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. 1988 Dec;85(23):9204–9208. doi: 10.1073/pnas.85.23.9204

Anti-immunoglobulin pretreatment induces a calcium-mobilization response to the chemotactic agent N-formylmethionylleucylphenylalanine in Daudi lymphoblastoid cells.

C I Kalunta 1, J S Kaptein 1, H Niedzin 1, S J Scott 1, G H Lee 1, P M Lad 1
PMCID: PMC282707  PMID: 3194420

Abstract

Anti-immunoglobulin treatment of fura-2-loaded Daudi cells induces a calcium mobilization as judged by the increase in the fluorescence of the dye fura-2, AM. No calcium mobilization by N-fMet-Leu-Phe is observed in these cells. However, exposure of the cells to N-fMet-Leu-Phe after the first hit with anti-immunoglobulin (but not after soluble IgG) shows a rapid, dose-dependent calcium mobilization by N-fMet-Leu-Phe. The expression of the calcium-mobilizing response occurs in less than 2 min and is stable. Binding of tritiated N-fMet-Leu-Phe is increased in anti-immunoglobulin-treated but not control cells. The induction is specific for N-fMet-Leu-Phe because the chemoattractant platelet-activating factor did not induce any calcium mobilization. The N-fMet-Leu-Phe antagonist t-butoxycarbonyl-L-Phe-D-Leu-L-Phe-D-Leu-L-Phe- OH did not show any calcium mobilization on its own, either before or after anti-immunoglobulin treatment, and inhibited the calcium mobilization of N-fMet-Leu-Phe at low concentrations. Treatment of the cells with phorbol 12-myristate 13-acetate or pertussis toxin prior to anti-immunoglobulin treatment caused a dose-dependent abolition of both the anti-immunoglobulin-mediated calcium mobilization and the subsequent calcium mobilization by N-fMet-Leu-Phe. Metabolic inhibitors that act predominantly by lowering the ATP levels within the cell (iodoacetate, sodium fluoride, oligomycin, and 2-deoxyglucose) all produced a greater inhibition of the N-fMet-Leu-Phe-mediated calcium mobilization than the anti-immunoglobulin-mediated response. Lowering the temperature from 37 degrees C to 22 degrees C reduced the anti-immunoglobulin response and completely inhibited the expression of the N-fMet-Leu-Phe effect. Our results indicate that activation of the calcium-mobilization pathway in B cells by crosslinking of bound surface immunoglobulin causes an induction of N-fMet-Leu-Phe-sensitive calcium mobilization.

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Selected References

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

  1. Anderson R. A., Marchesi V. T. Regulation of the association of membrane skeletal protein 4.1 with glycophorin by a polyphosphoinositide. Nature. 1985 Nov 21;318(6043):295–298. doi: 10.1038/318295a0. [DOI] [PubMed] [Google Scholar]
  2. Becker E. L., Kermode J. C., Naccache P. H., Yassin R., Munoz J. J., Marsh M. L., Huang C. K., Sha'afi R. I. Pertussis toxin as a probe of neutrophil activation. Fed Proc. 1986 Jun;45(7):2151–2155. [PubMed] [Google Scholar]
  3. Becker E. L. Leukocyte stimulation: receptor, membrane, and metabolic events. Introduction and summary. Fed Proc. 1986 Jun;45(7):2148–2150. [PubMed] [Google Scholar]
  4. 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]
  5. Bijsterbosch M. K., Meade C. J., Turner G. A., Klaus G. G. B lymphocyte receptors and polyphosphoinositide degradation. Cell. 1985 Jul;41(3):999–1006. doi: 10.1016/s0092-8674(85)80080-5. [DOI] [PubMed] [Google Scholar]
  6. Bretscher M. S. Endocytosis: relation to capping and cell locomotion. Science. 1984 May 18;224(4650):681–686. doi: 10.1126/science.6719108. [DOI] [PubMed] [Google Scholar]
  7. Cambier J. C., Ransom J. T. Molecular mechanisms of transmembrane signaling in B lymphocytes. Annu Rev Immunol. 1987;5:175–199. doi: 10.1146/annurev.iy.05.040187.001135. [DOI] [PubMed] [Google Scholar]
  8. Connolly T. M., Lawing W. J., Jr, Majerus P. W. Protein kinase C phosphorylates human platelet inositol trisphosphate 5'-phosphomonoesterase, increasing the phosphatase activity. Cell. 1986 Sep 12;46(6):951–958. doi: 10.1016/0092-8674(86)90077-2. [DOI] [PubMed] [Google Scholar]
  9. Dahlgren C., Andersson T., Stendahl O. Chemotactic factor binding and functional capacity: a comparison between human granulocytes and differentiated HL-60 cells. J Leukoc Biol. 1987 Sep;42(3):245–252. doi: 10.1002/jlb.42.3.245. [DOI] [PubMed] [Google Scholar]
  10. Dulis B. H., Kloppel T. M., Grey H. M., Kubo R. T. Regulation of catabolism of IgM heavy chains in a B lymphoma cell line. J Biol Chem. 1982 Apr 25;257(8):4369–4374. [PubMed] [Google Scholar]
  11. Fletcher M. P., Gallin J. I. Degranulating stimuli increase the availability of receptors on human neutrophils for the chemoattractant f-met-leu-phe. J Immunol. 1980 Apr;124(4):1585–1588. [PubMed] [Google Scholar]
  12. 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]
  13. Goldman D. W., Goetzl E. J. Heterogeneity of human polymorphonuclear leukocyte receptors for leukotriene B4. Identification of a subset of high affinity receptors that transduce the chemotactic response. J Exp Med. 1984 Apr 1;159(4):1027–1041. doi: 10.1084/jem.159.4.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grewal I. S., Olson C. V., Scott S. J., Lad P. M. Cap formation in a B-lymphocyte cell line is inhibited by pertussis toxin and phorbol ester. Immunology. 1987 Jun;61(2):131–135. [PMC free article] [PubMed] [Google Scholar]
  15. Karnieli E., Chernow B., Hissin P. J., Simpson I. A., Foley J. E. Insulin stimulates glucose transport in isolated human adipose cells through a translocation of intracellular glucose transporters to the plasma membrane: a preliminary report. Horm Metab Res. 1986 Dec;18(12):867–868. doi: 10.1055/s-2007-1012458. [DOI] [PubMed] [Google Scholar]
  16. Klein E., Klein G., Nadkarni J. S., Nadkarni J. J., Wigzell H., Clifford P. Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res. 1968 Jul;28(7):1300–1310. [PubMed] [Google Scholar]
  17. Korchak H. M., Rutherford L. E., Weissmann G. Stimulus response coupling in the human neutrophil. I. Kinetic analysis of changes in calcium permeability. J Biol Chem. 1984 Apr 10;259(7):4070–4075. [PubMed] [Google Scholar]
  18. Kubagawa H., Burrows P. D., Grossi C. E., Cooper M. D. Epstein-Barr virus induced differentiation of early B-lineage cells. Curr Top Microbiol Immunol. 1986;132:246–250. doi: 10.1007/978-3-642-71562-4_37. [DOI] [PubMed] [Google Scholar]
  19. Lad P. M., Olson C. V., Grewal I. S. Role of a pertussis toxin substrate in the control of lectin-induced cap formation in human neutrophils. Biochem J. 1986 Aug 15;238(1):29–36. doi: 10.1042/bj2380029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lad P. M., Olson C. V., Grewal I. S., Scott S. J. A pertussis toxin-sensitive GTP-binding protein in the human neutrophil regulates multiple receptors, calcium mobilization, and lectin-induced capping. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8643–8647. doi: 10.1073/pnas.82.24.8643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lassing I., Lindberg U. Specific interaction between phosphatidylinositol 4,5-bisphosphate and profilactin. Nature. 1985 Apr 4;314(6010):472–474. doi: 10.1038/314472a0. [DOI] [PubMed] [Google Scholar]
  22. Lew P. D., Monod A., Waldvogel F. A., Dewald B., Baggiolini M., Pozzan T. Quantitative analysis of the cytosolic free calcium dependency of exocytosis from three subcellular compartments in intact human neutrophils. J Cell Biol. 1986 Jun;102(6):2197–2204. doi: 10.1083/jcb.102.6.2197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Liao C. S., Freer R. J. Cryptic receptors for chemotactic peptides in rabbit neutrophils. Biochem Biophys Res Commun. 1980 Mar 28;93(2):566–571. doi: 10.1016/0006-291x(80)91114-6. [DOI] [PubMed] [Google Scholar]
  24. Maly F. E., Cross A. R., Jones O. T., Wolf-Vorbeck G., Walker C., Dahinden C. A., De Weck A. L. The superoxide generating system of B cell lines. Structural homology with the phagocytic oxidase and triggering via surface Ig. J Immunol. 1988 Apr 1;140(7):2334–2339. [PubMed] [Google Scholar]
  25. Morabito F., Prasthofer E. F., Dunlap N. E., Grossi C. E., Tilden A. B. Expression of myelomonocytic antigens on chronic lymphocytic leukemia B cells correlates with their ability to produce interleukin 1. Blood. 1987 Dec;70(6):1750–1757. [PubMed] [Google Scholar]
  26. Morgan E. L., Thoman M. L., Weigle W. O., Hugli T. E. Anaphylatoxin-mediated regulation of the immune response. II. C5a-mediated enhancement of human humoral and T cell-mediated immune responses. J Immunol. 1983 Mar;130(3):1257–1261. [PubMed] [Google Scholar]
  27. Nachshen D. A., Pfeffer L. M., Tamm I. Effect of anti-Ig on cytosolic Ca2+ in Daudi lymphoblastoid cells. J Biol Chem. 1986 Nov 15;261(32):15134–15139. [PubMed] [Google Scholar]
  28. Patrignani P., Valitutti S., Aiello F., Musiani P. Platelet-activating factor (PAF) receptor antagonists inhibit mitogen-induced human peripheral blood T-cell proliferation. Biochem Biophys Res Commun. 1987 Oct 29;148(2):802–810. doi: 10.1016/0006-291x(87)90947-8. [DOI] [PubMed] [Google Scholar]
  29. Pozzan T., Arslan P., Tsien R. Y., Rink T. J. Anti-immunoglobulin, cytoplasmic free calcium, and capping in B lymphocytes. J Cell Biol. 1982 Aug;94(2):335–340. doi: 10.1083/jcb.94.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rola-Pleszczynski M., Pignol B., Pouliot C., Braquet P. Inhibition of human lymphocyte proliferation and interleukin 2 production by platelet activating factor (PAF-acether): reversal by a specific antagonist, BN 52021. Biochem Biophys Res Commun. 1987 Feb 13;142(3):754–760. doi: 10.1016/0006-291x(87)91478-1. [DOI] [PubMed] [Google Scholar]
  31. Rothstein T. L., Kolber D. L., Simons E. R., Baeker T. R. Inhibition by phorbol esters of antiimmunoglobulin-induced calcium signalling and B-cell activation. J Cell Physiol. 1986 Dec;129(3):347–355. doi: 10.1002/jcp.1041290313. [DOI] [PubMed] [Google Scholar]
  32. Singer P. A., Singer H. H., Williamson A. R. Different species of messenger RNA encode receptor and secretory IgM mu chains differing at their carboxy termini. Nature. 1980 May 29;285(5763):294–300. doi: 10.1038/285294a0. [DOI] [PubMed] [Google Scholar]
  33. Smith C. D., Lane B. C., Kusaka I., Verghese M. W., Snyderman R. Chemoattractant receptor-induced hydrolysis of phosphatidylinositol 4,5-bisphosphate in human polymorphonuclear leukocyte membranes. Requirement for a guanine nucleotide regulatory protein. J Biol Chem. 1985 May 25;260(10):5875–5878. [PubMed] [Google Scholar]
  34. Tedder T. F., Weis J. J., Clement L. T., Fearon D. T., Cooper M. D. The role of receptors for complement in the induction of polyclonal B-cell proliferation and differentiation. J Clin Immunol. 1986 Jan;6(1):65–73. doi: 10.1007/BF00915366. [DOI] [PubMed] [Google Scholar]
  35. Toyoda N., Robinson F. W., Smith M. M., Flanagan J. E., Kono T. Apparent translocation of glucose transport activity in rat epididymal adipocytes by insulin-like effects of high pH or hyperosmolarity. J Biol Chem. 1986 Feb 15;261(5):2117–2122. [PubMed] [Google Scholar]
  36. Unanue E. R., Allen P. M. The basis for the immunoregulatory role of macrophages and other accessory cells. Science. 1987 May 1;236(4801):551–557. doi: 10.1126/science.2437650. [DOI] [PubMed] [Google Scholar]
  37. Verghese M. W., Smith C. D., Snyderman R. Potential role for a guanine nucleotide regulatory protein in chemoattractant receptor mediated polyphosphoinositide metabolism, Ca++ mobilization and cellular responses by leukocytes. Biochem Biophys Res Commun. 1985 Mar 15;127(2):450–457. doi: 10.1016/s0006-291x(85)80181-9. [DOI] [PubMed] [Google Scholar]
  38. Volkman D. J., Buescher E. S., Gallin J. I., Fauci A. S. B cell lines as models for inherited phagocytic diseases: abnormal superoxide generation in chronic granulomatous disease and giant granules in Chediak-Higashi syndrome. J Immunol. 1984 Dec;133(6):3006–3009. [PubMed] [Google Scholar]
  39. Volpi M., Yassin R., Tao W., Molski T. F., Naccache P. H., Sha'afi R. I. Leukotriene B4 mobilizes calcium without the breakdown of polyphosphoinositides and the production of phosphatidic acid in rabbit neutrophils. Proc Natl Acad Sci U S A. 1984 Oct;81(19):5966–5969. doi: 10.1073/pnas.81.19.5966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weigle W. O., Goodman M. G., Morgan E. L., Hugli T. E. Regulation of immune response by components of the complement cascade and their activated fragments. Springer Semin Immunopathol. 1983;6(2-3):173–194. doi: 10.1007/BF00205872. [DOI] [PubMed] [Google Scholar]
  41. Yancey K. B., O'Shea J., Chused T., Brown E., Takahashi T., Frank M. M., Lawley T. J. Human C5a modulates monocyte Fc and C3 receptor expression. J Immunol. 1985 Jul;135(1):465–470. [PubMed] [Google Scholar]

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