The Src homology 2 domain-containing inositol 5-phosphatase negatively regulates Fcgamma receptor-mediated phagocytosis through immunoreceptor tyrosine-based activation motif-bearing phagocytic receptors.

Molecular mechanisms by which the Src homology 2 domain-containing inositol 5-phosphatase (SHIP) negatively regulates phagocytosis in macrophages are unclear. We addressed the issue using bone marrow-derived macrophages from FcgammaR- or SHIP-deficient mice. Phagocytic activities of macrophages from FcgammaRII(b)(-/-) and SHIP(-/-) mice were enhanced to a similar extent, relative to those from wild type. However, calcium influx was only marginally affected in FcgammaRII(b)(-/-), but greatly enhanced in SHIP(-/-) macrophages. Furthermore, SHIP was phosphorylated on tyrosine residues upon FcgammaR aggregation even in macrophages from FcgammaRII(b)(-/-) mice or upon clustering of a chimeric receptor containing CD8 and the immunoreceptor tyrosine-based activation motif (ITAM)-bearing gamma-chain or human-restricted FcgammaRIIa. These findings indicate that, unlike B cells, SHIP is efficiently phosphorylated in the absence of an immunoreceptor tyrosine-based inhibition motif (ITIM)-bearing receptor. We further demonstrate that SHIP directly bound to phosphorylated peptides derived from FcgammaRIIa with a high affinity, comparable to that of FcgammaRII(b). Lastly, FcgammaRIIa-mediated phagocytosis was significantly enhanced in THP-1 cells overexpressing dominant-negative form of SHIP in the absence of FcgammaRII(b). These results indicate that SHIP negatively regulates FcgammaR-mediated phagocytosis through all ITAM-containing IgG receptors using a molecular mechanism distinct from that in B cells.

[1]  J. Swanson,et al.  A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages , 1996, The Journal of cell biology.

[2]  O. Hazeki,et al.  Involvement of phosphatidylinositol 3-kinase in Fc gamma receptor signaling. , 1994, The Journal of biological chemistry.

[3]  G. Krystal,et al.  Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. , 1998, Genes & development.

[4]  K. Coggeshall Positive and negative signaling in B lymphocytes. , 2000, Current topics in microbiology and immunology.

[5]  D. McVicar,et al.  Paired inhibitory and activating receptor signals. , 2000, Reviews in immunogenetics.

[6]  Min Zhang,et al.  A novel human immunoglobulin Fc gamma Fc epsilon bifunctional fusion protein inhibits Fc epsilon RI-mediated degranulation. , 2002, Nature medicine.

[7]  M. Pradhan,et al.  Activation‐induced bi‐dentate interaction of SHIP and Shc in B lymphocytes , 1997, Journal of cellular biochemistry.

[8]  H. Korn,et al.  Different patterns of calcium signaling triggered through two components of the B lymphocyte antigen receptor. , 1994, The Journal of biological chemistry.

[9]  A. DeFranco,et al.  A Critical Role for Syk in Signal Transduction and Phagocytosis Mediated by Fcγ Receptors on Macrophages , 1997, The Journal of experimental medicine.

[10]  J. Freed,et al.  Differential Regulation of B Cell Development, Activation, and Death by the Src Homology 2 Domain–Containing 5′ Inositol Phosphatase (Ship) , 2000, The Journal of experimental medicine.

[11]  C. Anderson,et al.  Identification of a second class of IgG Fc receptors on human neutrophils. A 40 kilodalton molecule also found on eosinophils , 1986, The Journal of experimental medicine.

[12]  Sinclair Why So Many Coinhibitory Receptors? , 1999, Scandinavian journal of immunology.

[13]  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.

[14]  B. Pyrzyńska,et al.  Syk kinase, tyrosine-phosphorylated proteins and actin filaments accumulate at forming phagosomes during Fcgamma receptor-mediated phagocytosis. , 1997, Cell motility and the cytoskeleton.

[15]  D. Cooney,et al.  The SH2-containing 5'-inositol phosphatase (SHIP) is tyrosine phosphorylated after Fc gamma receptor clustering in monocytes. , 1999, Journal of immunology.

[16]  C. Sautès-Fridman,et al.  Differential Modulation of Stimulatory and Inhibitory Fcγ Receptors on Human Monocytes by Th1 and Th2 Cytokines1 , 2001, The Journal of Immunology.

[17]  K. Coggeshall,et al.  Inhibitory signaling by B cell Fc?RIIb , 1998 .

[18]  W. Fridman,et al.  Regulation of high-affinity IgE receptor-mediated mast cell activation by murine low-affinity IgG receptors. , 1995, The Journal of clinical investigation.

[19]  M. Daëron,et al.  Fc receptor biology. , 2003, Annual review of immunology.

[20]  M. Hughes,et al.  SHIP, a new player in cytokine-induced signalling , 1997, Leukemia.

[21]  J. Unkeless Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors , 1979, The Journal of experimental medicine.

[22]  K. Austen,et al.  Mouse mast cell gp49B1 contains two immunoreceptor tyrosine-based inhibition motifs and suppresses mast cell activation when coligated with the high-affinity Fc receptor for IgE. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  C. Lagenaur,et al.  Negative Regulation of Phagocytosis in Murine Macrophages by the Src Kinase Family Member, Fgr , 2000, The Journal of experimental medicine.

[24]  K. Coggeshall Inhibitory signaling by B cell Fc gamma RIIb. , 1998, Current opinion in immunology.

[25]  Min Zhang,et al.  A novel human immunoglobulin Fcγ–Fcɛ bifunctional fusion protein inhibits FcɛRI-mediated degranulation , 2002, Nature Medicine.

[26]  C. Helgason,et al.  A Regulatory Role for Src Homology 2 Domain–Containing Inositol 5′-Phosphatase (Ship) in Phagocytosis Mediated by Fcγ Receptors and Complement Receptor 3 (αMβ2; Cd11b/Cd18) , 2001, The Journal of experimental medicine.

[27]  T. Kelley,et al.  Recruitment and phosphorylation of SH2-containing inositol phosphatase and Shc to the B-cell Fc gamma immunoreceptor tyrosine-based inhibition motif peptide motif , 1997, Molecular and cellular biology.

[28]  T. Sasaki,et al.  SHIP is a negative regulator of growth factor receptor-mediated PKB/Akt activation and myeloid cell survival. , 1999, Genes & development.

[29]  J. Ravetch,et al.  FcR γ chain deletion results in pleiotrophic effector cell defects , 1994, Cell.

[30]  A. Jacob,et al.  Enzymatic Activity of the Src Homology 2 Domain-containing Inositol Phosphatase Is Regulated by a Plasma Membrane Location* , 2000, The Journal of Biological Chemistry.

[31]  J. Ravetch,et al.  FcR gamma chain deletion results in pleiotrophic effector cell defects. , 1994, Cell.

[32]  T. Kelley,et al.  Role of SHIP in FcgammaRIIb-mediated inhibition of Ras activation in B cells. , 1998, Molecular immunology.

[33]  A. Jacob,et al.  Signal Transduction by Human-Restricted FcγRIIa Involves Three Distinct Cytoplasmic Kinase Families Leading to Phagocytosis1 , 2001, The Journal of Immunology.

[34]  A. DeFranco,et al.  Fcγ Receptor–Mediated Phagocytosis in Macrophages Lacking the Src Family Tyrosine Kinases Hck, Fgr, and Lyn , 2000, The Journal of experimental medicine.

[35]  Taylor Ls,et al.  Paired inhibitory and activating receptor signals. , 2000 .

[36]  H. Korn,et al.  Cross-linking of IgG receptors inhibits membrane immunoglobulin- stimulated calcium influx in B lymphocytes , 1993, The Journal of cell biology.

[37]  G. Krystal,et al.  Negative signaling in B lymphocytes induces tyrosine phosphorylation of the 145-kDa inositol polyphosphate 5-phosphatase, SHIP. , 1996, Journal of immunology.

[38]  K. Ravichandran,et al.  Shc Interaction with Src Homology 2 Domain Containing Inositol Phosphatase (SHIP) in Vivo Requires the Shc-Phosphotyrosine Binding Domain and Two Specific Phosphotyrosines on SHIP* , 1997, The Journal of Biological Chemistry.

[39]  M. Ono,et al.  Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. , 1996, Nature.

[40]  Cameron,et al.  The human high‐affinity immunoglobulin G receptor activates SH2‐containing inositol phosphatase (SHIP) , 1999, Immunology.

[41]  M. Cooper,et al.  The paired Ig-like receptor PIR-B is an inhibitory receptor that recruits the protein-tyrosine phosphatase SHP-1. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Cambier,et al.  Effects of Src Homology Domain 2 (SH2)-Containing Inositol Phosphatase (SHIP), SH2-Containing Phosphotyrosine Phosphatase (SHP)-1, and SHP-2 SH2 Decoy Proteins on FcγRIIB1-Effector Interactions and Inhibitory Functions1 , 2000, The Journal of Immunology.

[43]  M. Osborne,et al.  The Inositol 5′-Phosphatase SHIP Binds to Immunoreceptor Signaling Motifs and Responds to High Affinity IgE Receptor Aggregation* , 1996, The Journal of Biological Chemistry.

[44]  M. Ono,et al.  Modulation of Immune Complex–induced Inflammation In Vivo by the Coordinate Expression of Activation and Inhibitory Fc Receptors , 1999, The Journal of experimental medicine.

[45]  A. Duchemin,et al.  Chimeric Receptors Composed of Phosphoinositide 3-Kinase Domains and Fcγ Receptor Ligand-binding Domains Mediate Phagocytosis in COS Fibroblasts* , 1998, The Journal of Biological Chemistry.

[46]  G. Krystal,et al.  Differential association of phosphatases with hematopoietic co‐receptors bearing immunoreceptor tyrosine‐based inhibition motifs , 1997, European journal of immunology.

[47]  P. Majerus,et al.  The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Pradhan,et al.  Protein interactions of Src homology 2 (SH2) domain-containing inositol phosphatase (SHIP): association with Shc displaces SHIP from FcgammaRIIb in B cells. , 1999, Journal of immunology.

[49]  M. Ono,et al.  Augmented humoral and anaphylactic responses in FcγRII-deficient mice , 1996, Nature.

[50]  K. Coggeshall,et al.  Phosphoinositide 3-Kinase and p72 Noncovalently Associate with the Low Affinity Fc Receptor on Human Platelets through an Immunoreceptor Tyrosine-based Activation Motif , 1996, The Journal of Biological Chemistry.

[51]  J. Cheung,et al.  Calcium transients during Fc receptor-mediated and nonspecific phagocytosis by murine peritoneal macrophages , 1991, The Journal of cell biology.

[52]  B. Avalos,et al.  Phosphatidylinositol 3'-kinase and SH2-containing inositol phosphatase (SHIP) are recruited by distinct positive and negative growth-regulatory domains in the granulocyte colony-stimulating factor receptor. , 1998, Journal of immunology.

[53]  K. Coggeshall,et al.  Visualization of Negative Signaling in B Cells by Quantitative Confocal Microscopy , 2001, Molecular and Cellular Biology.