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. 1991 Apr 15;88(8):3019–3023. doi: 10.1073/pnas.88.8.3019

Intracellular sites for storage and recycling of C3b receptors in human neutrophils.

M Berger 1, E M Wetzler 1, E Welter 1, J R Turner 1, A M Tartakoff 1
PMCID: PMC51375  PMID: 1826558

Abstract

Upon activation of human neutrophils, C3b receptors (type 1 complement receptors, CR1) are rapidly translocated from an intracellular pool to the surface, increasing plasma membrane expression 6- to 10-fold. This is followed by reinternalization and degradation of the receptors, even in the absence of ligand. Upregulation of surface CR1 may occur without exocytosis of primary or secondary granules, and intracellular CR1 in resting neutrophils does not sediment with these granules on density gradient fractionation. To directly localize the intracellular pools of CR1, we used immunoelectron microscopy of fixed, permeabilized cells. In resting neutrophils, CR1 is associated with the membranes of smooth-surfaced, empty-appearing vesicles whose irregular borders clearly distinguish them from primary and secondary granules. After activation by fMet-Leu-Phe, the intracellular pool is primarily found in large, conspicuous, multivesicular bodies. These bodies also incorporate colloidal gold from the extracellular fluid, suggesting that they are formed by endocytosis. Thus, the sites in which CR1 is stored in resting cells, and recycled in activated cells, are structurally unique and morphologically distinguishable.

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Selected References

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

  1. Arnaout M. A., Spits H., Terhorst C., Pitt J., Todd R. F., 3rd Deficiency of a leukocyte surface glycoprotein (LFA-1) in two patients with Mo1 deficiency. Effects of cell activation on Mo1/LFA-1 surface expression in normal and deficient leukocytes. J Clin Invest. 1984 Oct;74(4):1291–1300. doi: 10.1172/JCI111539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bainton D. F., Miller L. J., Kishimoto T. K., Springer T. A. Leukocyte adhesion receptors are stored in peroxidase-negative granules of human neutrophils. J Exp Med. 1987 Dec 1;166(6):1641–1653. doi: 10.1084/jem.166.6.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berger M., Birx D. L., Wetzler E. M., O'Shea J. J., Brown E. J., Cross A. S. Calcium requirements for increased complement receptor expression during neutrophil activation. J Immunol. 1985 Aug;135(2):1342–1348. [PubMed] [Google Scholar]
  4. Berger M., Medof M. E. Increased expression of complement decay-accelerating factor during activation of human neutrophils. J Clin Invest. 1987 Jan;79(1):214–220. doi: 10.1172/JCI112786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berger M., O'Shea J., Cross A. S., Folks T. M., Chused T. M., Brown E. J., Frank M. M. Human neutrophils increase expression of C3bi as well as C3b receptors upon activation. J Clin Invest. 1984 Nov;74(5):1566–1571. doi: 10.1172/JCI111572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berger M., Wetzler E. M., Wallis R. S. Tumor necrosis factor is the major monocyte product that increases complement receptor expression on mature human neutrophils. Blood. 1988 Jan;71(1):151–158. [PubMed] [Google Scholar]
  7. Blok J., Gibbs E. M., Lienhard G. E., Slot J. W., Geuze H. J. Insulin-induced translocation of glucose transporters from post-Golgi compartments to the plasma membrane of 3T3-L1 adipocytes. J Cell Biol. 1988 Jan;106(1):69–76. doi: 10.1083/jcb.106.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Borregaard N., Heiple J. M., Simons E. R., Clark R. A. Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J Cell Biol. 1983 Jul;97(1):52–61. doi: 10.1083/jcb.97.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Borregaard N., Miller L. J., Springer T. A. Chemoattractant-regulated mobilization of a novel intracellular compartment in human neutrophils. Science. 1987 Sep 4;237(4819):1204–1206. doi: 10.1126/science.3629236. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Dewald B., Bretz U., Baggiolini M. Release of gelatinase from a novel secretory compartment of human neutrophils. J Clin Invest. 1982 Sep;70(3):518–525. doi: 10.1172/JCI110643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fearon D. T., Collins L. A. Increased expression of C3b receptors on polymorphonuclear leukocytes induced by chemotactic factors and by purification procedures. J Immunol. 1983 Jan;130(1):370–375. [PubMed] [Google Scholar]
  13. Fletcher M. P., Gallin J. I. Human neutrophils contain an intracellular pool of putative receptors for the chemoattractant N-formyl-methionyl-leucyl-phenylalanine. Blood. 1983 Oct;62(4):792–799. [PubMed] [Google Scholar]
  14. Fletcher M. P., Seligmann B. E., Gallin J. I. Correlation of human neutrophil secretion, chemoattractant receptor mobilization, and enhanced functional capacity. J Immunol. 1982 Feb;128(2):941–948. [PubMed] [Google Scholar]
  15. Harbeck R. J., Hoffman A. A., Redecker S., Biundo T., Kurnick J. The isolation and functional activity of polymorphonuclear leukocytes and lymphocytes separated from whole blood on a single percoll density gradient. Clin Immunol Immunopathol. 1982 Jun;23(3):682–690. doi: 10.1016/0090-1229(82)90331-2. [DOI] [PubMed] [Google Scholar]
  16. Hibbs M. S., Bainton D. F. Human neutrophil gelatinase is a component of specific granules. J Clin Invest. 1989 Nov;84(5):1395–1402. doi: 10.1172/JCI114312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jost C. R., Huizinga T. W., de Goede R., Fransen J. A., Tetteroo P. A., Daha M. R., Ginsel L. A. Intracellular localization and de novo synthesis of FcRIII in human neutrophil granulocytes. Blood. 1990 Jan 1;75(1):144–151. [PubMed] [Google Scholar]
  18. McLean I. W., Nakane P. K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem. 1974 Dec;22(12):1077–1083. doi: 10.1177/22.12.1077. [DOI] [PubMed] [Google Scholar]
  19. McPhail L. C., Clayton C. C., Snyderman R. A potential second messenger role for unsaturated fatty acids: activation of Ca2+-dependent protein kinase. Science. 1984 May 11;224(4649):622–625. doi: 10.1126/science.6231726. [DOI] [PubMed] [Google Scholar]
  20. Miller L. J., Bainton D. F., Borregaard N., Springer T. A. Stimulated mobilization of monocyte Mac-1 and p150,95 adhesion proteins from an intracellular vesicular compartment to the cell surface. J Clin Invest. 1987 Aug;80(2):535–544. doi: 10.1172/JCI113102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Shea J. J., Brown E. J., Seligmann B. E., Metcalf J. A., Frank M. M., Gallin J. I. Evidence for distinct intracellular pools of receptors for C3b and C3bi in human neutrophils. J Immunol. 1985 Apr;134(4):2580–2587. [PubMed] [Google Scholar]
  22. Ohno Y., Gallin J. I. Diffusion of extracellular hydrogen peroxide into intracellular compartments of human neutrophils. Studies utilizing the inactivation of myeloperoxidase by hydrogen peroxide and azide. J Biol Chem. 1985 Jul 15;260(14):8438–8446. [PubMed] [Google Scholar]
  23. Petrequin P. R., Todd R. F., 3rd, Devall L. J., Boxer L. A., Curnutte J. T., 3rd Association between gelatinase release and increased plasma membrane expression of the Mo1 glycoprotein. Blood. 1987 Feb;69(2):605–610. [PubMed] [Google Scholar]
  24. Petty H. R., Smith L. M., Fearon D. T., McConnell H. M. Lateral distribution and diffusion of the C3b receptor of complement, HLA antigens, and lipid probes in peripheral blood leukocytes. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6587–6591. doi: 10.1073/pnas.77.11.6587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rouzer C. A., Kargman S. Translocation of 5-lipoxygenase to the membrane in human leukocytes challenged with ionophore A23187. J Biol Chem. 1988 Aug 5;263(22):10980–10988. [PubMed] [Google Scholar]
  26. Rustin G. J., Wilson P. D., Peters T. J. Studies on the subcellular localization of human neutrophil alkaline phosphatase. J Cell Sci. 1979 Apr;36:401–412. doi: 10.1242/jcs.36.1.401. [DOI] [PubMed] [Google Scholar]
  27. Todd R. F., 3rd, Arnaout M. A., Rosin R. E., Crowley C. A., Peters W. A., Babior B. M. Subcellular localization of the large subunit of Mo1 (Mo1 alpha; formerly gp 110), a surface glycoprotein associated with neutrophil adhesion. J Clin Invest. 1984 Oct;74(4):1280–1290. doi: 10.1172/JCI111538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tougard C., Louvard D., Picart R., Tixier-Vidal A. Antibodies against a lysosomal membrane antigen recognize a prelysosomal compartment involved in the endocytic pathway in cultured prolactin cells. J Cell Biol. 1985 Mar;100(3):786–793. doi: 10.1083/jcb.100.3.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Turner J. R., Tartakoff A. M., Berger M. Intracellular degradation of the complement C3b/C4b receptor in the absence of ligand. J Biol Chem. 1988 Apr 5;263(10):4914–4920. [PubMed] [Google Scholar]
  30. Zabucchi G., Menegazzi R., Soranzo M. R., Patriarca P. Uptake of human eosinophil peroxidase by human neutrophils. Am J Pathol. 1986 Sep;124(3):510–518. [PMC free article] [PubMed] [Google Scholar]

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