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. 1980 Oct 1;87(1):209–218. doi: 10.1083/jcb.87.1.209

Membrane structure of nonactivated and activated human blood platelets as revealed by freeze-fracture: evidence for particle redistribution during platelet contraction

PMCID: PMC2110721  PMID: 7191427

Abstract

The distribution of intramembrane particles of nonactivated and activated human blood platelets was studied by freeze-fracture under various experimental conditions to see whether morphological evidence for a structural coupling between the platelet actomyosin system and the fibrin network in a retracting clot could be established. Membrane particles were evenly distributed in nonactivated platelets; the total number (E + P faces) was approximately 1,500/micrometers 2 of membrane, and there were two to three times more particles present on the E face than on the P face. Transformation of discoid platelets to "spiny spheres" by cooling did not change the particle distribution. Platelet activation and aggregation by serum or ADP caused no change in membrane particle density or distribution. Particle distribution was not changed in Ca2+-activated platelets fixed immediately before fibrin formation, but after fibrin formation and during clot retraction, particles were sometimes most frequent on the P face and tended to form distinct clusters, and aggregates of E face pits were observed. Blood platelets contain contractile proteins that are distinct as filaments in platelets in retracting clots. We suggest that the redistribution of particles seen in activated platelets during clot retraction reflects the esablishment of mechanical transmembrane links between the platelet actomyosin system and the fibrin net. The P-face particle clusters may represent sites of force transmission between actin filaments bonded to the inside of the membrane and the fibrin network at the outside. Thus, whereas membrane particles may not be directly involved in the attachment of actin filaments to membranes, the transmission of the force of the contractile system to an exterior substrate apparently involves the intramembrane particles.

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Selected References

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

  1. BETTEX-GALLAND M., LUESCHER E. F. Extraction of an actomyosin-like protein from human thrombocytes. Nature. 1959 Jul 25;184(Suppl 5):276–277. doi: 10.1038/184276b0. [DOI] [PubMed] [Google Scholar]
  2. Behnke O., Kristensen B. I., Nielsen L. E. Electron microscopical observations on actinoid and myosinoid filaments in blood platelets. J Ultrastruct Res. 1971 Nov;37(3):351–369. doi: 10.1016/s0022-5320(71)80129-6. [DOI] [PubMed] [Google Scholar]
  3. Behnke O. Microtubules in disk-shaped blood cells. Int Rev Exp Pathol. 1970;9:1–92. [PubMed] [Google Scholar]
  4. Chevalier J., Nurden A. T., Thiery J. M., Savariau E., Caen J. P. Freeze-fracture studies on the plasma membranes of normal human, thrombasthenic, and Bernard-Soulier platelets. J Lab Clin Med. 1979 Aug;94(2):232–245. [PubMed] [Google Scholar]
  5. Cohen I. The contractile system of blood platelets and its function. Methods Achiev Exp Pathol. 1979;9:40–86. [PubMed] [Google Scholar]
  6. Dempsey G. P., Bullivant S., Watkins W. B. Endothelial cell membranes: polarity of particles as seen by freeze-fracturing. Science. 1973 Jan 12;179(4069):190–192. doi: 10.1126/science.179.4069.190. [DOI] [PubMed] [Google Scholar]
  7. Geiger B., Singer S. J. The participation of alpha-actinin in the capping of cell membrane components. Cell. 1979 Jan;16(1):213–222. doi: 10.1016/0092-8674(79)90202-2. [DOI] [PubMed] [Google Scholar]
  8. Gerrard J. M., Schollmeyer J. V., Phillips D. R., White J. G. alpha-Actinin deficiency in thrombasthenia: possible identity of alpha-actinin and glycoprotein III. Am J Pathol. 1979 Mar;94(3):509–528. [PMC free article] [PubMed] [Google Scholar]
  9. Hull B. E., Staehelin L. A. The terminal web. A reevaluation of its structure and function. J Cell Biol. 1979 Apr;81(1):67–82. doi: 10.1083/jcb.81.1.67. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Landon F., Huc C., Thomé F., Oriol C., Olomucki A. Human platelet actin. Evidence of beta and gamma forms and similarity of properties with sarcomeric actin. Eur J Biochem. 1977 Dec;81(3):571–577. doi: 10.1111/j.1432-1033.1977.tb11984.x. [DOI] [PubMed] [Google Scholar]
  11. Lazarides E., Burridge K. Alpha-actinin: immunofluorescent localization of a muscle structural protein in nonmuscle cells. Cell. 1975 Nov;6(3):289–298. doi: 10.1016/0092-8674(75)90180-4. [DOI] [PubMed] [Google Scholar]
  12. Lüscher E. F., Probst E., Bettex-Galland M. Thrombosthenin: structure and function. Ann N Y Acad Sci. 1972 Oct 27;201:122–130. doi: 10.1111/j.1749-6632.1972.tb16293.x. [DOI] [PubMed] [Google Scholar]
  13. McIntyre J. A., Gilula N. B., Karnovsky M. J. Cryoprotectant-induced redistribution of intramembranous particles in mouse lymphocytes. J Cell Biol. 1974 Jan;60(1):192–203. doi: 10.1083/jcb.60.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McNutt N. S. A thin-section and freeze-fracture study of microfilament-membrane attachments in choroid plexus and intestinal microvilli. J Cell Biol. 1978 Dec;79(3):774–787. doi: 10.1083/jcb.79.3.774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nachmias V., Sullender J., Asch A. Shape and cytoplasmic filaments in control and lidocaine-treated human platelets. Blood. 1977 Jul;50(1):39–53. [PubMed] [Google Scholar]
  16. Niederman R., Pollard T. D. Human platelet myosin. II. In vitro assembly and structure of myosin filaments. J Cell Biol. 1975 Oct;67(1):72–92. doi: 10.1083/jcb.67.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Pollard T. D., Thomas S. M., Niederman R. Human platelet myosin. I. Purification by a rapid method applicable to other nonmuscle cells. Anal Biochem. 1974 Jul;60(1):258–266. doi: 10.1016/0003-2697(74)90152-3. [DOI] [PubMed] [Google Scholar]
  18. Pricam C., Fisher K. A., Friend D. S. Intramembranous particle distribution in human erythrocytes: effects of lysis, glutaraldehyde, and poly-L-lysine. Anat Rec. 1977 Dec;189(4):595–607. doi: 10.1002/ar.1091890405. [DOI] [PubMed] [Google Scholar]
  19. Satir P., Satir B. Partition coefficient of membrane particles in the fusion rosette. Exp Cell Res. 1974 Dec;89(2):404–407. doi: 10.1016/0014-4827(74)90807-6. [DOI] [PubMed] [Google Scholar]
  20. Taylor D. G., Mapp R. J., Crawford N. The identification of actin associated with pig platelet membranes and granules. Biochem Soc Trans. 1975;3(1):161–164. doi: 10.1042/bst0030161. [DOI] [PubMed] [Google Scholar]
  21. Tilney L. G., Clain J. G., Tilney M. S. Membrane events in the acrosomal reaction of Limulus sperm. Membrane fusion, filament-membrane particle attachment, and the source and formation of new membrane surface. J Cell Biol. 1979 Apr;81(1):229–253. doi: 10.1083/jcb.81.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tilney L. G., Mooseker M. S. Actin filament-membrane attachment: are membrane particles involved? J Cell Biol. 1976 Nov;71(2):402–416. doi: 10.1083/jcb.71.2.402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zucker-Franklin D., Grusky G. The actin and myosin filaments of human and bovine blood platelets. J Clin Invest. 1972 Feb;51(2):419–430. doi: 10.1172/JCI106828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. van Deurs B., Koehler J. K. Tight junctions in the choroid plexus epithelium. A freeze-fracture study including complementary replicas. J Cell Biol. 1979 Mar;80(3):662–673. doi: 10.1083/jcb.80.3.662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. van Deurs B., Luft J. H. Effects of glutaraldehyde fixation on the structure of tight junctions: a quantitative freeze-fracture analysis. J Ultrastruct Res. 1979 Aug;68(2):160–172. doi: 10.1016/s0022-5320(79)90151-5. [DOI] [PubMed] [Google Scholar]

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