Skip to main content
NCBI home page
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1989 Jan;134(1):15–26.

Rapid fragmentation and reorganization of Golgi membranes during frustrated phagocytosis of immobile immune complexes by macrophages.

D F Bainton 1, R Takemura 1, P E Stenberg 1, Z Werb 1
PMCID: PMC1879551  PMID: 2913823

Abstract

The authors have observed the rapid reorganization of the cellular membranes of macrophages during Fc receptor-mediated frustrated phagocytosis of immune complex-coated surfaces. As the macrophages spread, large, clear basal vacuoles and anastamosing tubules were formed, occasionally contiguous with the adherent surface. Coated vesicles also were observed. This process was accompanied by a rapid reorganization of the Golgi complex region of the macrophages, which was observed using trimetaphosphatase histochemistry and an antibody to a Golgi membrane antigen as markers. On contact of the macrophages with the immune complexes, the Golgi complexes, which were tightly clustered around the centrioles, dispersed into vesicles and reorganized near the basal surface. The Golgi cisternae swelled, fragmented, and decreased in number. Golgi membrane antigen was found in the large basal vacuoles and also associated with the adherent basal surface of the macrophages. This indicates that the Golgi complexes were reorganized, in part, by a direct recruitment of their membranes to the increasing basal surface area of the spreading macrophages. The changes in the structure of the Golgi complexes were reversible; by 2 hours, the complexes had recovered their normal organization, with an accompanying decrease in the number of large basal vacuoles. These data suggest that the dynamic interrelationship among the Golgi membranes, intracellular vacuoles, and the plasma membrane can be perturbed by membrane spreading on a nonphagocytosable surface.

Full text

PDF
15

Images in this article

16Figure 1
on p.16
17Figure 2
on p.17
18Figure 3
on p.18
20Figure 4
on p.20
21Figure 5
on p.21
23Figure 6
on p.23
24Figure 7
on p.24

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aggeler J., Takemura R., Werb Z. High-resolution three-dimensional views of membrane-associated clathrin and cytoskeleton in critical-point-dried macrophages. J Cell Biol. 1983 Nov;97(5 Pt 1):1452–1458. doi: 10.1083/jcb.97.5.1452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aggeler J., Werb Z. Initial events during phagocytosis by macrophages viewed from outside and inside the cell: membrane-particle interactions and clathrin. J Cell Biol. 1982 Sep;94(3):613–623. doi: 10.1083/jcb.94.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berlin R. D., Oliver J. M., Walter R. J. Surface functions during Mitosis I: phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell. 1978 Oct;15(2):327–341. doi: 10.1016/0092-8674(78)90002-8. [DOI] [PubMed] [Google Scholar]
  4. Brown W. J., Constantinescu E., Farquhar M. G. Redistribution of mannose-6-phosphate receptors induced by tunicamycin and chloroquine. J Cell Biol. 1984 Jul;99(1 Pt 1):320–326. doi: 10.1083/jcb.99.1.320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown W. J., Farquhar M. G. The mannose-6-phosphate receptor for lysosomal enzymes is concentrated in cis Golgi cisternae. Cell. 1984 Feb;36(2):295–307. doi: 10.1016/0092-8674(84)90223-x. [DOI] [PubMed] [Google Scholar]
  6. Burke B., Griffiths G., Reggio H., Louvard D., Warren G. A monoclonal antibody against a 135-K Golgi membrane protein. EMBO J. 1982;1(12):1621–1628. doi: 10.1002/j.1460-2075.1982.tb01364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collot M., Louvard D., Singer S. J. Lysosomes are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci U S A. 1984 Feb;81(3):788–792. doi: 10.1073/pnas.81.3.788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Doty S. B., Smith C. E., Hand A. R., Oliver C. Inorganic trimetaphosphatase as a histochemical marker for lysosomes in light and electron microscopy. J Histochem Cytochem. 1977 Dec;25(12):1381–1384. doi: 10.1177/25.12.200672. [DOI] [PubMed] [Google Scholar]
  9. Eccles M. H., Glauert A. M. The response of human monocytes to interaction with immobilized immune complexes. J Cell Sci. 1984 Oct;71:141–157. doi: 10.1242/jcs.71.1.141. [DOI] [PubMed] [Google Scholar]
  10. Farquhar M. G. Multiple pathways of exocytosis, endocytosis, and membrane recycling: validation of a Golgi route. Fed Proc. 1983 May 15;42(8):2407–2413. [PubMed] [Google Scholar]
  11. Farquhar M. G. Recovery of surface membrane in anterior pituitary cells. Variations in traffic detected with anionic and cationic ferritin. J Cell Biol. 1978 Jun;77(3):R35–R42. doi: 10.1083/jcb.77.3.r35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Friend D. S., Farquhar M. G. Functions of coated vesicles during protein absorption in the rat vas deferens. J Cell Biol. 1967 Nov;35(2):357–376. doi: 10.1083/jcb.35.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Glauert A. M., Oliver R. C., Thorne K. J. The interaction of human eosinophils and neutrophils with non-phagocytosable surfaces: a model for studying cell-mediated immunity in schistosomiasis. Parasitology. 1980 Jun;80(3):525–537. doi: 10.1017/s0031182000000986. [DOI] [PubMed] [Google Scholar]
  14. Griffiths G., Simons K. The trans Golgi network: sorting at the exit site of the Golgi complex. Science. 1986 Oct 24;234(4775):438–443. doi: 10.1126/science.2945253. [DOI] [PubMed] [Google Scholar]
  15. Hart P. D., Young M. R., Jordan M. M., Perkins W. J., Geisow M. J. Chemical inhibitors of phagosome-lysosome fusion in cultured macrophages also inhibit saltatory lysosomal movements. A combined microscopic and computer study. J Exp Med. 1983 Aug 1;158(2):477–492. doi: 10.1084/jem.158.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Henson P. M. Interaction of cells with immune complexes: adherence, release of constituents, and tissue injury. J Exp Med. 1971 Sep 1;134(3 Pt 2):114s–135s. [PubMed] [Google Scholar]
  17. Johnston R. B., Jr, Lehmeyer J. E., Guthrie L. A. Generation of superoxide anion and chemiluminescence by human monocytes during phagocytosis and on contact with surface-bound immunoglobulin G. J Exp Med. 1976 Jun 1;143(6):1551–1556. doi: 10.1084/jem.143.6.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Keeling P. J., Henson P. M. Lysosomal enzyme release from human monocytes in response to particulate stimuli. J Immunol. 1982 Feb;128(2):563–567. [PubMed] [Google Scholar]
  19. Kupfer A., Dennert G., Singer S. J. Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7224–7228. doi: 10.1073/pnas.80.23.7224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kupfer A., Louvard D., Singer S. J. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2603–2607. doi: 10.1073/pnas.79.8.2603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Louvard D., Reggio H., Warren G. Antibodies to the Golgi complex and the rough endoplasmic reticulum. J Cell Biol. 1982 Jan;92(1):92–107. doi: 10.1083/jcb.92.1.92. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lucocq J. M., Pryde J. G., Berger E. G., Warren G. A mitotic form of the Golgi apparatus in HeLa cells. J Cell Biol. 1987 Apr;104(4):865–874. doi: 10.1083/jcb.104.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lucocq J. M., Warren G. Fragmentation and partitioning of the Golgi apparatus during mitosis in HeLa cells. EMBO J. 1987 Nov;6(11):3239–3246. doi: 10.1002/j.1460-2075.1987.tb02641.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mellman I., Plutner H., Ukkonen P. Internalization and rapid recycling of macrophage Fc receptors tagged with monovalent antireceptor antibody: possible role of a prelysosomal compartment. J Cell Biol. 1984 Apr;98(4):1163–1169. doi: 10.1083/jcb.98.4.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Michl J., Pieczonka M. M., Unkeless J. C., Bell G. I., Silverstein S. C. Fc receptor modulation in mononuclear phagocytes maintained on immobilized immune complexes occurs by diffusion of the receptor molecule. J Exp Med. 1983 Jun 1;157(6):2121–2139. doi: 10.1084/jem.157.6.2121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moskalewski S., Thyberg J., Friberg U. In vitro influence of colchicine on the Golgi complex in A- and B-cells of guinea pig pancreatic islets. J Ultrastruct Res. 1976 Feb;54(2):304–317. doi: 10.1016/s0022-5320(76)80159-1. [DOI] [PubMed] [Google Scholar]
  27. Orci L., Halban P., Amherdt M., Ravazzola M., Vassalli J. D., Perrelet A. A clathrin-coated, Golgi-related compartment of the insulin secreting cell accumulates proinsulin in the presence of monensin. Cell. 1984 Nov;39(1):39–47. doi: 10.1016/0092-8674(84)90189-2. [DOI] [PubMed] [Google Scholar]
  28. Ottosen P. D., Courtoy P. J., Farquhar M. G. Pathways followed by membrane recovered from the surface of plasma cells and myeloma cells. J Exp Med. 1980 Jul 1;152(1):1–19. doi: 10.1084/jem.152.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Petty H. R., Hafeman D. G., McConnell H. M. Disappearance of macrophage surface folds after antibody-dependent phagocytosis. J Cell Biol. 1981 May;89(2):223–229. doi: 10.1083/jcb.89.2.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Petty H. R., Hermann W., McConnell H. M. Cytochemical study of macrophage lysosomal inorganic trimetaphosphatase and acid phosphatase. J Ultrastruct Res. 1985 Jan;90(1):80–88. doi: 10.1016/0889-1605(85)90118-1. [DOI] [PubMed] [Google Scholar]
  31. Phaire-Washington L., Silverstein S. C., Wang E. Phorbol myristate acetate stimulates microtubule and 10-nm filament extension and lysosome redistribution in mouse macrophages. J Cell Biol. 1980 Aug;86(2):641–655. doi: 10.1083/jcb.86.2.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Quintart J., Leroy-Houyet M. A., Baudhuin P. Stereological analysis of synchronized hepatoma cells as a function of the cell cycle. J Ultrastruct Res. 1980 Jul;72(1):76–89. doi: 10.1016/s0022-5320(80)90137-9. [DOI] [PubMed] [Google Scholar]
  33. Rogalski A. A., Singer S. J. Associations of elements of the Golgi apparatus with microtubules. J Cell Biol. 1984 Sep;99(3):1092–1100. doi: 10.1083/jcb.99.3.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rothman J. E., Miller R. L., Urbani L. J. Intercompartmental transport in the Golgi complex is a dissociative process: facile transfer of membrane protein between two Golgi populations. J Cell Biol. 1984 Jul;99(1 Pt 1):260–271. doi: 10.1083/jcb.99.1.260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Saraste J., Kuismanen E. Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell. 1984 Sep;38(2):535–549. doi: 10.1016/0092-8674(84)90508-7. [DOI] [PubMed] [Google Scholar]
  36. Swanson J. A., Yirinec B. D., Silverstein S. C. Phorbol esters and horseradish peroxidase stimulate pinocytosis and redirect the flow of pinocytosed fluid in macrophages. J Cell Biol. 1985 Mar;100(3):851–859. doi: 10.1083/jcb.100.3.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Takemura R., Stenberg P. E., Bainton D. F., Werb Z. Rapid redistribution of clathrin onto macrophage plasma membranes in response to Fc receptor-ligand interaction during frustrated phagocytosis. J Cell Biol. 1986 Jan;102(1):55–69. doi: 10.1083/jcb.102.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tartakoff A. M. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell. 1983 Apr;32(4):1026–1028. doi: 10.1016/0092-8674(83)90286-6. [DOI] [PubMed] [Google Scholar]
  39. Walter R. J., Berlin R. D., Pfeiffer J. R., Oliver J. M. Polarization of endocytosis and receptor topography on cultured macrophages. J Cell Biol. 1980 Jul;86(1):199–211. doi: 10.1083/jcb.86.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang E., Michl J., Pfeffer L. M., Silverstein S. C., Tamm I. Interferon suppresses pinocytosis but stimulates phagocytosis in mouse peritoneal macrophages: related changes in cytoskeletal organization. J Cell Biol. 1984 Apr;98(4):1328–1341. doi: 10.1083/jcb.98.4.1328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Warren G., Featherstone C., Griffiths G., Burke B. Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis. J Cell Biol. 1983 Nov;97(5 Pt 1):1623–1628. doi: 10.1083/jcb.97.5.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wright S. D., Silverstein S. C. Phagocytosing macrophages exclude proteins from the zones of contact with opsonized targets. Nature. 1984 May 24;309(5966):359–361. doi: 10.1038/309359a0. [DOI] [PubMed] [Google Scholar]
  43. Yamashiro D. J., Tycko B., Fluss S. R., Maxfield F. R. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell. 1984 Jul;37(3):789–800. doi: 10.1016/0092-8674(84)90414-8. [DOI] [PubMed] [Google Scholar]
  44. Young J. D., Ko S. S., Cohn Z. A. The increase in intracellular free calcium associated with IgG gamma 2b/gamma 1 Fc receptor-ligand interactions: role in phagocytosis. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5430–5434. doi: 10.1073/pnas.81.17.5430. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES