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Golgi-membrane dynamics are cytoskeleton dependent: A study on Golgi stack movement induced by brefeldin A

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Summary

Brefeldin A (BFA) induces a major aggregation of the Golgi apparatus (GA) in root cells followed by a complete, but reversible, vesiculation of the Golgi stacks which form two or more BFA compartments in the cytosol. This effect is monitored by the immunofluorescence of a Golgi antigen stained with a monoclonal antibody JIM 84, and by transmission electron microscopy. Depolymerisation of the microtubule cytoskeleton after oryzalin or colchicine treatment does not disturb the three dimensional organisation of the GA in control cells and does not affect any BFA induced Golgi stack movements. After disruption of the actin cytoskeleton with cytochalasin D many aggregates of Golgi stacks can be observed in root cells and these are sensitive to BFA treatment, forming multiple BFA compartments. N-ethyl-maleimide has no effect on the organisation of the GA in control roots but totally inhibits the action of BFA. Thus, it appears that spatial organisation of the GA and the BFA induced Golgi stack movements are actin dependent whilst BFA induced vesiculation of the GA is a structurally separate event.

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References

  • Betina V (1992) Biological effects of the antibiotic brefeldin A (Decumbin, Cyanein, Ascotoxin, Synergisidin): a retrospective. Folia Microbiol 37: 3–11

    Google Scholar 

  • Bourett TM, Howard RJ (1996) Brefeldin A-induced structural changes in the endomembrane system of a filamentous fungus,Magnaporthe grisea. Protoplasma 190: 151–163

    Google Scholar 

  • Cole NB, Lippincott-Schwartz J (1995) Organization of organelles and membrane traffic by microtubules. Curr Opin Cell Biol 7: 55–65

    Google Scholar 

  • Doms RW, Russ G, Yewdell JW (1989) Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J Cell Biol 24: 61–72

    Google Scholar 

  • Driouich A, Zhang GF, Staehelin AL (1993) Effect of Brefeldin A on the structure of GA and on the synthesis and secretion of proteins and polysaccharides in sycamore maple (Acer pseudoplatanus) suspension-cultured cells. Plant Physiol 101: 1363–1373

    Google Scholar 

  • Fowke LC, Tanchak MA, Galway ME (1991) Ultrastructural cytology of the endocytotic pathway in plants. In: Hawes CR, Coleman JOD, Evans DE (eds) Endocytosis, exocytosis and vesicle traffic in plants. Cambridge University Press, Cambridge, pp 15–40

    Google Scholar 

  • Fujiwara T, Oda K, Yokota S, Takatsuki A, Ikehara Y (1988) Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J Biol Chem 263: 18545–18552

    Google Scholar 

  • Grolig F (1990) Actin-based organeile movements in interphase spirogyra. Protoplasma 155: 29–42

    Google Scholar 

  • Hawes C (1991) Stereo-electron microscopy. In: Hall JL, Hawes C (eds) Electron microscopy of plant cells. Academic Press, San Diego, pp 67–85

    Google Scholar 

  • Helms JB, Rothman JE (1992) Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360: 352–354

    Google Scholar 

  • Horsley D, Coleman J, Evans D, Crooks K, Peart J, Satiat-Jeunemaitre B, Hawes C (1993) A monoclonal antibody, JIM 84, recognizes the GA and plasma membrane in plant cells. J Exp Bot 44: 223–229

    Google Scholar 

  • Juniper BE, Horne C, Hawes CR (1981) The relationships between the dictyosomes and the forms of endoplasmic reticulum in plant cells with different export programs. Bot Gaz 143: 135–145

    Google Scholar 

  • Kachar B, Reese T (1988) The mechanisms of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actinfilaments. J Cell Biol 106: 1545–1552

    Google Scholar 

  • Kakimoto T, Shibaoka H (1988) Cytoskeletal ultrastracture of phragmoplast-nuclei complexes isolated from cultured tobacco cells. Protoplasma Suppl 2: 95–103

    Google Scholar 

  • Klausner RD, Donaldson JG, Lippincott-Schwartz J (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116: 1071–1080

    Google Scholar 

  • Kreis TE (1990) Role of microtubules in the organisation of the GA. Cell Motil Cytoskeleton 15: 67–70

    Google Scholar 

  • — (1992) Regulation of vesicular and tubular membrane traffic of the Golgi complex by coat proteins. Curr Opin Cell Biol 4: 609–615

    Google Scholar 

  • Lancelle SA, Hepler PK (1988) Cytochalasin-induced ultrastructural alterations inNicotiana pollen tubes. Protoplasma Suppl 2: 65–75

    Google Scholar 

  • Lichtscheidl IK, Lancelle SA, Hepler PK (1990) Actin-endoplasmic reticulum complexes inDrosera. Their structural relationship with the plasmalemma, nucleus, and organelles in cells prepared by high pressure freezing. Protoplasma 155: 116–126

    Google Scholar 

  • Liebe S, Quader H (1994) Myosin in onion (Allium cepa) bulb scale epidermal cells: involvement in dynamics of organelles and endoplasmic reticulum. Physiol Plant 90: 114–124

    Google Scholar 

  • Lippincott-Schwartz J, Yuan L, Bonifacino J, Klausner R (1989) Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56: 801–813

    Google Scholar 

  • —, Donaldson JG, Schweizer A, Berger EG, Hauri HP, Yuan LC, Klausner RD (1990) Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60: 821–836

    Google Scholar 

  • —, Yuan L, Tipper C, Amherdt M, Orci L, Klausner R (1991) Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67: 601–616

    Google Scholar 

  • —, Cole NB, Marotta A, Conrad PA, Bloom GS (1995) Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J Cell Biol 128: 293–306

    Google Scholar 

  • Malhotra V, Orci L, Glick BS, Block M, Rothman JE (1988) Role of an N-ethylmaleimide-sensitive transport component in promoting fusion of transport vesicles with cisternae of the Golgi stacks. Cell 54: 221–227

    Google Scholar 

  • Menzel D (1994) Dynamics and pharmacological perturbations of the endoplasmic reticulum in the unicellular green algaAcetabularia. Eur J Cell Biol 64: 113–119

    Google Scholar 

  • Mollenhauer HH, Morré DJ (1976) Cytochalasin B, but not colchicine inhibits migration of secretory vesicles in root tips of maize. Protoplasma 87: 39–48

    Google Scholar 

  • — — (1994) Structure of Golgi apparatus. Protoplasma 180: 14–28

    Google Scholar 

  • Palevitz BA (1988) Cytochalasin-induced reorganization of actin inAllium root cells. Cell Motil Cytoskeleton 9: 283–298

    Google Scholar 

  • Park J, Miller C, Anderton BH (1986) Higher plant myosin heavychain identified using a monoclonal antibody. Eur J Cell Biol 41: 9–13

    Google Scholar 

  • Pemrick S, Weber A (1976) Mechanism of inhibition of relaxation by N-ethylmaleimide treatment of myosin. Biochemistry 15: 5193–5198

    Google Scholar 

  • Picton JM, Steer MW (1983) The effect of cycloheximide on dictyosome activity inTradescantia pollen tubes determined using cytochalasin D. Eur J Cell Biol 29: 133–138

    Google Scholar 

  • Quader H (1990) Formation and disintegration of cisternae of the endoplasmic reticulum visualized in live cells by conventional fluorescence and confocal laser scanning microscopy: evidence for the involvement of calcium and the cytoskeleton. Protoplasma 155: 166–175

    Google Scholar 

  • —, Hofmann A, Schnepf E (1987) Shape and movement of the endoplasmic reticulum in onion bulb epidermis cells: possible involvement of actin. Eur J Cell Biol 44: 17–26

    Google Scholar 

  • — — — (1989) Reorganisation of the endoplasmic reticulum in epidermal cells of onion bulb scales after cold stress: involvement of cytoskeletal elements. Planta 177: 273–280

    Google Scholar 

  • Rambourg A, Clermont Y, Jackson CL, Képès F (1995) Effects of brefeldin A on the three-dimensional structures of the GA in a sensitive strain ofSaccharomyces cerevisiae. Anat Re 24: 1–9

    Google Scholar 

  • Rothman JE (1984) Mechanisms of intracellular protein transport. Nature 372: 55–63

    Google Scholar 

  • —, Orci L (1992) Molecular dissection of the secretory pathway. Nature 355: 409–415

    Google Scholar 

  • Salitz A, Schmilz K (1989) Influence of microfilament and microtubule inhibitors applied by immersion and microinjection on circulation streaming in the staminal hairs ofTradescantia blossfeldiana. Protoplasma 153: 37–45

    Google Scholar 

  • Satiat-Jeunemaitre B, Hawes C (1992a) Reversible dissociation of the plant Golgi apparatus by brefeldin A. Biol Cell 74: 325–328

    Google Scholar 

  • — — (1992b) Redistribution of a Golgi glycoprotein in plant cells treated with brefeldin A. J Cell Sci 103: 1153–1156

    Google Scholar 

  • — — (1993a) The distribution of secretory products in plant cells is affected by brefeldin A. Cell Biol Int 17: 183–193

    Google Scholar 

  • — — (1993b) Insights into the secretory pathway and vesicular transport in plant cells. Biol Cell 79: 7–15

    Google Scholar 

  • — — (1994) G.A.T.T. (a General Agreement on Traffic and Transport) and brefeldin A in plant cells. Plant Cell 6: 463–467

    Google Scholar 

  • Schindler T, Bergfeld R, Hohl M, Schopfer P (1994) Inhibition of Golgi apparatus function by brefeldin A in maize coleoptiles and its consequences on auxin mediated growth, cell-wall extensibility, and secretion of cell wall proteins. Planta 192: 404–413

    Google Scholar 

  • Schroer TA, Sheetz MP (1991) Functions of microtubule-based motors. Annu Rev Physiol 53: 629–652

    Google Scholar 

  • Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148: 80–86

    Google Scholar 

  • Staiger CJ, Schliwa M (1987) Actin localization and function in higher plants. Protoplasma 141: 1–12

    Google Scholar 

  • Steer MW, O'Driscoll D (1991) Vesicle dynamics and membrane turnover in plant cells. In: Hawes C, Coleman J, Evans D (eds) Endocytosis, exocytosis and vesicle traffic in plants. Cambridge University Press, Cambridge, pp 129–142

    Google Scholar 

  • Williamson RE (1993) Organelle movements. Annu Rev Plant Physiol Plant Mol Biol 44: 181–202

    Google Scholar 

  • Wood SA, Park JE, Brown WJ (1991) Brefeldin A causes a microtubulemediated fusion of the trans-Golgi network and early endosomes. Cell 67: 591–600

    Google Scholar 

  • Yokota E, McDonald AR, Liu B, Shimmen T, Palevitz BA (1995) Localization of a 170 kDa myosin heavy chain in plant cells. Protoplasma 185: 178–187

    Google Scholar 

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  1. B. Satiat-Jeunemaitre

    Present address: Institut des Sciences Végétales, CNRS, Bât. 23-24, Avenue de la Terrasse, F-91198, Gif sur Yvette Cedex, France

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  1. School of Biological and Molecular Sciences, Oxford Brookes University, Oxford

    B. Satiat-Jeunemaitre, C. Steele & C. Hawes

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  3. C. Hawes
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Satiat-Jeunemaitre, B., Steele, C. & Hawes, C. Golgi-membrane dynamics are cytoskeleton dependent: A study on Golgi stack movement induced by brefeldin A. Protoplasma 191, 21–33 (1996). https://doi.org/10.1007/BF01280822

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  • DOI: https://doi.org/10.1007/BF01280822

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