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160 H 0 Gutzeit, Fig 1 Nurse cell regression Nurse cell chambers of stage 10B A and stage 12 B. follicles photographed by differential interference contrast At stage 10B nurse cell. cytoplasm begins to stream into the oocyte ooc This process is completed at stage 12 B. when only the shrunken nurse cell nuclei ncn remain in the degenerate nurse cell. chamber At the anterior egg pole the follicle cells differentiate the chorionic appendages. open arrowhead and the micropyle arrowhead fc somatic follicle cells Bar 50 fJin. MATERIALS AND METHODS,Time lapse filming, Cytoplasmic streaming has been recorded by time lapse cinematography as described previously. Gutzeit Koppa 1982 In order to ensure fast and homogeneous exchange of culture me. dium during filming a newly designed flow through chamber was used for details see Gutzeit. Kaltenbach 1985 Isolated follicles of stage 10B or 11 were placed in the chamber and cultured. in Robb s R 14 medium Robb 1969 which was pumped through the chamber at a rate of. 0 26mlmin After recording the normal pattern of streaming for about 15min 50 90. frames min 1 the culture medium was replaced by medium containing the inhibitor to be tested. Cytochalasin B and D Sigma were dissolved in dimethylsulphoxide DMSO or ethanol Uvasol. Merck The stock solutions of the inhibitors contained lOmgml 1 and 2mgml 1 respectively. These solutions were diluted at least 1 1000 with culture medium see Table 1 for details Control. follicles were cultured in medium containing only the solvent ethanol or DMSO at 1 1000. dilution but not the inhibitor Under these conditions there was no effect on cytoplasmic. Medium with and without the inhibitor was exchanged by means of a two way valve. Pharmacia Since the flow through chamber ensures uniform and reliable replacement of differ. ent media it was possible to estimate the time when the follicle became exposed to the inhibitor. From tests with Trypan Blue dye we estimated the accuracy to be of the order of 30 s For details. concerning the concentrations of applied inhibitor see Table 1 The effect of the drug on. cytoplasmic streaming was only followed for up to 2 h of culture in vitro since by about that time. cytoplasmic streaming is arrested in control follicles not exposed to the drug Gutzeit Koppa. Whenever the effect of the drug was studied for longer than 30 min we filmed short sequences. at 15 or 30 min intervals in order to avoid possible artefacts that may be caused by constant. illumination of the follicles with the microscope lamp. Micrvfilaments in cytoplasmic streaming 161, Drawings from time lapse films were made by projecting the film by a system of mirrors onto. drawing paper and the direction of streaming was marked wherever it could be seen clearly. Fluorescence microscopy ofF actin in nurse cells, Staining of MF with rhodaminyl phalloidin RH phalloidin was carried out as described. previously Warn et cd 1985 their method 2 Rh phalloidin was a generous gift from Professor. Th Wieland Heidelberg FRG The preparations were viewed in a Leitz microscope using a X63. oil immersion objective and photographs were taken on Ilford HP5 high speed film In some cases. we teased nurse cell chambers apart with tungsten needles after fixation The preferred fracture. plane was usually along the nurse cell membranes so that single cells or a small number of nurse. cells could be isolated Owing to the much reduced thickness of such preparations their MF. pattern was usually easier to analyse as compared to in toto stained follicles. Nurse cell nuclei were isolated by cutting through the nurse cell cluster with tungsten needles. before fixation thereby rupturing the cell membranes The large nuclei can easily be recognized. in the stereomicroscope under transmitted light The nuclei were washed by sucking them up. several times in a micropipette pulled from a 200 il measuring capillary When viewed in the. microscope many nuclei showed no trace of cytoplasm adhering to the nuclear membrane F actin. associated with such nuclei was stained as described above. Electron microscopy, The ultrastructural observations were made during the course of a study concerning the.
ultrastructural differentiation of centripetally migrating follicle cells in stage 10B follicles For. technical details see Heinrich Gutzeit 1985, Table 1 Effect of cytochalasins on cytoplasmic streaming. Inhibitor NC cytoplasm Ooplasmic NC streaming, concentration complete inhibition of streaming release of inhibition. igmP1 streaming after min min after wash min,CyB 10 2 2 n e 2 8. 3 5 n e n d,2 6 n e n d,4 0 n e n d,n d n e 103 n d. 3 5 n e n d,2 0 n e 112 142 n d,CyB 2 1 9 n e 5 5,1 2 n e 3 1.
CyD 2 3 8 n e 1 8,7 5 n e 3 2,8 3 n e 17 1,9 0 n e 14 6 34 6. 2 1 n e n d,CyD 1 13 n e n d,5 1 n e 13 6, In each line the measurements on a single follicle are presented n e no effect during analysed. period 15 30min after cessation of nurse cell streaming n d not determined CyB cyto. chalasin B CyD cytochalasin D NC nurse cell, Drastically reduced streaming but not complete inhibition. 162 H 0 Gutzeit,Inhibition of cytoplasmic streaming. The effect of cytoskeletal inhibitors on cytoplasmic streaming in stage 10B 11. follicles was studied by time lapse film analysis Using an improved flow through. chamber connected to a two way valve the effects of the drugs tested could be. studied in follicles whose normal pattern of streaming had previously been recorded. When follicles were exposed to cytochalasin B or D l lOjigmF 1 the cyto. plasmic streaming from the nurse cells to the oocyte stopped within a few minutes. for qualitative description see Fig 2 for quantitative data Table 1 Appropriate. controls see Materials and Methods showed that this inhibitory effect cannot be. attributed to the small quantities of ethanol or DMSO in the culture medium which. were used as solvents for the applied inhibitors From the first noticeable slow down. of cytoplasmic streaming to its complete cessation it usually took less than 1 min. except in some experiments using cytochalasin D when the inhibition was more. gradual and it took a few minutes longer for cytoplasmic streaming to cease Table. 1 The time until complete inhibition was achieved seemed to depend partly on the. velocity of streaming before the inhibitors were applied follicles with particularly. fast nurse cell streaming of several xms 1 often took a few minutes longer for. inhibition to be complete However the inhibitory effect of cytochalasin B and D on. nurse cell streaming was clearly observed in all follicles analysed Table 1. Surprisingly ooplasmic streaming was not affected by these drugs and continued for. up to roughly 2h Fig 2 Table 1 The final cessation of ooplasmic streaming is. probably not due to the drug action since ooplasmic streaming also stops in normally. developing follicles at the end of vitellogenesis Gutzeit Koppa 1982. When cytochalasin B treated follicles were incubated subsequently in drug free. culture medium the nurse cell plasm resumed its streaming Fig 2 Table 1 and. nurse cell regression continued normally up to stage 12 The reversible inhibition of. nurse cell streaming by cytochalasins gives strong evidence that this process depends. Fig 2 Effect of cytochalasin B cyB on cytoplasmic streaming Drawings from time. lapse films showing the direction of cytoplasmic streaming before and after the admin. istration of cytochalasin B 10 igml Broken arrows indicate direction of streaming. not quantified Unbroken arrows show the velocity of streaming distance covered. within 20s triangles areas with no cytoplasmic streaming nc nuree cells ooc oocyte. fc follicle cells,Micrvfilaments in cytoplasmic streaming 163.
Fig 3 Transient changes in pattern of cytoplasmic streaming Drawings from a time. lapse film showing four subsequent phases of streaming in the nurse cell chamber nc of a. stage 11 follicle Arrows indicate the direction of cytoplasmic streaming velocity not. quantified Duration of each phase 1 5 min A 0 2min B 0 7min c l 9min D. ooc oocyte c follicle cells path of cytoplasm after sudden local contraction in the. nurse cell cytoplasm presumably the cytoplasm is forced to flow around a nurse cell. nucleus A transient reversal in direction of streaming local cytoplasmic motion. lasting for less than ISs and without long range effect. on the activity of microfilaments Colchicine or other microtubule inhibitors had no. effect on nurse cell streaming Gutzeit unpublished data. Transient changes in the pattern of cytoplasmic streaming in regressing nurse cells. During stage 10B the pattern of cytoplasmic streaming in the nurse cells is stable. and the reduction in size of all nurse cells is roughly to scale However in some. exceptional cases late stage 11 and stage 12 follicles showed transient changes in the. pattern of cytoplasmic streaming in the nurse cells These sudden changes appeared. to be due to altered intracellular pressure so that the cytoplasm was forced toflowvia. an alternative route and sometimes a longer route towards the oocyte An example. of this observation is shown in Fig 3 Cytoplasm in a nurse cell was suddenly forced. to reverse its previous direction of streaming and flowed towards the periphery of the. follicle Fig 3B from where it moved anteriorly Fig 3c and finally the diverted. cytoplasm contributed to the central stream of cytoplasm that flowed towards the. oocyte This process took less than 2 min The transient changes in intracellular. pressure of one cell are likely to affect the pattern of streaming in other sister cells. Fig 3B open triangle for possible example In some cases minor local contractions. had no visible long range effect 3c asterisk In follicles treated with cytochalasins. the cytoplasm always became motionless The observed transient changes in nurse. cell streaming are therefore likely to be due to the activity of F actin Although it. was not possible with the available techniques to see directly MF bundles contracting. or possile effects on cell wall or nucleus the occasionally observed sudden pressure. changes in stage 11 12 follicles are compatible with the notion of a contractile. At late stage 12 and stage 13 when cytoplasmic streaming has ceased Gutzeit. Koppa 1982 regressing nurse cell nuclei were frequently seen to become suddenly. deformed to rotate or to change their location in the degenerate nurse chamber The. same observation has also been made in late vitellogenic follicles of the mutant. dicephalic Bohrmann 1981,164 H O Gutzeit, Miavfilament pattern in vitellogenic follicles before cytoplasmic streaming. Since F actin the principal constituent of MF is likely to be the force generating. molecule for cytoplasmic streaming we studied the F actin distribution by staining. follicles with RH phalloidin before during and after the phase of nurse cell. streaming as defined by time lapse films In young vitellogenic follicles stages 7 9. the nurse cell membranes stain intensely The fine network of MF often cannot be. resolved into individual strands see also Frey et al 1984 In stage 10A follicles. which are characterized by the presence of ooplasmic streaming and absence of. nurse cell streaming MF bundles can be identified in the plane of the membrane. Fig 4A c In median optical sections Fig 4B these bundles do not extend into the. nurse cell cytoplasm since only cell membranes stain intensely The only exceptions. Fig 4 Changes in microfilament pattern during stage 10 A C MF pattern in a stage. 10A nurse cell A Upper focus plane of nurse cell membrane B median optical section. arrowheads point to MF associated with ring canals C lower focus plane of nurse cell. membrane Bar 20 an D MF associated with nurse cell membranes of stage 10B 11. follicle Note brightly fluorescent ring ring canal Bar 20 an E Median optical section. of isolated stage 10B nurse cell MF are seen to extend from the plasma membrane. presumably to the nuclear membrane Bar 20 an,Microfilaments in cytoplasmic streaming 165. are MF bundles around the ring canals these bundles extend for some distance into. the nurse cell cytoplasm Fig 4B see also Warn et al 1985. Microfilament distribution at the time of nurse cell streaming. At stage lOB ll when nurse cell streaming is most intense the MF pattern. changes drastically as compared to stage 10A Thick MF bundles can be seen to span. the nurse cell cytoplasm On closer inspection at different focal levels it becomes. apparent that many MF bundles radiate from the nurse cell membrane into the cell. when focused on the level of the nurse cell membrane the contact sites of the MF. bundles with the membrane appear as brightly fluorescent dots Fig 4D from which. the bundles can be seen to extend for some distance into the interior of the nurse cell. In median optical sections MF bundles were seen to traverse the cytoplasm in the. plane of focus Fig 4E in contrast to the situation observed in stage 10A follicles. compare Fig 4B and E In many cases MF bundles terminate at or close to the. nuclear membrane Fig 4E We have identified these MF bundles also in the. electron microscope Fig 5 Casual reference to these structures had been made. previously Giorgi 1976 In the electron microscope we have seen particularly. conspicuous MF bundles in the posterior nurse cells bordering centripetally mi. grated follicle cells an observation that is also corroborated by the RH phalloidin. staining pattern These MF bundles are anchored in cell membrane imaginations of. both nurse cell and adjacent follicle cell Fig 5 suggesting that mechanical strain. acts on these structures Some MF bundles could be followed from the nurse. cell follicle cell border to the region of the nurse cell nucleus. F actin bundles are not distributed homogeneously in the nurse cells Rather in. some areas of a particular nurse cell a large number of conspicuous MF bundles may. be present while in other regions of the same cell few if any can be seen Fig 4D. Fig 5 Ultrastructural identification of microfilament bundles Electron micrograph. showing MF bundles in a nurse cell that borders a centripetally migrated follicle cell fjfc. between the nurse cell cluster and the oocyte Note the infolding of nurse cell and follicle. cell plasma membranes at the base of an MF bundle nc nurse cell Bar 1 an. 166 H 0 Gutzeit, Fig 6 F actin in degenerate nurse cells A Late stage 12 nurse cell chamber with short. and thick MF bundles and aggregates of F actin B Fragment of stage 12 nurse cell. chamber The nuclear membranes of both nuclei are lined with F actin Irregular masses. of F actin are associated with one side of each nucleus only Bars 20 fan. Concomitant with the decrease in nurse cell diameter during stages 10B to 12 the. length of the MF bundles also decreases but at the same time the thickness of the. bundles increases, Follicles were cultured in cytochalasin B containing medium and stained with. RH phalloidin after different incubation times to study the effect of the inhibitor on. the MF pattern The MF bundles did not depolymerize even after 24 h culture. However the MF pattern became gradually abnormal and after a few hours of. incubation MF bundles were often seen to be arranged irregularly around the nurse. cell nuclei without any connection to the cell membranes. Pattern of microfilament distribution after cessation of cytoplasmic streaming. In late stage 12 follicles large and irregularly shaped masses of F actin accumulate. in the nurse cell chambers Fig 6A Warn et al 1985 Since nurse cell membranes. break down at this stage Cummings King 1970 a connection between MF. bundles and the remaining cell membranes can no longer be recognized Much of the. actin appears to be at or in nurse cell nuclei Often actin associates with nuclei in an. asymmetric fashion and only one side of the nuclei is stained brightly Fig 6B. MicrofHaments associated with isolated nuclei, In order to verify that MF bundles indeed associate with the nucleus we broke the.
nurse cells open with tungsten needles and mechanically isolated nuclei of stage. 10B 11 and stage 12 follicles After staining with RH phalloidin MF bundles were. always found to be associated with nuclei albeit in varying quantities In isolated. nuclei of stage 10B and stage 11 follicles MF bundles were found exclusively at the. nuclear membrane Fig 7A In median optical sections F actin forms an often. interrupted ring of staining material around the circumference of the nucleus but no. bundles inside the nucleus are in focus Fig 7B This observation suggests that the. Microfilaments in cytoplasmic streaming 167, stained F actin is mainly or exclusively localized at the nuclear membrane but not. inside the nucleus, During the final phase of nurse cell degeneration however F actin filaments also. appear to be in focus in median optical sections Fig 7c D For this reason. aggregates of F actin may not only be associated with the nuclear membrane but also. be present inside the degenerating nuclei Fig 7D,DISCUSSION. Nurse cell regression is a most rapid process inDrosophila follicles the nurse cell. cytoplasm streams into the oocyte terminal injection where owing to ooplasmic. streaming it becomes rapidly mixed with the ooplasm Nurse cell streaming and. ooplasmic streaming have been postulated to be under different control since onset. and cessation of both processes are different Gutzeit Koppa 1982 This has. been confirmed by the inhibitor studies which show that nurse cell streaming and. ooplasmic streaming can be uncoupled by cytochalasins. Transport of molecules from the nurse cells to the oocyte must also occur in the. absence of cytoplasmic streaming Nurse cell streaming in Drosophila has to be seen. rather as an adaptation to rapid oogenesis than as a principal mechanism for mol. ecular transport In some insects with polytrophic ovaries e g Hyalophora the. phase of terminal injection is never obvserved It has been suggested that in. Hyalophora molecular transport occurs by way of intercellular electrophoresis. Woodruff Telfer 1980 However there is yet no evidence for such a mechanism. in Drosophila follicles Bohrmann Huebner Sander Gutzeit 1986 Cytoskeletal. elements may well be involved in the localization of molecules at specific sites within. the egg as has been demonstrated in other species for the differentiation of the germ. plasm Gutzeit 1985 Strome Wood 1983, Fig 7 Microfilament bundles attached to isolated nuclei F actin associated with. isolated nuclei of stage 10B follicles A B and stage 12 follicle C D A C top view focus. in plane of nuclear membrane B D median optical section Arrows in B point to F actin. lining the nuclear membrane Bar A D 20 tfn,168 H 0 Gutzeit.
The reversible inhibition of cytoplasmic streaming by cytochalasins gives indirect. support for a contractile mechanism Cytoplasmic streaming and cell locomotion in a. number of different cell types have been studied intensively and a role of the MF. network in these processes has been clearly demonstrated in some systems for recent. reviews see Taylor Condeelis 1979 Schliwa 1984 However the exact mech. anisms are still poorly understood In the myxomycete plasmodium Physarum. polycephalum cytoplasmic streaming has been thoroughly analysed reviewed by. Kamiya 1981 In principle local contractions of membrane bound actin filaments. are thought to lead to local differences in the internal pressure thus resulting in. cytoplasmic streaming pressure flow When the cytoplasmic strand of Physarum is. induced to contract isometrically MF bundles appear in the cytoplasm during the. contraction phase Wohlfarth Bottermann Fleischer 1976 MF bundles can. actively contract in situ as well as after laser micro dissection Isenberg Rathke. Hiilsmann Franke Wohlfarth Bottermann 1976 If the MF bundles seen in. Dmsophila follicles at the time of nurse cell streaming are contractile structures a. similar pressure flow mechanism as in the myxomycete plasmodium may be. The arrangement and anchoring of MF bundles suggest that cell membrane and. nuclear membrane transmit the force generated by MF contractions onto the. cytoplasm which owing to increased pressure is forced to flow out of the nurse cell. through the cytoplasmic bridge s into the oocyte Nurse cell streaming begins in the. proximal nurse cells at stage 10B Gutzeit Koppa 1982 If pressure is generated. in all nurse cells at the same time only those cells that are connected directly to the. oocyte by ring canals proximal nurse cells are expected to show cytoplasmic. streaming at the beginning of the contraction phase As the pressure in these nurse. cells decreases owing to the loss of cytoplasm streaming in more distal nurse cell. begins as seen in in time lapse films Gutzeit Koppa 1982. The uniform regression of nurse cells during stages 10B 12 implies that the. suggested contractile MF system must be highly regulated and dynamic to ensure. that all cells function in concert The simultaneous and uniform regression of the. nurse cells is complicated by the fact that all cells are densely packed and conse. quently often irregularly shaped Furthermore if neighbouring nurse cells belong to. different nurse cell families Frey et al 1984 their cytoplasm must stream into the. oocyte via different routes Because of the inferred dynamic regulatory mechanisms. we are likely to visualize in our preparations only the momentary MF pattern at the. time of fixation, Transient changes in the streaming pattern during stages 11 and 12 when masses. of MF bundles accumulate in the degenerating nurse cells give further indirect. evidence for cytoplasmic streaming by way of a contractile mechanism based on. On present evidence alternative explanations for nurse cell streaming in. Drosophila are conceivable Yet the concept of pressure flow although only. supported by circumstantial evidence appears most attractive. Microfilaments in cytoplasmic streaming 169, The excellent technical assistance of Mrs M Stubbe is acknowledged Fig 5 was kindly. contributed by Ulf R Heinrich I am grateful to Professor K Sander for his support and critical. reading of the manuscript This work was supported by the D F G. REFERENCES, BOHRMANN J 1981 Entwicklung der Follikel der Drosophila Mutante dicephalic in vitro. Staatsexamensarbeit FakultSt fur Biologie Universitfit Freiburg. BOHRMANN J HUEBNER E SANDER K GUTZEIT H 1986 Intracellular electrical potential. measurements in Drosophila follicles J Cell Sci 81 in press. CUMMINGS M R KING R C 1970 Ultrastructural changes in nurse and follicle cells during. late stages of oogenesis in Drosophila melanogaster Z Zellforsch mikrosk Anat 110 1 8. FREY A SANDER K GUTZEIT H 1984 The spatial arrangement of germ line cells in. ovarian follicles of the mutant dicephalic in Drosophila melanogaster Wilhelm Roux Arch Devi. Biol 193 388 393, GIORGI F 1976 Ultrastructural observations on the degenerating nurse cells of late ovarian. chambers of Drosophila melanogaster Ada embryol exp 2 225 236. GUTZEIT H O 1985 Oosome formation during in vitro oogenesis in Bradysia tritici syn. Sciara ocellaris Wilhelm Roux Arch Devi Biol 194 404 410. GUTZEIT H O KALTENBACH L 1985 An improved flow through chamber for time lapse. film analysis of of oogenesis and embryogenesis Experientia 41 527 528. GUTZEIT H O KOPPA R 1982 Time lapse film analysis of cytoplasmic streaming during. late oogenesis of Drosophila J Embryol exp Morph 67 101 111. HEINRICH U R GUTZEIT H O 1985 Characterization of cation rich follicle cells in. vitellogenic follicles of Drosophila melanogaster Differentiation 28 237 243. ISENBERG G RATHKE P C HULSMANN N FRANKE W W WOHLFARTH BOTTERMANN. K E 1976 Cytoplasmic actomyosin fibrils in tissue culture cells Direct proof of contractility. by visualisation of ATP induced contraction in fibrils isolated by laser microbeam dissection. Cell Tiss Res 166 427 443, KAMIYA N 1981 Physical and chemical basis of cytoplasmic streaming A Rev PI Physiol 32.
KING R C 1970 Ovarian development in Drosophila melanogaster New York Academic. LOHS SCHARDIN M 1982 Dicephalic Drosophila mutant affecting polarity in follicle. organization and embryonic patterning Willhelm Roux Arch Devi Biol 191 28 36. ROBB J A 1969 Maintenance of imaginal discs of Drosophila melanogaster in chemically. defined media J Cell Biol 41 876 885, SCHLIWA M 1984 Mechanisms of intracellular organelle transport In Cell and Muscle Motility. vol 5 The Cytoskeleton ed J W Shay pp 1 82 New York London Plenum Press. STROME S WOOD W B 1983 Generation of asymmetry and segregation of germ line. granules in early C elegans embryos Cell 35 15 25, TAYLOR D L CONDEELIS J S 1979 Cytoplasmic structure and contractility in amoeboid. cells Int Rev Cytol 56 57 114, WARN R M GUTZEIT H O SMITH L WARN A 1985 F actin rings are associated with. the Drosophila egg chamber canals Expl Cell Res 157 355 363. WOHLFARTH BOTTERMANN K E FLEISCHER M 1976 Cycling aggregation patterns of. cytoplasmic F actin coordinated with oscillating tension force generation Cell Tiss Res 165. WOODRUFF R J TELFER W H 1980 Electrophoresis of proteins in intercellular bridges. Nature Land 286 84 86,Received 25 May 1985 Accepted 16 July 1985.

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