Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1974 Sep 1;62(3):594–609. doi: 10.1083/jcb.62.3.594

THE REGULATORY ROLE OF DIVALENT CATIONS IN HUMAN GRANULOCYTE CHEMOTAXIS

Evidence for an Association between Calcium Exchanges and Microtubule Assembly

John I Gallin 1, Alan S Rosenthal 1
PMCID: PMC2109215  PMID: 4855032

Abstract

Optimal human granulocyte chemotaxis has been shown to require both calcium and magnesium. Exposure of granulocytes to three different chemotactic factors (C5a, kallikrein, and dialyzable transfer factor) yielded a rapid calcium release, depressed calcium uptake, and was associated with a shift of calcium out of the cytoplasm and into a granule fraction. Colchicine, sodium azide, and cytochalasin B, in concentrations that inhibited chemotaxis, also inhibited calcium release while low concentrations of cytochalasin B, which enhanced chemotaxis, also enhanced calcium release. Microtubule assembly was visualized both in cells suspended in C5a without a chemotactic gradient and in cells actively migrating through a Micropore filter. The data suggest microtubule assembly is regulated, at least, in part, by the level of cytoplasmic calcium. It is proposed that asymmetric assembly of microtubules may be instrumental in imparting the net vector of motion during chemotaxis.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. 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]
  2. Atherton A., Born G. V. Quantitative investigations of the adhesiveness of circulating polymorphonuclear leucocytes to blood vessel walls. J Physiol. 1972 Apr;222(2):447–474. doi: 10.1113/jphysiol.1972.sp009808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Becker E. L., Davis A. T., Estensen R. D., Quie P. G. Cytochalasin B. IV. Inhibition and stimulation of chemotaxis of rabbit and human polymorphonuclear leukocytes. J Immunol. 1972 Feb;108(2):396–402. [PubMed] [Google Scholar]
  4. Becker E. L., Showell H. J. The effect of Ca2+ and Mg2+ on the chemotactic responsiveness and spontaneous motility of rabbit polymorphonuclear leukocytes. Z Immunitatsforsch Exp Klin Immunol. 1972 Jun;143(5):466–476. [PubMed] [Google Scholar]
  5. Berry R. W., Shelanski M. L. Interactions of tubulin with vinblastine and guanosine triphosphate. J Mol Biol. 1972 Oct 28;71(1):71–80. doi: 10.1016/0022-2836(72)90401-9. [DOI] [PubMed] [Google Scholar]
  6. Brinley F. J., Jr Calcium and magnesium transport in single cells. Fed Proc. 1973 Jul;32(7):1735–1739. [PubMed] [Google Scholar]
  7. Bryant R. E., DesPrez R. M., VanWay M. H., Rogers D. E. Studies on human leukocyte motility. I. Effects of alterations in pH, electrolyte concentration, and phagocytosis on leukocyte migration, adhesiveness, and aggregation. J Exp Med. 1966 Sep 1;124(3):483–499. doi: 10.1084/jem.124.3.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  9. Chi Y. Y., Francis D. Cyclic AMP and calcium exchange in a cellular slime mold. J Cell Physiol. 1971 Apr;77(2):169–174. doi: 10.1002/jcp.1040770206. [DOI] [PubMed] [Google Scholar]
  10. Clark R. A., Frank M. M., Kimball H. R. Generation of chemotactic factors in guinea pig serum via activation of the classical and alternate complement pathways. Clin Immunol Immunopathol. 1973 Apr;1(3):414–426. doi: 10.1016/0090-1229(73)90058-5. [DOI] [PubMed] [Google Scholar]
  11. Clark R. A., Kimball H. R. Defective granulocyte chemotaxis in the Chediak-Higashi syndrome. J Clin Invest. 1971 Dec;50(12):2645–2652. doi: 10.1172/JCI106765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gallin J. I., Clark R. A., Kimball H. R. Granulocyte chemotaxis: an improved in vitro assay employing 51 Cr-labeled granulocytes. J Immunol. 1973 Jan;110(1):233–240. [PubMed] [Google Scholar]
  13. Gallin J. I., Kirkpatrick C. H. Chemotactic activity in dialyzable transfer factor. Proc Natl Acad Sci U S A. 1974 Feb;71(2):498–502. doi: 10.1073/pnas.71.2.498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goldstein I., Hoffstein S., Gallin J., Weissmann G. Mechanisms of lysosomal enzyme release from human leukocytes: microtubule assembly and membrane fusion induced by a component of complement. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2916–2920. doi: 10.1073/pnas.70.10.2916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Huxley H. E. Muscular contraction and cell motility. Nature. 1973 Jun 22;243(5408):445–449. doi: 10.1038/243445a0. [DOI] [PubMed] [Google Scholar]
  16. Kaplan A. P., Kay A. B., Austen K. F. A prealbumin activator of prekallikrein. 3. Appearance of chemotactic activity for human neutrophils by the conversion of human prekallikrein to kallikrein. J Exp Med. 1972 Jan;135(1):81–97. doi: 10.1084/jem.135.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kvarstein B. Effects of proteins and inorganic ions on the adhesiveness of human leucocytes to glass beads. Scand J Clin Lab Invest. 1969 Aug;24(1):41–48. doi: 10.3109/00365516909080130. [DOI] [PubMed] [Google Scholar]
  18. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  19. POST R. L., SEN A. K., ROSENTHAL A. S. A PHOSPHORYLATED INTERMEDIATE IN ADENOSINE TRIPHOSPHATE-DEPENDENT SODIUM AND POTASSIUM TRANSPORT ACROSS KIDNEY MEMBRANES. J Biol Chem. 1965 Mar;240:1437–1445. [PubMed] [Google Scholar]
  20. Phelps P., Stanislaw D. Polymorphonuclear leukocyte motility in vitro. I. Effect of pH, temperature, ethyl alcohol, and caffeine, using a modified Boyden chamber technic. Arthritis Rheum. 1969 Jun;12(3):181–188. doi: 10.1002/art.1780120304. [DOI] [PubMed] [Google Scholar]
  21. Ramsey W. S. Locomotion of human polymorphonuclear leucocytes. Exp Cell Res. 1972 Jun;72(2):489–501. doi: 10.1016/0014-4827(72)90019-5. [DOI] [PubMed] [Google Scholar]
  22. Shelanski M. L., Gaskin F., Cantor C. R. Microtubule assembly in the absence of added nucleotides. Proc Natl Acad Sci U S A. 1973 Mar;70(3):765–768. doi: 10.1073/pnas.70.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Vallota E. H., Müller-Eberhard H. J. Formation of C3a and C5a anaphylatoxins in whole human serum after inhibition of the anaphylatoxin inactivator. J Exp Med. 1973 May 1;137(5):1109–1123. doi: 10.1084/jem.137.5.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ward P. A. Leukotactic factors in health and disease. Am J Pathol. 1971 Sep;64(3):521–530. [PMC free article] [PubMed] [Google Scholar]
  25. Weisenberg R. C. Microtubule formation in vitro in solutions containing low calcium concentrations. Science. 1972 Sep 22;177(4054):1104–1105. doi: 10.1126/science.177.4054.1104. [DOI] [PubMed] [Google Scholar]

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

RESOURCES