (1970). However, we have made several minor modifications which we have found to be important for obtaining consistently highly purified oral apparatuses. Cells were grown in bactopeptone supplemented with yeast extract since proteose peptone- Oral apparatus polypeptides 319 grown cells yielded lysates containing flocculent debris which was not removed during the centrifugations through sucrose. After the addition of the isolation medium and Triton X-100 (Wolfe, 1970), cell contents were dispersed, resulting in 'ghosts' which retained cell shape. At this stage the preparation was vigorously stirred (in an ice bath) by means of a magnetic stirrer until all oral apparatuses became detached from the disintegrating pellicle. This step was the most time-consuming, frequently requiring 1-2 h. The suspension was then centrifuged as described by Wolfe (1970). The resulting pellet was vortexed on a vortex mixer and resuspended in isolation medium which contained 2#o% Triton X-100. All subsequent centrifugations were carried out with 2-o% Triton X-100 in the isolation medium. Prior to the final centrifugation the suspension was filtered through a polycarbonate filter (pore size 8-o /tm, Nuclepore Filter Corp., Pleasanton, Calif.). Ciliary axoneme isolation Tetrahymena cilia were isolated according to procedures described by Gibbons (1965). An added step in the procedure was filtration of the isolated cilia suspension through a poly- carbonate filter as described for oral apparatus isolation. The filtrate was centrifuged at 10000 g for 30 min to pellet the cilia. In order to effect demembranation of the ciliary axoneme, the wet cilia pellet was resuspended in the Triton X-100 isolation medium that was used for oral apparatus isolation. The suspension was vigorously vortexed and left in an ice bath for 30 min. Subsequently the suspension was centrifuged at 10000 g for 30 min. The axoneme pellet was washed once with distilled water and retained for electrophoretic analysis. Oral apparatus fractionation Isolated oral apparatuses were resuspended in i-o M KC1 and maintained at 4 °C for 18 h. Subsequently, the suspension was centrifuged at ioooog' for 30 min and the supernatant, which contained solubilized basal bodies (Gavin, 1977), was retained for further analysis. The pellet, which contained the oral apparatus framework (Gavin, 1977), was washed twice in distilled water and retained for further analysis. Protein assays Protein assays were performed as described by Lowry, Rosebrough, Farr & Randall (1951) using serum albumin standards. Radioactive labelling Cells were grown in a medium consisting of 1 % bactopeptone and 01 % yeast extract and containing 5 /iCi/ml of pHJleucine (42 Ci/mM). When the culture reached stationary phase cells were harvested and oral apparatuses isolated. The radioactive cell lysate was retained. In order to determine the extent to which cellular proteins could be adsorbed to isolated oral apparatuses during the isolation procedure, non-radioactive cells were lysed in the radio- active lysate retained from the isolation of labelled oral apparatuses. Prior to use, the radio- active lysate was centrifuged at ioooog for 45 min to remove any remaining labelled oral apparatuses. Oral apparatuses were then isolated from cells that were lysed in the radioactive lysate and subsequently assayed for acid-precipitable radioactivity. For acid precipitations, an aliquot of the desired sample was mixed with 2 ml of cold 10 % TCA and passed through a Millipore filter. The filter was washed with at least 25 ml of cold 5 % TCA, dried and dissolved in Bray's solution (Bray, i960) for scintillation counting. Electrophoresis Chemicals. Acrylamide, A^iV'-methylene bis acrylamide, and AT.TV.iV'.iV'-tetramethylene- diamine were obtained from Eastman Kodak. Ultrapure urea was purchased from Schwarz/ Mann. Ampholines and Coomassie Brilliant Blue R-250 were obtained from Bio-Rad Labora- tories. Glycine, Tris base and ammonium persulphate were obtained from Sigma Chemical Co. 320 R. H. Gavin Preparation of samples. A wet pellet of isolated oral apparatuses was mixed with approxi- mately 4-5 vol. of solubilizing solution consisting of 8 M urea, o-oi M Tris pH 8-o, and 2 % pH range 3-10 ampholines or pH range 5-7 ampholines. This solution solubilized more than 90 % of the oral apparatus protein (Gavin, 1974). The sample was vortexed and left in an ice bath for 30 min. Subsequently the sample was returned to room temperature and clarified by centri- fugation. A small residue remaining in the bottom of the centrifuge tube was discarded. The solubilized protein was then used directly for isoelectric focusing gels. The KCl-soluble oral apparatus fraction was first dialysed at 4 °C against distilled water to remove salt and then dried in vacuo. The powder was dissolved in solubilizing solution as described above. The KC1- insoluble oral apparatus fraction (framework) was solubilized as described for oral apparatuses. All preparations were used for isoelectric focusing within 30 min after solubilization. Isoelectric focusing. Isoelectric focusing was carried out in glass tubes 5 mm x 140 mm or 5 mm x 80 mm using the procedure described by O'Farrell (1975). The gel mixture was as described by O'Farrell except that it contained 5 % ampholines (either pH range 3-10 or pH range 5-7) and detergent was omitted. Gels were prerun for 1 h at 250 V. The sample (500 fig protein in 150 ji\) was then loaded and subjected to electrophoresis at 250 V for 16—18 h at room temperature (24-26 CC). znd-dimension electrophoresis. Isoelectric focusing gels were extruded from the tubes and immediately frozen at — 20 °C. The frozen gel was cut transversely
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