Phagocytosis induces superoxide formation and apoptosis in macrophages

Phagocytosis by inflammatory cells is an essential step and a part of innate immunity for protection against foreign pathogens, microorganism or dead cells. Phagocytosis, endocytotic events sequel to binding particle ligands to the specific receptors on phagocyte cell surface such as Fcγ recptor (FcγR), complement receptor (CR), β-glucan receptor, and phosphatidylserine (PS) receptor, require actin assembly, pseudopod extension and phagosome closure. Rho GTPases (RhoA, Cdc42, and Rac1) are critically involved in these processes. Abrupt superoxide formation, called as oxidative burst, occurs through NADPH oxidase complex in leukocytes following phagocytosis. NADPH oxidase complex is composed of membrane proteins, p22(PHOX)and gp91(PHOX), and cytosolic proteins, p40(PHOX), p47(PHOX)and p67(PHOX). The cytosolic subunits and Rac-GTP are translocated to the membrane, forming complete NADPH oxidase complex with membrane part subunits. Binding of imunoglobulin G (IgG)- and complement-opsonized particles to FcγR and CR of leukocytes induces apoptosis of the cells, which may be due to oxidative burst and accompanying cytochrome c release and casapase-3 activation.

[1]  P. Lachmann,et al.  Membrane complement receptor type three (CR3) has lectin-like properties analogous to bovine conglutinin as functions as a receptor for zymosan and rabbit erythrocytes as well as a receptor for iC3b. , 1985, Journal of immunology.

[2]  G. D. Ross,et al.  Regulation of the adhesion versus cytotoxic functions of the Mac-1/CR3/alphaMbeta2-integrin glycoprotein. , 2000, Critical reviews in immunology.

[3]  V. Souvannavong,et al.  Nitric oxide synthase induces macrophage death by apoptosis. , 1993, Biochemical and biophysical research communications.

[4]  A. Jesaitis,et al.  Phosphorylation of p 22 phox Is Mediated by Phospholipase D-dependent and-independent Mechanisms , 2000 .

[5]  P. Poindron,et al.  Both mannose and β‐glucan receptors are involved in phagocytosis of unopsonized, heat‐killed Saccharomyces cerevisiae by murine macrophages , 1993, Journal of leukocyte biology.

[6]  S. Becker,et al.  Mitochondrial oxidant production by a pollutant dust and NO-mediated apoptosis in human alveolar macrophage. , 2003, American journal of physiology. Cell physiology.

[7]  J. Bos,et al.  Activation of the small GTPase rap1 in human neutrophils. , 1998, Blood.

[8]  W. Nauseef,et al.  Neutrophil nicotinamide adenine dinucleotide phosphate oxidase assembly. Translocation of p47-phox and p67-phox requires interaction between p47-phox and cytochrome b558. , 1991, The Journal of clinical investigation.

[9]  Robert M. Stahl,et al.  Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: Cell fate is regulated at the level of gene expression , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  L. Schlesinger,et al.  Activation of phospholipase D is tightly coupled to the phagocytosis of Mycobacterium tuberculosis or opsonized zymosan by human macrophages , 1996, The Journal of experimental medicine.

[11]  O. Inanami,et al.  Relationship between p38 mitogen-activated protein kinase and small GTPase Rac for the activation of NADPH oxidase in bovine neutrophils. , 2002, Biochemical and biophysical research communications.

[12]  Mike Rothe,et al.  Tumor necrosis factor's cytotoxic activity is signaled by the p55 TNF receptor , 1993, Cell.

[13]  M. Benito,et al.  Reactive oxygen species (ROS) mediates the mitochondrial‐dependent apoptosis induced by transforming growth factor ß in fetal hepatocytes , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[14]  Bin Zhang,et al.  Elucidation of Molecular Events Leading to Neutrophil Apoptosis following Phagocytosis , 2003, Journal of Biological Chemistry.

[15]  K. Ha,et al.  The essential role of H2O2 in the regulation of intracellular Ca2+ by epidermal growth factor in rat-2 fibroblasts. , 2000, Cellular signalling.

[16]  Jae-Bong Park,et al.  Phagocytosis of serum-and IgG-opsonized zymosan particles induces apoptosis through superoxide but not nitric oxide in macrophage J774A.1 , 2003, Experimental & Molecular Medicine.

[17]  S. Estus,et al.  t NADPH Oxidase Contributes Directly to Oxidative Stress and Apoptosis in Nerve Growth Factor-Deprived Sympathetic Neurons , 2000, The Journal of Neuroscience.

[18]  S. Orkin,et al.  Association of a Ras-related protein with cytochrome b of human neutrophils , 1989, Nature.

[19]  A. Hall,et al.  Rho GTPases and the actin cytoskeleton. , 1998, Science.

[20]  O. Inanami,et al.  Roles of p38 MAPK, PKC and PI3‐K in the signaling pathways of NADPH oxidase activation and phagocytosis in bovine polymorphonuclear leukocytes , 2000, FEBS letters.

[21]  M. Symons,et al.  Activation of rat liver phospholipase D by the small GTP-binding protein RhoA. , 1994, The Journal of biological chemistry.

[22]  D. Bar-Sagi,et al.  Redox-dependent downregulation of Rho by Rac , 2003, Nature Cell Biology.

[23]  S. Grinstein,et al.  Rho is Required for the Initiation of Calcium Signaling and Phagocytosis by Fcγ Receptors in Macrophages , 1997, The Journal of experimental medicine.

[24]  B. Babior,et al.  Activation of the leukocyte NADPH oxidase subunit p47phox by protein kinase C. A phosphorylation-dependent change in the conformation of the C-terminal end of p47phox. , 1997, Biochemistry.

[25]  D. Rotrosen,et al.  Production of recombinant cytochrome b558 allows reconstitution of the phagocyte NADPH oxidase solely from recombinant proteins. , 1993, The Journal of biological chemistry.

[26]  S. Grinstein,et al.  v-SNARE-dependent secretion is required for phagocytosis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  K. Kaibuchi,et al.  Regulation of the superoxide-generating NADPH oxidase by a small GTP-binding protein and its stimulatory and inhibitory GDP/GTP exchange proteins. , 1992, The Journal of biological chemistry.

[28]  R. May,et al.  Phagocytosis and the actin cytoskeleton. , 2001, Journal of cell science.

[29]  T. Tsuruo,et al.  Caspase-mediated cleavage of p21Waf1/Cip1 converts cancer cells from growth arrest to undergoing apoptosis , 1999, Oncogene.

[30]  Philippe Montcourrier,et al.  Fc receptor‐mediated phagocytosis requires CDC42 and Rac1 , 1998, The EMBO journal.

[31]  M. Dinauer,et al.  Rac2 Is an Essential Regulator of Neutrophil Nicotinamide Adenine Dinucleotide Phosphate Oxidase Activation in Response to Specific Signaling Pathways1 , 2001, The Journal of Immunology.

[32]  Fumio Matsumura,et al.  Distinct Roles of Rock (Rho-Kinase) and Mlck in Spatial Regulation of Mlc Phosphorylation for Assembly of Stress Fibers and Focal Adhesions in 3t3 Fibroblasts , 2000, The Journal of cell biology.

[33]  K. Park,et al.  Genomic organization and expression of parkin in Drosophila melanogaster , 2003, Experimental & Molecular Medicine.

[34]  B. Robinson,et al.  Mitochondria, oxygen free radicals, and apoptosis. , 2001, American journal of medical genetics.

[35]  T. Miyawaki,et al.  Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. , 1997, Blood.

[36]  Yong-Sun Kim,et al.  Identification of amyloid β-peptide responsive genes by cDNA microarray technology: Involvement of RTP801 in amyloid β-peptide toxicity , 2003, Experimental & Molecular Medicine.

[37]  Laura M. Machesky,et al.  Scar1 and the related Wiskott–Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex , 1998, Current Biology.

[38]  A. Gomez-Muñoz,et al.  Dissociated ROS production and ceramide generation in sulfasalazine‐induced cell death in Raw 264.7 cells , 2002, Journal of leukocyte biology.

[39]  J. Lambeth,et al.  Participation of the small molecular weight GTP-binding protein Rac1 in cell-free activation and assembly of the respiratory burst oxidase. Inhibition by a carboxyl-terminal Rac peptide. , 1994, The Journal of biological chemistry.

[40]  I. Maridonneau-Parini,et al.  Nonopsonic Phagocytosis of Zymosan and Mycobacterium kansasii by CR3 (CD11b/CD18) Involves Distinct Molecular Determinants and Is or Is Not Coupled with NADPH Oxidase Activation , 2000, Infection and Immunity.

[41]  Hidemi Watanabe,et al.  LIM Kinase 1 Modulates Opsonized Zymosan-triggered Activation of Macrophage-like U937 Cells , 2002, The Journal of Biological Chemistry.

[42]  J. Shayman,et al.  Regulation of polymorphonuclear leukocyte phagocytosis by myosin light chain kinase after activation of mitogen-activated protein kinase. , 2000, Blood.

[43]  Byung-Hyun Park,et al.  D4-GDI is cleaved by caspase-3 during daunorubicin-induced apoptosis in HL-60 cells , 2002, Experimental & Molecular Medicine.

[44]  C. Bogdan,et al.  LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-alpha. , 2000, Blood.

[45]  V. Fadok,et al.  Activation of SHIP by NADPH Oxidase-stimulated Lyn Leads to Enhanced Apoptosis in Neutrophils* , 2002, The Journal of Biological Chemistry.

[46]  C. Ong,et al.  Reactive oxygen species and caspase activation mediate silica-induced apoptosis in alveolar macrophages. , 2001, American journal of physiology. Lung cellular and molecular physiology.

[47]  A. Hall,et al.  Vav regulates activation of Rac but not Cdc42 during FcγR-mediated phagocytosis , 2002 .

[48]  M. Matsuo,et al.  Oxidative stress-induced cell death of human oral neutrophils. , 2003, American journal of physiology. Cell physiology.

[49]  C. Dahlgren,et al.  Particles binding beta(2)-integrins mediate intracellular production of oxidative metabolites in human neutrophils independently of phagocytosis. , 1999, Biochimica et biophysica acta.

[50]  S. Kong,et al.  Gliotoxin induces apoptosis in cultured macrophages via production of reactive oxygen species and cytochrome c release without mitochondrial depolarization , 2001, Free radical research.

[51]  A. Ridley,et al.  Rho family proteins: coordinating cell responses. , 2001, Trends in cell biology.

[52]  J. Geffner,et al.  Modulation of human neutrophil apoptosis by immune complexes. , 1998, Journal of immunology.

[53]  Arturo Casadevall,et al.  CR3 (CD11b/CD18) and CR4 (CD11c/CD18) are involved in complement-independent antibody-mediated phagocytosis of Cryptococcus neoformans. , 2002, Immunity.

[54]  J. A. Badwey,et al.  Naphthalenesulphonamides block neutrophil superoxide production by intact cells and in a cell-free system: is myosin light chain kinase responsible for these effects? , 1995, The Biochemical journal.

[55]  J. Massagué,et al.  Myc suppression of the p21Cip1 Cdk inhibitor influences the outcome of the p53 response to DNA damage , 2002, Nature.

[56]  S. H. Lee,et al.  Roles of RhoA and phospholipase A2 in the elevation of intracellular H2O2 by transforming growth factor-beta in Swiss 3T3 fibroblasts. , 1999, Cellular signalling.

[57]  S. Grinstein,et al.  Restricted Accumulation of Phosphatidylinositol 3-Kinase Products in a Plasmalemmal Subdomain during Fcγ Receptor-Mediated Phagocytosis , 2001, The Journal of cell biology.

[58]  G. Bokoch,et al.  Inhibition of myosin light chain kinase by p21-activated kinase. , 1999, Science.

[59]  C. Tseng,et al.  A requirement for ARF6 in Fcgamma receptor-mediated phagocytosis in macrophages. , 1998, The Journal of biological chemistry.