, Volume 210, Issue 1–2, pp 25–30 | Cite as

Endocytic transit inDictyostelium discoideum

  • M. Maniak
Focus on Cellular Biochemistry


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.


Actin cytoskeleton Dictyostelium discoideum Exocytosis Lysosomes Phagocytosis Pinocytosis 


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  1. 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: 3331–3337Google Scholar
  2. Aubry L, Klein G, Martiel JL, Satre M (1993) Kinetics of pH evolution inDictyostelium discoideum. J Cell Sci 105: 861–866Google Scholar
  3. 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: 37–40Google Scholar
  4. 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: 1343–1360Google Scholar
  5. 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: 2801–2812Google Scholar
  6. —, 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: 1623–1638Google Scholar
  7. 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: 803–823Google Scholar
  8. De Camilli P, Benfenati F, Valtorta F, Greengard P (1990) The synapsins. Annu Rev Cell Biol 6: 433–460Google Scholar
  9. 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: 233–243Google Scholar
  10. 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: 4097–4104Google Scholar
  11. 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: 44–53Google Scholar
  12. Fukui Y, Lynch TJ, Brzeska H, Korn ED (1989) Myosin I is located at the leading edges of locomotingDictyostelium amoebae. Nature 341: 328–331Google Scholar
  13. 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: 46–56Google Scholar
  14. 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: 83–98Google Scholar
  15. 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: 1853–1856Google Scholar
  16. 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: 3071–3081Google Scholar
  17. Hacker U, Albrecht R, Maniak M (1997) Fluid-phase uptake by macropinocytosis inDictyostelium. J Cell Sci 110: 105–112Google Scholar
  18. 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: 303–314Google Scholar
  19. Heuser J, Zhu Q, Clarke M (1993) Proton pumps populate the contractile vacuoles ofDictyostelium amoebae. J Cell Biol 121: 1311–1327Google Scholar
  20. 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: 61–70Google Scholar
  21. 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: 793–799Google Scholar
  22. Lenhard JM, Mayorga L, Stahl PD (1992) Characterization of endosome-endosome fusion in a cell-free system usingDictyostelium discoideum. J Biol Chem 267: 1896–1903Google Scholar
  23. Ludin B, Matus A (1998) GFP illuminates the cytoskeleton. Trends Cell Biol 8: 72–77Google Scholar
  24. Maniak M (1999) Green fluorescent protein in the visualisation of particle uptake and fluid-phase endocytosis. Methods Enzymol 302: 43–50Google Scholar
  25. —, 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: 915–924Google Scholar
  26. Mellman I (1996) Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12: 575–625Google Scholar
  27. 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: 349–361Google Scholar
  28. Nolta KV, Rodriguez-Paris JM, Steck TL (1994) Analysis of successive endocytic compartments isolated fromDictyostelium discoideum by magnetic fractionation. Biochim Biophys Acta 1224: 237–246Google Scholar
  29. Novick P, Zerial M (1997) The diversity of rab proteins in vesicle transport. Curr Opin Cell Biol 9: 496–504Google Scholar
  30. 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: 1371–1377Google Scholar
  31. Ostap EM, Pollard TD (1996) Overlapping functions of myosin-I isoforms. J Cell Biol 133: 221–224Google Scholar
  32. Padh H, Lavasa M, Steck TL (1989) Prelysosomal acidic vacuoles inDictyostelium discoideum. J Cell Biol 108: 865–874Google Scholar
  33. —, Ha J, Lavasa M, Steck TL (1993) A post-lysosomal compartment inDictyostelium discoideum. J Biol Chem 268: 6742–6747Google Scholar
  34. 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: 1529–1537Google Scholar
  35. 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: 83–95Google Scholar
  36. 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: 215–218Google Scholar
  37. 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: 965–980Google Scholar
  38. —, 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: 2679–2691Google Scholar
  39. 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: 343–352Google Scholar
  40. 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: 266–269Google Scholar
  41. 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: 2239–2248Google Scholar
  42. Swanson JA, Baer SC (1995) Phagocytosis by zippers and triggers. Trends Cell Biol 5: 89–93Google Scholar
  43. —, Watts C (1995) Macropinocytosis. Trends Cell Biol 5: 424–428Google Scholar
  44. 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: 25719–25727Google Scholar
  45. — — —, 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: 1479–1495Google Scholar
  46. Veithen A, Cupers P, Baudhuin P, Courtoy PJ (1996) V-src induces constitutive macropinocytosis in rat fibroblasts. J Cell Sci 109: 2005–2012Google Scholar
  47. 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: 456–465Google Scholar
  48. 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: 225–243Google Scholar
  49. 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: 53–62Google Scholar

Copyright information

© Springer-Verlag 1999

Authors and Affiliations

  • M. Maniak
    • 1
  1. 1.MRC Laboratory for Molecular Cell BiologyUniversity College LondonLondon

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