Home LiteratureArticle Details
PMID: 8383692 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Immune complex-stimulated neutrophil LTB4 production is dependent on beta 2 integrins.

The Journal of cell biology ·Vol. 120 ·No. 6 ·1993-03-00 ·Pages 1509-17

Graham IL, Lefkowith JB, Anderson DC, Brown EJ

Abstract

The beta 2 integrins (LFA-1, Mac-1, and p150,95) are critical for many adhesive functions of leukocytes. Although the binding of the IgG-opsonized particles occurs normally in the absence of beta 2 integrins, phagocytosis of IgG-opsonized particles by activated neutrophils (PMN) requires these integrins. This observation suggests a role for beta 2 integrins in phagocytosis subsequent to particle binding. To investigate the mechanism of involvement of beta 2 integrins in IgG-mediated functions, we examined the role of beta 2 integrins in adhesion to immune complex (IC)-coated surfaces. Initial adhesion and spreading on IC-coated surfaces were equivalent in control and beta 2-deficient phagocytes. However, both genetically beta 2-deficient PMN and PMN treated with the anti-beta 2 mAb IB4 subsequently detached from the IC-coated surfaces. To determine whether biochemical consequences of IgG activation were also affected by beta 2 deficiency, LTB4 production in response to Fc receptor ligation was assessed. LTB4 production by beta 2-deficient PMN adherent to IC-coated surfaces was markedly decreased in comparison with control PMN. Importantly, LTB4 production by PMN stimulated with fluid phase heat-aggregated IgG also required the beta 2 integrins, showing that the defect was not a simple consequence of abnormal adhesion. In contrast, superoxide production by IC-adherent PMN was equivalent in control and beta 2-deficient PMN. The initial rises in intracytoplasmic [Ca2+]i in response to aggregated IgG also were unaffected by inhibition of beta 2 integrins. These data show that lack of beta 2 integrins does not inhibit all FcR-dependent signal transduction. Finally, LTB4 production by normal PMN adherent to ICs was inhibited by antibodies to FcRII, but not FcRIII, showing that FcRII ligation was required for this effect. Together these data identify a role for the beta 2 integrins in a signal transduction pathway leading to sustained adhesion and LTB4 production in response to IC. Since both beta 2 integrins and FcRII are required for these effects, the data further suggest cooperation between these receptors in generating PMN activation in response to IC stimulation.

MeSH Terms
Actins/analysis,blood Antibodies, Monoclonal Antigen-Antibody Complex Calcium/blood Cell Adhesion Cell Line Humans Immunoglobulin G/pharmacology Kinetics Leukotriene B4/biosynthesis,blood Lymphocyte Function-Associated Antigen-1/genetics,physiology Muramidase/blood N-Formylmethionine Leucyl-Phenylalanine/pharmacology Neutrophils/cytology,drug effects,physiology Receptors, IgG/physiology
Chemicals
Actins Antibodies, Monoclonal Antigen-Antibody Complex Immunoglobulin G Lymphocyte Function-Associated Antigen-1 Receptors, IgG Leukotriene B4 N-Formylmethionine Leucyl-Phenylalanine Muramidase Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Graham I L
Department of Pediatrics, Washington University Medical School, St. Louis, Missouri 63110.
Lefkowith J B
Anderson D C
Brown E J
References (44)
44 references, click to expand
  1. Cytosolic free calcium increases before and oscillates during frustrated phagocytosis in macrophages.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2685-93 PMID: 3693396
  2. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1).
    Cell. 1987 Dec 4;51(5):813-9 PMID: 3315233
  3. Increased surface expression of CD11b/CD18 (Mac-1) is not required for stimulated neutrophil adherence to cultured endothelium.
    J Clin Invest. 1988 Mar;81(3):676-82 PMID: 3278004
  4. Dissociation between increased surface expression of gp165/95 and homotypic neutrophil aggregation.
    J Immunol. 1988 May 1;140(9):3156-60 PMID: 3283242
  5. Kinetic effects of ATP and two cellular stimulatory components on human leukocyte 5-lipoxygenase.
    Ann N Y Acad Sci. 1988;524:1-11 PMID: 3382136
  6. Translocation of 5-lipoxygenase to the membrane in human leukocytes challenged with ionophore A23187.
    J Biol Chem. 1988 Aug 5;263(22):10980-8 PMID: 3134355
  7. Lymphocyte function-associated antigen-1 (LFA-1) interaction with intercellular adhesion molecule-1 (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells.
    J Cell Biol. 1988 Jul;107(1):321-31 PMID: 3134364
  8. Leukocyte locomotion and chemotaxis. New methods for evaluation, and demonstration of a cell-derived chemotactic factor.
    J Exp Med. 1973 Feb 1;137(2):387-410 PMID: 4568301
  9. Molecular complexity of leukocyte surface glycoproteins related to the macrophage differentiation antigen Mac-1.
    J Exp Med. 1981 Nov 1;154(5):1517-24 PMID: 7299345
  10. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies.
    Proc Natl Acad Sci U S A. 1983 Sep;80(18):5699-703 PMID: 6225125
  11. Definition of a common leukocyte cell-surface antigen (Lp95-150) associated with diverse cell-mediated immune functions.
    J Immunol. 1983 Dec;131(6):2913-8 PMID: 6644024
  12. A human leukocyte differentiation antigen family with distinct alpha-subunits and a common beta-subunit: the lymphocyte function-associated antigen (LFA-1), the C3bi complement receptor (OKM1/Mac-1), and the p150,95 molecule.
    J Exp Med. 1983 Dec 1;158(6):1785-1803 PMID: 6196430
  13. Superoxide production.
    Methods Enzymol. 1984;105:370-8 PMID: 6328189
  14. Abnormalities of polymorphonuclear leukocyte function associated with a heritable deficiency of high molecular weight surface glycoproteins (GP138): common relationship to diminished cell adherence.
    J Clin Invest. 1984 Aug;74(2):536-51 PMID: 6746906
  15. Ca2+-dependent and Ca2+-independent phagocytosis in human neutrophils.
    Nature. 1985 Jun 6-12;315(6019):509-11 PMID: 3158824
  16. Deficiency of two human leukocyte surface membrane glycoproteins (Mo1 and LFA-1).
    Fed Proc. 1985 Jul;44(10):2664-70 PMID: 3891419
  17. Studies on the molecular mechanisms of human Fc receptor-mediated phagocytosis. Amplification of ingestion is dependent on the generation of reactive oxygen metabolites and is deficient in polymorphonuclear leukocytes from patients with chronic granulomatous disease.
    J Clin Invest. 1988 Oct;82(4):1192-201 PMID: 3049672
  18. An immobile subset of plasma membrane CD11b/CD18 (Mac-1) is involved in phagocytosis of targets recognized by multiple receptors.
    J Immunol. 1989 Apr 1;142(7):2352-8 PMID: 2538507
  19. Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1.
    Nature. 1989 May 4;339(6219):61-4 PMID: 2497351
  20. Formyl peptide-induced chemotaxis of human polymorphonuclear leukocytes does not require either marked changes in cytosolic calcium or specific granule discharge. Role of formyl peptide receptor reexpression (or recycling).
    J Clin Invest. 1989 Jun;83(6):1963-70 PMID: 2723068
  21. Cytokine-induced respiratory burst of human neutrophils: dependence on extracellular matrix proteins and CD11/CD18 integrins.
    J Cell Biol. 1989 Sep;109(3):1341-9 PMID: 2475511
  22. Enzymes involved in the biosynthesis of leukotriene B4.
    J Biol Chem. 1989 Nov 25;264(33):19469-72 PMID: 2555321
  23. Identification and isolation of a membrane protein necessary for leukotriene production.
    Nature. 1990 Jan 18;343(6255):278-81 PMID: 2300172
  24. Requirement of a 5-lipoxygenase-activating protein for leukotriene synthesis.
    Nature. 1990 Jan 18;343(6255):282-4 PMID: 2300173
  25. Human neutrophil adherence to laminin in vitro. Evidence for a distinct neutrophil integrin receptor for laminin.
    J Exp Med. 1990 Apr 1;171(4):1221-37 PMID: 1969920
  26. The glycosyl phosphatidylinositol-linked Fc gamma RIIIPMN mediates transmembrane signaling events distinct from Fc gamma RII.
    J Exp Med. 1990 Apr 1;171(4):1239-55 PMID: 2139101
  27. Adhesion receptors of the immune system.
    Nature. 1990 Aug 2;346(6283):425-34 PMID: 1974032
  28. Soluble and insoluble immune complexes activate human neutrophil NADPH oxidase by distinct Fc gamma receptor-specific mechanisms.
    J Immunol. 1990 Nov 1;145(9):3026-32 PMID: 2170530
  29. Tumor necrosis factor and CD11/CD18 (beta 2) integrins act synergistically to lower cAMP in human neutrophils.
    J Cell Biol. 1990 Nov;111(5 Pt 1):2171-81 PMID: 1699953
  30. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18).
    J Cell Biol. 1990 Dec;111(6 Pt 2):3129-39 PMID: 1980124
  31. Extracellular calcium results in a conformational change in Mac-1 (CD11b/CD18) on neutrophils. Differentiation of adhesion and phagocytosis functions of Mac-1.
    J Immunol. 1991 Jan 15;146(2):685-91 PMID: 1702813
  32. Multiple elevations of cytosolic-free Ca2+ in human neutrophils: initiation by adherence receptors of the integrin family.
    J Cell Biol. 1991 Mar;112(6):1249-57 PMID: 1900302
  33. Leukocyte adhesion-deficient neutrophils fail to amplify phagocytic function in response to stimulation. Evidence for CD11b/CD18-dependent and -independent mechanisms of phagocytosis.
    J Clin Invest. 1991 Aug;88(2):588-97 PMID: 1677946
  34. Fc receptors.
    Annu Rev Immunol. 1991;9:457-92 PMID: 1910686
  35. The cytoplasmic domain of the integrin lymphocyte function-associated antigen 1 beta subunit: sites required for binding to intercellular adhesion molecule 1 and the phorbol ester-stimulated phosphorylation site.
    J Exp Med. 1991 Nov 1;174(5):1227-38 PMID: 1682411
  36. Generation of signals activating neutrophil functions by leukocyte integrins: LFA-1 and gp150/95, but not CR3, are able to stimulate the respiratory burst of human neutrophils.
    J Cell Biol. 1992 Feb;116(4):1007-17 PMID: 1346398
  37. Insoluble immune complex-stimulated neutrophil leukotriene B4 production is dependent on Fc gamma RII and Fc gamma RIII and independent of pertussis toxin-sensitive signal transduction pathways.
    Am J Pathol. 1992 Mar;140(3):613-20 PMID: 1312307
  38. Integrins: versatility, modulation, and signaling in cell adhesion.
    Cell. 1992 Apr 3;69(1):11-25 PMID: 1555235
  39. On the expression and regulation of 5-lipoxygenase in human lymphocytes.
    Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3521-5 PMID: 1314391
  40. Surface-bound immune complexes trigger transmembrane proximity between complement receptor type 3 and the neutrophil's cortical microfilaments.
    J Immunol. 1992 Jun 1;148(11):3550-3 PMID: 1534099
  41. Phospholipase activation during monocyte adherence and spreading.
    J Immunol. 1992 Sep 1;149(5):1729-35 PMID: 1506690
  42. Stimulation of human neutrophil Fc receptor-mediated phagocytosis by a low molecular weight cytokine.
    J Immunol. 1986 Aug 1;137(3):868-75 PMID: 3522738
  43. Metabolic and functional alterations in macrophages induced by essential fatty acid deficiency.
    J Biol Chem. 1987 May 15;262(14):6668-75 PMID: 3571276
  44. Mechanism of inhibition of immunoglobulin G-mediated phagocytosis by monoclonal antibodies that recognize the Mac-1 antigen.
    J Clin Invest. 1988 Feb;81(2):365-75 PMID: 2963020
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1993-03-00
Pages
1509-17
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119752
Subset
IM
Grants
NIAID NIH HHS · AI-24674 · United States
NIGMS NIH HHS · GM-38330 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com