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. 1973 Oct 1;59(1):12–27. doi: 10.1083/jcb.59.1.12

SUBPLASMALEMMAL MICROFILAMENTS AND MICROTUBULES IN RESTING AND PHAGOCYTIZING CULTIVATED MACROPHAGES

Eve P Reaven 1, Stanton G Axline 1
PMCID: PMC2110909  PMID: 4356569

Abstract

The subplasmalemmal organization of the free and glass-attached surfaces of resting and phagocytizing cultivated macrophages were examined in an attempt to define specific membrane-associated structures related to phagocytosis. From analysis of serial thin sections of oriented cells it was found that the subplasmalemmal region of the attached cell surface has a complex microfilament and microtubule organization relative to the subplasmalemmal area of the free surface. A filamentous network composed of 40–50-Å microfilaments extended for a depth of 400–600 Å from the attached plasma membrane. Immediately subjacent to the filamentous network was a zone of oriented bundles of 40–50-Å microfilaments and a zone of microtubules. Additional microtubules were found to extend from the plasma membrane to the interior of the cell in close association with electron-dense, channellike structures. In contrast, the free aspect of the cultivated macrophage contained only the subplasmalemmal filamentous network. However, after a phagocytic pulse with polystyrene particles (14 µm diam) microtubules and oriented filaments similar to those found on the attached surface were observed surrounding the ingested particles. The observations reported in this paper provide support for the hypothesis that microfilaments and/or microtubules play a role in the translocation of plasma membrane required for the functionally similar processes of phagocytosis and cell attachment to glass.

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Selected References

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  1. Abercrombie M., Heaysman J. E., Pegrum S. M. The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella. Exp Cell Res. 1971 Aug;67(2):359–367. doi: 10.1016/0014-4827(71)90420-4. [DOI] [PubMed] [Google Scholar]
  2. Allison A. C., Davies P., De Petris S. Role of contractile microfilaments in macrophage movement and endocytosis. Nat New Biol. 1971 Aug 4;232(31):153–155. doi: 10.1038/newbio232153a0. [DOI] [PubMed] [Google Scholar]
  3. Bhisey A. N., Freed J. J. Altered movement of endosomes in colchicine-treated cultured macrophages. Exp Cell Res. 1971 Feb;64(2):430–438. doi: 10.1016/0014-4827(71)90097-8. [DOI] [PubMed] [Google Scholar]
  4. Bhisey A. N., Freed J. J. Ameboid movement induced in cultured macrophages by colchicine or vinblastine. Exp Cell Res. 1971 Feb;64(2):419–429. doi: 10.1016/0014-4827(71)90096-6. [DOI] [PubMed] [Google Scholar]
  5. Branson S. H. Epon-embedded cell monolayers. Separating partially polymerized blocks from glass surfaces. Exp Cell Res. 1971 Mar;65(1):253–256. doi: 10.1016/s0014-4827(71)80076-9. [DOI] [PubMed] [Google Scholar]
  6. Clawson C. C., Good R. A. Micropapillae: a surface specialization of human leukocytes. J Cell Biol. 1971 Jan;48(1):207–211. doi: 10.1083/jcb.48.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohn Z. A. The structure and function of monocytes and macrophages. Adv Immunol. 1968;9:163–214. doi: 10.1016/s0065-2776(08)60443-5. [DOI] [PubMed] [Google Scholar]
  8. DE PETRIS S., KARLSBAD G., PERNIS B. Filamentous structures in the cytoplasm of normal mononuclear phagocytes. J Ultrastruct Res. 1962 Aug;7:39–55. doi: 10.1016/s0022-5320(62)80025-2. [DOI] [PubMed] [Google Scholar]
  9. Davis A. T., Estensen R., Quie P. G. Cytochalasin B. 3. Inhibition of human polymorphonuclear leukocyte phagocytosis. Proc Soc Exp Biol Med. 1971 May;137(1):161–164. doi: 10.3181/00379727-137-35535. [DOI] [PubMed] [Google Scholar]
  10. Dumont A. Ultrastructural aspects of phagocytosis of facultative intracellular parasites by hamster peritoneal macrophages. J Reticuloendothel Soc. 1972 May;11(5):469–491. [PubMed] [Google Scholar]
  11. Fedorko M. E., Hirsch J. G. Structure of monocytes and macrophages. Semin Hematol. 1970 Apr;7(2):109–124. [PubMed] [Google Scholar]
  12. Goldman R. D. The role of three cytoplasmic fibers in BHK-21 cell motility. I. Microtubules and the effects of colchicine. J Cell Biol. 1971 Dec;51(3):752–762. doi: 10.1083/jcb.51.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirsch J. G., Fedorko M. E. Ultrastructure of human leukocytes after simultaneous fixation with glutaraldehyde and osmium tetroxide and "postfixation" in uranyl acetate. J Cell Biol. 1968 Sep;38(3):615–627. doi: 10.1083/jcb.38.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Malawista S. E., Gee J. B., Bensch K. G. Cytochalasin B reversibly inhibits phagocytosis: functional, metabolic, and ultrastructural effects in human blood leukocytes and rabbit alveolar macrophages. Yale J Biol Med. 1971 Dec;44(3):286–300. [PMC free article] [PubMed] [Google Scholar]
  15. North R. J. Endocytosis. Semin Hematol. 1970 Apr;7(2):161–171. [PubMed] [Google Scholar]
  16. PEACHEY L. D. Thin sections. I. A study of section thickness and physical distortion produced during microtomy. J Biophys Biochem Cytol. 1958 May 25;4(3):233–242. doi: 10.1083/jcb.4.3.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pollard T. D., Shelton E., Weihing R. R., Korn E. D. Ultrastructural characterization of F-actin isolated from Acanthamoeba castellanii and identification of cytoplasmic filaments as F-actin by reaction with rabbit heavy meromyosin. J Mol Biol. 1970 May 28;50(1):91–97. doi: 10.1016/0022-2836(70)90106-3. [DOI] [PubMed] [Google Scholar]
  18. Spooner B. S., Yamada K. M., Wessells N. K. Microfilaments and cell locomotion. J Cell Biol. 1971 Jun;49(3):595–613. doi: 10.1083/jcb.49.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sutton J. S., Weiss L. Transformation of monocytes in tissue culture into macrophages, epithelioid cells, and multinucleated giant cells. An electron microscope study. J Cell Biol. 1966 Feb;28(2):303–332. doi: 10.1083/jcb.28.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tilney L. G., Gibbins J. R. Microtubules and filaments in the filopodia of the secondary mesenchyme cells of Arbacia punctulata and Echinarachnius parma. J Cell Sci. 1969 Jul;5(1):195–210. doi: 10.1242/jcs.5.1.195. [DOI] [PubMed] [Google Scholar]
  21. Wagner R., Rosenberg M., Estensen R. Endocytosis in Chang liver cells. Quantitation by sucrose- 3 H uptake and inhibition by cytochalasin B. J Cell Biol. 1971 Sep;50(3):804–817. doi: 10.1083/jcb.50.3.804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wessells N. K., Spooner B. S., Ash J. F., Bradley M. O., Luduena M. A., Taylor E. L., Wrenn J. T., Yamada K. Microfilaments in cellular and developmental processes. Science. 1971 Jan 15;171(3967):135–143. doi: 10.1126/science.171.3967.135. [DOI] [PubMed] [Google Scholar]
  23. Yamada K. M., Spooner B. S., Wessells N. K. Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol. 1971 Jun;49(3):614–635. doi: 10.1083/jcb.49.3.614. [DOI] [PMC free article] [PubMed] [Google Scholar]

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