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Science 293 (5528): 306-311

Copyright © 2001 by the American Association for the Advancement of Science

Homeostatic Regulation of the Immune System by Receptor Tyrosine Kinases of the Tyro 3 Family

Qingxian Lu, Greg Lemke*

Receptor tyrosine kinases and their ligands mediate cell-cell communication and interaction in many organ systems, but have not been known to act in this capacity in the mature immune system. We now provide genetic evidence that three closely related receptor tyrosine kinases, Tyro 3, Axl, and Mer, play an essential immunoregulatory role. Mutant mice that lack these receptors develop a severe lymphoproliferative disorder accompanied by broad-spectrum autoimmunity. These phenotypes are cell nonautonomous with respect to lymphocytes and result from the hyperactivation of antigen-presenting cells in which the three receptors are normally expressed.

Molecular Neurobiology Laboratory, The Salk Institute, La Jolla, CA 92037, USA.
*   To whom correspondence should be addressed. E-mail: lemke{at}

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The scavenger receptor SR-A I/II (CD204) signals via the receptor tyrosine kinase Mertk during apoptotic cell uptake by murine macrophages.
J. C. Todt, B. Hu, and J. L. Curtis (2008)
J. Leukoc. Biol. 84, 510-518
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Defective Mer Receptor Tyrosine Kinase Signaling in Bone Marrow Cells Promotes Apoptotic Cell Accumulation and Accelerates Atherosclerosis.
H. Ait-Oufella, V. Pouresmail, T. Simon, O. Blanc-Brude, K. Kinugawa, R. Merval, G. Offenstadt, G. Leseche, P. L. Cohen, A. Tedgui, et al. (2008)
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Gas6 Deficiency Increases Oligodendrocyte Loss and Microglial Activation in Response to Cuprizone-Induced Demyelination.
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J. Neurosci. 28, 5195-5206
   Abstract »    Full Text »    PDF »
Gas6 promotes inflammation by enhancing interactions between endothelial cells, platelets, and leukocytes.
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   Abstract »    Full Text »    PDF »
Autophosphorylation Docking Site Tyr-867 in Mer Receptor Tyrosine Kinase Allows for Dissociation of Multiple Signaling Pathways for Phagocytosis of Apoptotic Cells and Down-modulation of Lipopolysaccharide-inducible NF-{kappa}B Transcriptional Activation.
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MerTK is required for apoptotic cell-induced T cell tolerance.
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J. Exp. Med. 205, 219-232
   Abstract »    Full Text »    PDF »
Gas6 and the Tyro 3 receptor tyrosine kinase subfamily regulate the phagocytic function of Sertoli cells.
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Reproduction 135, 77-87
   Abstract »    Full Text »    PDF »
Axl Mediates Vascular Remodeling Induced by Deoxycorticosterone Acetate Salt Hypertension.
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Hypertension 50, 1057-1062
   Abstract »    Full Text »    PDF »
The role of Tyro 3 subfamily receptors in the regulation of hemostasis and megakaryocytopoiesis.
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Haematologica 92, 643-650
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Macrophages and Dendritic Cells Use Different Axl/Mertk/Tyro3 Receptors in Clearance of Apoptotic Cells.
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J. Immunol. 178, 5635-5642
   Abstract »    Full Text »    PDF »
Apoptotic cells induce Mer tyrosine kinase-dependent blockade of NF-{kappa}B activation in dendritic cells.
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Blood 109, 653-660
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Tyro3 Family-Mediated Cell Entry of Ebola and Marburg Viruses.
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J. Virol. 80, 10109-10116
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Twist mediates suppression of inflammation by type I IFNs and Axl.
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J. Exp. Med. 203, 1891-1901
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Axl, A Receptor Tyrosine Kinase, Mediates Flow-Induced Vascular Remodeling.
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   Abstract »    Full Text »    PDF »
Gas6/Axl Signaling Activates the Phosphatidylinositol 3-Kinase/Akt1 Survival Pathway to Protect Oligodendrocytes from Tumor Necrosis Factor{alpha}-Induced Apoptosis.
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J. Neurosci. 26, 5638-5648
   Abstract »    Full Text »    PDF »
Structural basis for Gas6-Axl signalling.
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EMBO J. 25, 80-87
   Abstract »    Full Text »    PDF »
Heterogeneous Nuclear Ribonucleoprotein P2 Is an Autoantibody Target in Mice Deficient for Mer, Axl, and Tyro3 Receptor Tyrosine Kinases.
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J. Immunol. 176, 68-74
   Abstract »    Full Text »    PDF »
A promiscuous liaison between IL-15 receptor and Axl receptor tyrosine kinase in cell death control.
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   Abstract »    Full Text »    PDF »
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Inhibition of vascular endothelial growth factor receptor 2-mediated endothelial cell activation by Axl tyrosine kinase receptor.
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Blood 105, 1970-1976
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Imatinib mesylate (STI-571) enhances antigen-presenting cell function and overcomes tumor-induced CD4+ T-cell tolerance.
H. Wang, F. Cheng, A. Cuenca, P. Horna, Z. Zheng, K. Bhalla, and E. M. Sotomayor (2005)
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Signal Pathways in Up-regulation of Chemokines by Tyrosine Kinase MER/NYK in Prostate Cancer Cells.
Y.-M. Wu, D. R. Robinson, and H.-J. Kung (2004)
Cancer Res. 64, 7311-7320
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Hydrogen Peroxide Activates the Gas6-Axl Pathway in Vascular Smooth Muscle Cells.
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Nucleosomes Are Exposed at the Cell Surface in Apoptosis.
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Receptor tyrosine kinases and the regulation of macrophage activation.
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J. Leukoc. Biol. 75, 731-737
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The receptor tyrosine kinase MerTK activates phospholipase C {gamma}2 during recognition of apoptotic thymocytes by murine macrophages.
J. C. Todt, B. Hu, and J. L. Curtis (2004)
J. Leukoc. Biol. 75, 705-713
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Ligand Recognition and Homophilic Interactions in Tyro3: STRUCTURAL INSIGHTS INTO THE Axl/Tyro3 RECEPTOR TYROSINE KINASE FAMILY.
C. Heiring, B. Dahlback, and Y. A. Muller (2004)
J. Biol. Chem. 279, 6952-6958
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Macrophage-Stimulating Protein, the Ligand for the Stem Cell-Derived Tyrosine Kinase/RON Receptor Tyrosine Kinase, Inhibits IL-12 Production by Primary Peritoneal Macrophages Stimulated with IFN-{gamma} and Lipopolysaccharide.
A. C. Morrison, C. B. Wilson, M. Ray, and P. H. Correll (2004)
J. Immunol. 172, 1825-1832
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Impaired Clearance of Apoptotic Cells Induces the Activation of Autoreactive Anti-Sm Marginal Zone and B-1 B Cells.
Y. Qian, H. Wang, and S. H. Clarke (2004)
J. Immunol. 172, 625-635
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Molecular Basis of Constitutive Production of Basement Membrane Components: GENE EXPRESSION PROFILES OF ENGELBRETH-HOLM-SWARM TUMOR AND F9 EMBRYONAL CARCINOMA CELLS.
S. Futaki, Y. Hayashi, M. Yamashita, K. Yagi, H. Bono, Y. Hayashizaki, Y. Okazaki, and K. Sekiguchi (2003)
J. Biol. Chem. 278, 50691-50701
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An SH2 Domain-dependent, Phosphotyrosine-independent Interaction between Vav1 and the Mer Receptor Tyrosine Kinase: A MECHANISM FOR LOCALIZING GUANINE NUCLEOTIDE-EXCHANGE FACTOR ACTION.
N. P. Mahajan and H. S. Earp (2003)
J. Biol. Chem. 278, 42596-42603
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Control of myeloid activity during retinal inflammation.
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J. Leukoc. Biol. 74, 161-166
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Crystal Structure of a C-terminal Fragment of Growth Arrest-specific Protein Gas6. RECEPTOR TYROSINE KINASE ACTIVATION BY LAMININ G-LIKE DOMAINS.
T. Sasaki, P. G. Knyazev, Y. Cheburkin, W. Gohring, D. Tisi, A. Ullrich, R. Timpl, and E. Hohenester (2002)
J. Biol. Chem. 277, 44164-44170
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Delayed Apoptotic Cell Clearance and Lupus-like Autoimmunity in Mice Lacking the c-mer Membrane Tyrosine Kinase.
P. L. Cohen, R. Caricchio, V. Abraham, T. D. Camenisch, J. C. Jennette, R. A.S. Roubey, H. S. Earp, G. Matsushima, and E. A. Reap (2002)
J. Exp. Med. 196, 135-140
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B. A. Cocca, A. M. Cline, and M. Z. Radic (2002)
J. Immunol. 169, 159-166
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K. L. Guttridge, J. C. Luft, T. L. Dawson, E. Kozlowska, N. P. Mahajan, B. Varnum, and H. S. Earp (2002)
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IMMUNOLOGY: Tampering with the Immune System.
P. L. Schwartzberg (2001)
Science 293, 228-229
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