Skip to main content
Log in

Endocytic transit inDictyostelium discoideum

  • Focus on Cellular Biochemistry
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The cells ofDictyostelium discoideum are soil amoebae with a simple endocytic pathway: Particles or fluid are taken up at the plasma membrane in a process dependent on the actin cytoskeleton. After rapid acidification and subsequent neutralisation of the food vacuoles during which breakdown of the contents occurs, indigestible remnants are exocytosed. This tight coupling between endocytosis and exocytosis is thought to maintain membrane homeostasis. In spite of the apparent overall difference between the endocytic pathways of mammalian cells andD. discoideum, conserved proteins are involved in individual steps of endocytic transport, possibly indicating that in mammalian cells it is only the routing of marker that has evolved from a simple transit to a complex, branched pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adessi C, Chapel A, Vincon M, Rabilloud T, Klein G, Satre M, Garin J (1995) Identification of major proteins associated withDictyostelium discoideum endocytic vesicles. J Cell Sci 108: 3331–3337

    Google Scholar 

  • Aubry L, Klein G, Martiel JL, Satre M (1993) Kinetics of pH evolution inDictyostelium discoideum. J Cell Sci 105: 861–866

    Google Scholar 

  • Bracco E, Peracino B, Noegel AA, Bozzaro S (1997) Cloning and transcriptional regulation of the gene encoding the vacuolar H+-ATPase B-subunit ofDictyostelium discoideum. FEBS Lett 419: 37–40

    Google Scholar 

  • Buczynski G, Bush J, Zhang L, Rodriguez-Paris J, Cardelii J (1997) Evidence for a recycling role for rab7 in regulating a late step in endocytosis and in retention of lysosomal enzymes inDictyostelium discoideum. Mol Biol Cell 8: 1343–1360

    Google Scholar 

  • Bush J, Nolta K, Rodriguez-Paris J, Kaufmann N, O'Halloran T, Ruscetti T, Temesvari L, Steck T, Cardelli J (1994) A rab4-like GTPase inDictyostelium discoideum colocalizes with V-H+ATPases in reticular membranes of the contractile vacuole complex and in lysosomes. J Cell Sci 107: 2801–2812

    Google Scholar 

  • —, Temesvari L, Rodriuez-Paris J, Buczynski G, Cardelli JA (1996) A role for a rab4-like GTPase in endocytosis and in regulation of contractile vacuole structure and function inDictyostelium. Mol Biol Cell 7: 1623–1638

    Google Scholar 

  • Cox D, Wessels D, Soll DR, Hartwig J, Condeelis J (1996) Reexpression of ABP-120 rescues cytoskeletal, motility, and phagocytosis defects of ABP-120 Dictyostelium mutants. Mol Biol Cell 7: 803–823

    Google Scholar 

  • De Camilli P, Benfenati F, Valtorta F, Greengard P (1990) The synapsins. Annu Rev Cell Biol 6: 433–460

    Google Scholar 

  • de Chastellier C, Ryter A, Thilo L (1983) Membrane shuttle between plasma membrane, phagosomes, and pinosomes inDictyostelium discoideum amoeboid cells. Eur J Cell Biol 30: 233–243

    Google Scholar 

  • de Hostos EL, Bradtke B, Lottspeich F, Guggenheim R, Gerisch G (1991) Coronin, an actin binding protein ofDictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein β subunits. EMBO J 10: 4097–4104

    Google Scholar 

  • Dowrick P, Kenworthy P, McCann B, Warn R (1993) Circular ruffle formation and closure lead to macropinocytosis in hepatocyte growth factor/scatter factor treated cells. Eur J Cell Biol 61: 44–53

    Google Scholar 

  • Fukui Y, Lynch TJ, Brzeska H, Korn ED (1989) Myosin I is located at the leading edges of locomotingDictyostelium amoebae. Nature 341: 328–331

    Google Scholar 

  • Furukawa R, Fechheimer M (1994) Differential localization of α-actinin and the 30-kD actin-bundling protein in the cleavage furrow, phagocytic cup, and contractile vacuole ofDictyostelium discoideum. Cell Motil Cytoskeleton 29: 46–56

    Google Scholar 

  • Goode BL, Wong JJ, Butty AC, Peter M, McCormack AL, Yates JR, Drubin DG, Barnes G (1999) Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J Cell Biol 144: 83–98

    Google Scholar 

  • Greenberg S, Burridge K, Silverstein S (1990) Colocalization of F-actin and talin during Fc receptor-mediated phagocytosis in mouse macrophages. J Exp Med 172: 1853–1856

    Google Scholar 

  • Grogan A, Reeves E, Keep N, Wientjes F, Trotty N, Burlingame AL, Hsuan JJ, Segal AW (1997) Cytosolic phox proteins interact with and regulate the assembly of coronin in neutrophils. J Cell Sci 110: 3071–3081

    Google Scholar 

  • Hacker U, Albrecht R, Maniak M (1997) Fluid-phase uptake by macropinocytosis inDictyostelium. J Cell Sci 110: 105–112

    Google Scholar 

  • Haugwitz M, Noegel AA, Karakesisoglou J, Schleicher M (1994)Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell 79: 303–314

    Google Scholar 

  • Heuser J, Zhu Q, Clarke M (1993) Proton pumps populate the contractile vacuoles ofDictyostelium amoebae. J Cell Biol 121: 1311–1327

    Google Scholar 

  • Jenne N, Rauchenberger R, Hacker U, Kast T, Maniak M (1998) Targeted gene disruption reveals a role for vacuolin B in the late endocytic pathway and exocytosis. J Cell Sci 111: 61–70

    Google Scholar 

  • Laurent O, Bruckert F, Adessi C, Satre M (1998) In-vitro reconstitutedDictyostelium discoideum early endosome fusion is regulated by rab7 but proceeds in the absence of ATP-Mg2+ from the bulk solution. J Biol Chem 273: 793–799

    Google Scholar 

  • Lenhard JM, Mayorga L, Stahl PD (1992) Characterization of endosome-endosome fusion in a cell-free system usingDictyostelium discoideum. J Biol Chem 267: 1896–1903

    Google Scholar 

  • Ludin B, Matus A (1998) GFP illuminates the cytoskeleton. Trends Cell Biol 8: 72–77

    Google Scholar 

  • Maniak M (1999) Green fluorescent protein in the visualisation of particle uptake and fluid-phase endocytosis. Methods Enzymol 302: 43–50

    Google Scholar 

  • —, Rauchenberger R, Albrecht R, Murphy J, Gerisch G (1995) Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein tag. Cell 83: 915–924

    Google Scholar 

  • Mellman I (1996) Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12: 575–625

    Google Scholar 

  • Niewöhner J, Weber I, Maniak M, Müller-Taubenberger A, Gerisch G (1997) Talin-null cells ofDictyostelium are strongly defective in adhesion to particle and substrate surfaces and slightly impaired in cytokinesis. J Cell Biol 138: 349–361

    Google Scholar 

  • Nolta KV, Rodriguez-Paris JM, Steck TL (1994) Analysis of successive endocytic compartments isolated fromDictyostelium discoideum by magnetic fractionation. Biochim Biophys Acta 1224: 237–246

    Google Scholar 

  • Novick P, Zerial M (1997) The diversity of rab proteins in vesicle transport. Curr Opin Cell Biol 9: 496–504

    Google Scholar 

  • O'Halloran TJ, Anderson RGW (1992) Clathrin heavy chain is required for pinocytosis, the presence of large vacuoles and development inDictyostelium. J Cell Biol 118: 1371–1377

    Google Scholar 

  • Ostap EM, Pollard TD (1996) Overlapping functions of myosin-I isoforms. J Cell Biol 133: 221–224

    Google Scholar 

  • Padh H, Lavasa M, Steck TL (1989) Prelysosomal acidic vacuoles inDictyostelium discoideum. J Cell Biol 108: 865–874

    Google Scholar 

  • —, Ha J, Lavasa M, Steck TL (1993) A post-lysosomal compartment inDictyostelium discoideum. J Biol Chem 268: 6742–6747

    Google Scholar 

  • Peracino B, Borleis J, Jin T, Westphal M, Schwartz JM, Wu L, Bracco E, Gerisch G, Devreotes P, Bozzaro S (1997) G protein β subunitnull mutants are impaired in phagocytosis and chemotaxis due to inappropriate regulation of the actin cytoskeleton. J Cell Biol 141: 1529–1537

    Google Scholar 

  • Prassler J, Stocker S, Marriott G, Heidecker M, Kellermann J, Gerisch G (1996) Interaction of aDictyostelium member of the plastin/flmbrin family with actin filaments and actin-myosin complexes. Mol Biol Cell 8: 83–95

    Google Scholar 

  • Rauchenberger R, Hacker U, Murphy J, Niewöhner J, Maniak M (1997) Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment inDictyostelium. Curr Biol 7: 215–218

    Google Scholar 

  • Rivero F, Furukawa R, Noegel AA, Fechheimer M (1996a)Dictyostelium discoideum cells lacking the 34,000-dalton actinbinding protein can grow, locomote, and develop, but exhibit defects in regulation of cell structure and movement: a case of partial redundancy. J Cell Biol 135: 965–980

    Google Scholar 

  • —, Köppel B, Peracino B, Bozzaro S, Siegert F, Weijer CF, Schleicher M, Albrecht R, Noegel AA (1996b) The role of the cortical cytoskeleton: F-actin crosslinking proteins protect against osmotic stress, ensure cell size, cell shape and motility, and contribute to phagocytosis and development. J Cell Sci 109: 2679–2691

    Google Scholar 

  • Ruscetti T, Cardelli JA, Niswonger ML, O'Halloran TJ (1994) Clathrin heavy-chain functions in sorting and secretion of lysosomal-enzymes inDictyostelium discoideum. J Cell Biol 126: 343–352

    Google Scholar 

  • Rybin V, Ullrich O, Rubino M, Alexandrow K, Simon I, Seabra MC, Goody R, Zerial M (1996) GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature 383: 266–269

    Google Scholar 

  • Souza GM, Metha DP, Lammertz M, Rodriuez-Paris J, Wu R, Cardelli JA, Freeze HH (1997)Dictyostelium lysosomal proteins with different sugar modifications sort to functionally distinct compartments. J Cell Sci 110: 2239–2248

    Google Scholar 

  • Swanson JA, Baer SC (1995) Phagocytosis by zippers and triggers. Trends Cell Biol 5: 89–93

    Google Scholar 

  • —, Watts C (1995) Macropinocytosis. Trends Cell Biol 5: 424–428

    Google Scholar 

  • Temesvari L, Rodriguez-Paris J, Bush J, Steck TL, Cardelli J (1994) Characterization of lysosomal membrane-proteins ofDictyostelium discoideum: a complex population of acidic integral membrane-glycoproteins, rab GTP-binding proteins and vacuolar ATPase subunits. J Biol Chem 269: 25719–25727

    Google Scholar 

  • — — —, Zhang L, Cardelli JA (1996) Involvement of the protontranslocating ATPase in multiple steps of the endo-lysososmal system and in the contractile vacuole system ofDictyostelium discoideum. J Cell Sci 109: 1479–1495

    Google Scholar 

  • Veithen A, Cupers P, Baudhuin P, Courtoy PJ (1996) V-src induces constitutive macropinocytosis in rat fibroblasts. J Cell Sci 109: 2005–2012

    Google Scholar 

  • Vogel G, Thilo L, Schwarz H, Steinhart R (1980) Mechanism of phagocytosis inDictyostelium discoideum: phagocytosis is mediated by different recognition sites as disclosed by mutants with altered phagocytic properties. J Cell Biol 86: 456–465

    Google Scholar 

  • Wienke DC, Knetsch MLW, Neuhaus EM, Reedy MC, Manstein DJ (1999) Disruption of a dynamin homologue affects endocytosis, organelle morphology and cytokinesis inDictyostelium discoideum. Mol Biol Cell 10: 225–243

    Google Scholar 

  • Witke W, Schleicher M, Noegel AA (1992) Redundancy in the microfilament system: abnormal development ofDictyostelium cells lacking two F-actin cross-linking proteins. Cell 68: 53–62

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maniak, M. Endocytic transit inDictyostelium discoideum . Protoplasma 210, 25–30 (1999). https://doi.org/10.1007/BF01314951

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01314951

Keywords

Navigation