Microtubule Dependent Transport and Fusion of Phagosomes with the Endocytic Pathway

  • Janis K. Burkhardt
  • Ariel Blocker
  • Andrea Jahraus
  • Gareth Griffiths
Conference paper
Part of the NATO ASI Series book series (volume 91)

Abstract

Cells internalize material from the extracellular fluid by several different mechanisms (for a recent review on the diversity of mechanisms see Watts and Marsh, 1992). The two best characterized mechanisms are the clathrin-dependent pathway that functions for most receptor-mediated uptake as well as a variable proportion of the bulk fluid uptake, and phagocytosis. For a number of years our group has focused on the organization and function of the “classical” clathrin mediated endocytic pathway, both in fibroblasts and in polarized MDCK cells (see Griffiths and Gruenberg, 1991). Collectively, our results argue that, following the initial clathrin coated pit/vesicle uptake, material destined for degradation will traverse four distinct cellular organelles, the early endosome, the multivesicular body-like endosomal carrier vesicle (ECV), the late endosome (or prelysosomal compartment) and the terminal lysosome (Fig. 1). In our view the early and late endosomes represent true cellular compartments that are pre-existing in the cell and whose passage to daughter cells during mitosis is, we propose, essential for cell viability. In contrast, we propose that the ECV and the terminal lysosomes are transient vesicles (although these may be very long lived) which bud off the early and late endosomes, respectively. In line with this prediction we put forward the hypothesis that the ECV and dense lysosomes are not essential for daughter cell viability since they can be formed by budding from pre-existing compartments. While this view of the structures we now refer to as lysosomes may seem heretical, an increasing list of data can be put forward to argue that it is the late endosomes or prelysosomes that are the key functional degradation compartment in the cell (see Griffiths, 1990).

Keywords

Sucrose Tyrosine Argon Electrophoresis Cytosol 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aniento, F, Emans, N, Griffiths, G, and Gruenberg, J (1993) Cytopiasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123: 1373–1387.PubMedCrossRefGoogle Scholar
  2. Bergen, L, Kuriyama, R, and Borisy, GG (1980) Polarity of microtubules nucleated by centrosomes and chromosomes of CHO cells in vitro. J. cell Biol. 84: 151–159.PubMedCrossRefGoogle Scholar
  3. Burkhardt, JK, McIlvain, JM, Sheetz, MP, and Argon, Y (1993) Lyric granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro. J. Cell Sci. 104: 151–162.PubMedGoogle Scholar
  4. D’Arcy Hart, P, Young, MR, Gordon, AH, and Sullivan, KH (1987) Inhibition of phagosome-lysosome fusion in macrophages by certain mycobacteria can be explained by inhibition of lysosomal movements observed after phagocytosis. J. Exp. Med. 166: 933–946.CrossRefGoogle Scholar
  5. Desjardins, M, Huber, L, Parton, R, and Griffiths, G (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124: 677–688.PubMedCrossRefGoogle Scholar
  6. Desjardins, M, Celis, JE, van Meer, G, Dieplinger, H, Griffiths, G and Huber, L Molecular characterization of phagolysosomes in professional and non-professional phagocytes. (submitted)Google Scholar
  7. Greenberg, S, Chang, P, and Silverstein, SC (1993) Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177: 529–534.PubMedCrossRefGoogle Scholar
  8. Griffiths, G (1990) The compartments of the endocytic pathway. in Proc 2nd European Workshop on Endocytosis. P. Cortoy ed., pp73–83 Springer Verlag, Heidelberg.Google Scholar
  9. Griffiths, G and Gruenberg, J (1991) The arguments for pre-existing early and late endosomes. Trends Cell Biol. 1:5–9.PubMedCrossRefGoogle Scholar
  10. Gruenberg, J, Griffiths, G, and Howell, KE (1989) Characterization of an early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108: 1301–1316.PubMedCrossRefGoogle Scholar
  11. Gruenberg, J, and Clague, MJ (1992) Regulation of intracellular membrane transport. Curr. Opin. Cell Biol. 4: 593–599.PubMedCrossRefGoogle Scholar
  12. Hollenbeck, PJ and Swanson, JA (1990) Radial extension of macrophage tubular lysosomes supported by kinesin. Nature 346: 864–866.PubMedCrossRefGoogle Scholar
  13. Howard, J, and Hyman, AA (1993) Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence microscopy. in Motility Assays for Motor Proteins, Scholey, JM, ed. Academic Press, San Diego.Google Scholar
  14. Jahraus, A, Storrie, B, Griffiths, G and Desjardins, M (1994) Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment. J. Cell Sci. 107: 145–157.PubMedGoogle Scholar
  15. Knapp, PE, and Swanson, JA (1990) Plasticity of the tubular lysosomal compartment in macrophages. J. Cell Sci. 95: 433–439.PubMedGoogle Scholar
  16. Morel, F, Doussiere, J, and Vignais, PV (1991) The superoxide-generating oxidase of phagocytic cells: Physiological molecular and pathological aspects. Eur. J. Biochem. 201: 523–546.PubMedCrossRefGoogle Scholar
  17. Rabinowitz, S, Horstmann, H, Gordon, S and Griffiths, G (1992) Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J Cell Biol. 116: 95–112.PubMedCrossRefGoogle Scholar
  18. Schroer, TA (1991) Association of motor proteins with membranes. Curr. Opinion Cell Biol. 3: 133–137.PubMedCrossRefGoogle Scholar
  19. Schroer, TA, Sheetz, MP (1991) Functions of microtubule-based motors. Ann. Rev. Physiol. 53: 629–652.CrossRefGoogle Scholar
  20. Silverstein, SC, Greenberg, S, DiVirgilio, F, and Steinberg, TH (1989) Phagocytosis. in Fundamental Immunology. Paul, WE, ed. Raven Press, New York.Google Scholar
  21. Sorger, PK, Severin, FF, and Hyman, AA Factors required for the binding of reassembled yeast kinetochores to microtubules in vitro. Submitted.Google Scholar
  22. Swanson, J, Bushnell, A, and Silverstein, SC (1987) Tubular lysosome morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules. Proc. Nat. Acad. Sci. 84: 1921–1925.PubMedCrossRefGoogle Scholar
  23. Swanson, JA, Locke, A, Ansel, P, and Hollenbeck, PJ (1992) Radial movement of lysosomes along microtubules in permeabilized macrophages. J. Cell Sci. 103: 201–209.PubMedGoogle Scholar
  24. Wang, Y and Goren, MB (1987) Differential and sequential delivery of fluorescent lysosomal probes into phagosomes in mouse peritoneal macrophages. J. Cell Biol. 104: 1749–1754.PubMedCrossRefGoogle Scholar
  25. Watts, C and Marsh, M (1992) Endocytosis: what goes in and how. J. cell Sci. 103:1-8.PubMedGoogle Scholar
  26. Wetzel, MG and Korn, ED (1969) Phagocytosis of latex beads by Acanthamoeba castellanii (NEFF). III Isolation of the phagocytic vesicles and their membranes. J. cell Biol. 43: 90–104.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • Janis K. Burkhardt
    • 1
  • Ariel Blocker
    • 1
  • Andrea Jahraus
    • 1
  • Gareth Griffiths
    • 1
  1. 1.European Molecular Biology LaboratoryHeidelbergGermany

Personalised recommendations