Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Feb 1;108(2):467–479. doi: 10.1083/jcb.108.2.467

Association of gelsolin with actin filaments and cell membranes of macrophages and platelets

PMCID: PMC2115434  PMID: 2537317

Abstract

Recent evidence that polyphosphoinositides regulate the function of the actin-modulating protein gelsolin in vitro raises the possibility that gelsolin interacts with cell membranes. This paper reports ultrastructural immunohistochemical data revealing that gelsolin molecules localize with plasma and intracellular membranes, including rough endoplasmic reticulum, cortical vesicles and mitochondria of macrophages, and blood platelets. Anti-gelsolin gold also labeled the surface and interior of secondary lysosomes presumably representing plasma gelsolin ingested by these cells from the lung surface by endocytosis. Gelsolin molecules, visualized with colloidal gold in replicas of the cytoplasmic side of the substrate-adherent plasma membrane of mechanically unroofed and rapidly frozen and freeze-dried macrophages, associated with the ends of short actin filaments sitting on the cytoplasmic membrane surface. A generalized distribution of gelsolin molecules in thin sections of resting platelets rapidly became peripheral, and plasmalemma association increased following thrombin stimulation. At later times the distribution reverted to the cytoplasmic distribution of resting cells. These findings provide the first evidence for gelsolin binding to actin filament ends in cells and indicate that gelsolin functions in both cytoplasmic and membrane domains.

Full Text

The Full Text of this article is available as a PDF (6.7 MB).

Selected References

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

  1. Berridge M. J. Inositol trisphosphate and diacylglycerol as second messengers. Biochem J. 1984 Jun 1;220(2):345–360. doi: 10.1042/bj2200345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burn P. Amphitropic proteins: a new class of membrane proteins. Trends Biochem Sci. 1988 Mar;13(3):79–83. doi: 10.1016/0968-0004(88)90043-6. [DOI] [PubMed] [Google Scholar]
  3. Chaponnier C., Yin H. L., Stossel T. P. Reversibility of gelsolin/actin interaction in macrophages. Evidence of Ca2+-dependent and Ca2+-independent pathways. J Exp Med. 1987 Jan 1;165(1):97–106. doi: 10.1084/jem.165.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cooper J. A., Bryan J., Schwab B., 3rd, Frieden C., Loftus D. J., Elson E. L. Microinjection of gelsolin into living cells. J Cell Biol. 1987 Mar;104(3):491–501. doi: 10.1083/jcb.104.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cooper J. A., Loftus D. J., Frieden C., Bryan J., Elson E. L. Localization and mobility of gelsolin in cells. J Cell Biol. 1988 Apr;106(4):1229–1240. doi: 10.1083/jcb.106.4.1229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ezzell R. M., Kenney D. M., Egan S., Stossel T. P., Hartwig J. H. Localization of the domain of actin-binding protein that binds to membrane glycoprotein Ib and actin in human platelets. J Biol Chem. 1988 Sep 15;263(26):13303–13309. [PubMed] [Google Scholar]
  7. Fox J. E. Identification of actin-binding protein as the protein linking the membrane skeleton to glycoproteins on platelet plasma membranes. J Biol Chem. 1985 Oct 5;260(22):11970–11977. [PubMed] [Google Scholar]
  8. Glenney J. R., Jr, Tack B., Powell M. A. Calpactins: two distinct Ca++-regulated phospholipid- and actin-binding proteins isolated from lung and placenta. J Cell Biol. 1987 Mar;104(3):503–511. doi: 10.1083/jcb.104.3.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hartwig J. H., Shevlin P. The architecture of actin filaments and the ultrastructural location of actin-binding protein in the periphery of lung macrophages. J Cell Biol. 1986 Sep;103(3):1007–1020. doi: 10.1083/jcb.103.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Heuser J. E., Kirschner M. W. Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J Cell Biol. 1980 Jul;86(1):212–234. doi: 10.1083/jcb.86.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Janmey P. A., Iida K., Yin H. L., Stossel T. P. Polyphosphoinositide micelles and polyphosphoinositide-containing vesicles dissociate endogenous gelsolin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin. J Biol Chem. 1987 Sep 5;262(25):12228–12236. [PubMed] [Google Scholar]
  12. Janmey P. A., Stossel T. P. Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate. Nature. 1987 Jan 22;325(6102):362–364. doi: 10.1038/325362a0. [DOI] [PubMed] [Google Scholar]
  13. Kurth M. C., Bryan J. Platelet activation induces the formation of a stable gelsolin-actin complex from monomeric gelsolin. J Biol Chem. 1984 Jun 25;259(12):7473–7479. [PubMed] [Google Scholar]
  14. Kurth M. C., Wang L. L., Dingus J., Bryan J. Purification and characterization of a gelsolin-actin complex from human platelets. Evidence for Ca2+-insensitive functions. J Biol Chem. 1983 Sep 25;258(18):10895–10903. [PubMed] [Google Scholar]
  15. Langanger G., de Mey J., Moeremans M., Daneels G., de Brabander M., Small J. V. Ultrastructural localization of alpha-actinin and filamin in cultured cells with the immunogold staining (IGS) method. J Cell Biol. 1984 Oct;99(4 Pt 1):1324–1334. doi: 10.1083/jcb.99.4.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lind S. E., Janmey P. A., Chaponnier C., Herbert T. J., Stossel T. P. Reversible binding of actin to gelsolin and profilin in human platelet extracts. J Cell Biol. 1987 Aug;105(2):833–842. doi: 10.1083/jcb.105.2.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nichols B. A. Normal rabbit alveolar macrophages. I. The phagocytosis of tubular myelin. J Exp Med. 1976 Oct 1;144(4):906–919. doi: 10.1084/jem.144.4.906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  19. Okita J. R., Pidard D., Newman P. J., Montgomery R. R., Kunicki T. J. On the association of glycoprotein Ib and actin-binding protein in human platelets. J Cell Biol. 1985 Jan;100(1):317–321. doi: 10.1083/jcb.100.1.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rittenhouse S. E. Human platelets contain phospholipase C that hydrolyzes polyphosphoinositides. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5417–5420. doi: 10.1073/pnas.80.17.5417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schliwa M., van Blerkom J., Porter K. R. Stabilization and the cytoplasmic ground substance in detergent-opened cells and a structural and biochemical analysis of its composition. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4329–4333. doi: 10.1073/pnas.78.7.4329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Slot J. W., Geuze H. J. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol. 1985 Jul;38(1):87–93. [PubMed] [Google Scholar]
  23. Stendahl O. I., Hartwig J. H., Brotschi E. A., Stossel T. P. Distribution of actin-binding protein and myosin in macrophages during spreading and phagocytosis. J Cell Biol. 1980 Feb;84(2):215–224. doi: 10.1083/jcb.84.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wang E., Yin H. L., Krueger J. G., Caliguiri L. A., Tamm I. Unphosphorylated gelsolin is localized in regions of cell-substratum contact or attachment in Rous sarcoma virus-transformed rat cells. J Cell Biol. 1984 Feb;98(2):761–771. doi: 10.1083/jcb.98.2.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wuestehube L. J., Luna E. J. F-actin binds to the cytoplasmic surface of ponticulin, a 17-kD integral glycoprotein from Dictyostelium discoideum plasma membranes. J Cell Biol. 1987 Oct;105(4):1741–1751. doi: 10.1083/jcb.105.4.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yin H. L., Albrecht J. H., Fattoum A. Identification of gelsolin, a Ca2+-dependent regulatory protein of actin gel-sol transformation, and its intracellular distribution in a variety of cells and tissues. J Cell Biol. 1981 Dec;91(3 Pt 1):901–906. doi: 10.1083/jcb.91.3.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yin H. L., Hartwig J. H., Maruyama K., Stossel T. P. Ca2+ control of actin filament length. Effects of macrophage gelsolin on actin polymerization. J Biol Chem. 1981 Sep 25;256(18):9693–9697. [PubMed] [Google Scholar]
  28. Yin H. L., Iida K., Janmey P. A. Identification of a polyphosphoinositide-modulated domain in gelsolin which binds to the sides of actin filaments. J Cell Biol. 1988 Mar;106(3):805–812. doi: 10.1083/jcb.106.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yin H. L., Stossel T. P. Purification and structural properties of gelsolin, a Ca2+-activated regulatory protein of macrophages. J Biol Chem. 1980 Oct 10;255(19):9490–9493. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES