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Physical and Chemical Basis of Cytoplasmic Streaming

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Physical and Chemical Basis of Cytoplasmic Streaming Annual Reviews www.annualreviews.org/aronline .4n~t Rev. Plant Physiol 1981. 32:205-36 Copyright© 1981by AnnualReviews In~ All rights reserved PHYSICAL AND CHEMICAL BASIS OF CYTOPLASMIC ~7710 STREAMING Nobur6 Kamiya Department of Cell Biology, National Institute for Basic Biology, Okazaki, 444 Japan CONTENTS INTRODUCTION........................................................................................................ 206 SHUTI’LE STREAMINGIN THE MYXOMYCETEPLASMODIUM ................ 207 General...................................................................................................................... 207 ContractileProperties of the PlasmodialStrand ...................................................... 208 Activationcaused by stretching .................................................................................. 208 Activationcaused by loading .................................................................................... 209 Synchronizationof local ,hythms .............................................................................. 209 ContractileProteins .................................................................................................. 210 Plasmodiumactomyosin .......................................................................................... 210 Plusmodiummyosin ................................................................................................ 210 Plusmodiumactin.................................................................................................... 211 by STEWARD OBSERVATORY on 04/23/06. For personal use only. Tension Production of Reconstituted Actomyosin Threads from Physarum............ 212 Regulationof Movement .......................................................................................... 213 Therole of Ca ~...................................................................................................... 213 Therole of ATP ...................................................................................................... 214 StructuralBasis of MotiliO~...................................................................................... 216 Annu. Rev. Plant. Physiol. 1981.32:205-236. Downloaded from arjournals.annualreviews.org Contraction-relaxationcycleand actln transformations................................................ 216 FibrillogenesiS........................................................................................................ 217 Birefringence.......................................................................................................... 217 Summary.................................................................................................................. 218 ROTATIONALSTREAMING IN CHARACEANCELLS .................................... 219 General...................................................................................................................... 219 TheSite of MotiveForce Generation ........................................................................ 219 Subcortical Filaments, Their Identification as Actin, and Their Indispensability forStreaming .......................................................................................... 220 NitellaMyosin and its Localizationin the Cell ...................................................... 221 Motility of Fibrils and Organellesin Isolated CytoplasmicDroplets ...................... 222 Rotationof chloroplasts ............................................................................................ 222 Motilefibrils .......................................................................................................... 223 2O5 0066-4294/81/0601-0205501.00 Annual Reviews www.annualreviews.org/aronline 206 KAMIYA DemembranatedModelSystems .............................................................................. 224 Removaloftonoplast byuacuolar perfu~ion ................................................................ 224 Demembronatedcytoplasmicdroplets ........................................................................ 224 Activemovement in vitro of cytoplasmicflbeCls ............................................................ 225 Measurementof theMoti~e Force ............................................................................ 225 Centrifugationmethod............................................................................................ 226 Perfusionmetkod .................................................................................................... 226 Methodoflateral compassion .................................................................................. 227 MolecularMechanism of Rotational Streaming ...................................................... 228 CONCLUDINGREMARKS...................................................................................... 229 INTRODUCTION Twodecades have elapsed since this author wrote a review on cytoplasmic streaming for VolumeI 1 of this series (72). As is the case with other types of cell motility, research on cytoplasmic streaming has madegreat strides during this period--including isolating proteins related to streaming, eluci- dating its ultrastructural background, and developing new effective meth- ods for studying functional aspects of cytoplasmic streaming. There are a numberof reviews and symposia reports dealing with various aspects ofnonmuscularcell motility including cytoplasmic streaming (8, 10, 11, 23, 28, 31, 36, 48, 53, 59, 60, 62, 99, 100, 134, 136, 139, 15o, 151, 159). They will provide readers with more comprehensive information on the subject. In this report, I shall limit myconsideration to someselected topics in cytoplasmic streaming, focusing on its mechanismat the cellular and molecular levels. Generally speaking, minute structural shifts in the cytoplasm maybe a wide oecurrance in living cells, but they will not necessarily develop into significant movementunless they are coordinated. In a variety of cells, cytoplasmic particles are knownto make sudden excursions over distances too extensive to be accounted for as Brownianmotion (136). Such motions, called "saltatory movements,"were described long ago in plant literature by STEWARD OBSERVATORY on 04/23/06. For personal use only. as "Glitchbewegung" or "Digressionsbewegung" (of 71, 73). The move- ment of the particles is erratic and haphazard, yet it is not totally devoid of directional control as it would be in Brownianmotion. Accordingto the Annu. Rev. Plant. Physiol. 1981.32:205-236. Downloaded from arjournals.annualreviews.org degree of orderliness, intraeellular streaming manifests various patterns (71, 73). Cytoplasmic movementsexhibited by eukaryotic cells maybe classified into two major groups with respect to the proteins involved, i.e. the actin- myosin system and the tubulin-dynein system. Cytoplasmic streaming be- longs mostly to the first group. Possible roles for the tubulin-dynein system in cytoplasmic streaming have yet to be investigated. Fromthe phenomeno- logical point of view, it is customaryto classify the streaming of cytoplasm at the visual level into two major categories. One is the streaming closely associated with changes in cell form. This type of movementis usually Annual Reviews www.annualreviews.org/aronline CYTOPLASMIC STREAMING 207 referred to as amoeboid movementand is represented by the amoeba, acellnlar slime molds, and manyother systems. The other is the streaming not dependentupon changesin the external cell shape, as in most plant cells or dermatoplasts. In the following sections, I shall discuss the two best studied cases as representative modelsof cytoplasmic streaming. Oneis shuttle streaming in myxomyceteplasmodia of the amoeboid type, and the other is rotational streaming in eharacean cells of the other type. It is necessary to describe them separately because we still do not knowat what organizational level these two major categories of streaming share a commonmechanism. SHUTTLE STREAMING IN THE MYXOMYCETE PLASMODIUM General The plasmodium of myxomycetes, especially that of Physarum polyceph- alum, is classic material in whichthe physiology, biochemistry, biophysics, and ultrastructure of cytoplasmic streaming have been investigated most extensively (20, 35, 36, 71, 99, 133). The myxomyceteplasmodium shows various characteristic features in its cytoplasmic streaming. The rate of flow, as well as the amountof cytoplasm carded along with the streaming, is exceedingly great comparedwith ordi- nary cytoplasmic streaming in plant calls (71). Moreover, the direction streaming alternates according to a rhythmic pattern. There is good evi- dence to show that the flow of endoplasmis caused passively by a local difference in the intraplasmodial pressure (83). This differential pressure the motive force responsible for the streaming. It can be measuredby the so-called double-chambermethod, in which counterpressure just sutfieient to keep the endoplasm immobileis applied (70, 71). by STEWARD OBSERVATORY on 04/23/06. For personal use only. The waves representing spontaneous changes in the motive force are sometimesvery regular, but the amplitude of the waves often increases and decreases like beat waves. In someother cases, a peculiar wavepattern is Annu. Rev. Plant. Physiol. 1981.32:205-236. Downloaded from arjournals.annualreviews.org repeated over several waves. These waves can be reeonstrneted closely enough with only a few overlapping sine waves of appropriate periods, amplitudes and phases. This fact is interpreted as
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