Decoupling the Functional Pleiotropy of Stem Cell Factor by Tuning c-Kit Signaling

Akahoshi, 2011, Mast cell chymase reduces the toxicity of Gila monster venom, scorpion venom, and vasoactive intestinal polypeptide in mice, J. Clin. Invest., 121, 4180, 10.1172/JCI46139 Atanasova, 2012, Understanding cytokine and growth factor receptor activation mechanisms, Crit. Rev. Biochem. Mol. Biol., 47, 502, 10.3109/10409238.2012.729561 Baldo, 2014, Side effects of cytokines approved for therapy, Drug Saf., 37, 921, 10.1007/s40264-014-0226-z Bendall, 2014, G-CSF: From granulopoietic stimulant to bone marrow stem cell mobilizing agent, Cytokine Growth Factor Rev., 25, 355, 10.1016/j.cytogfr.2014.07.011 Birnbaum, 2014, Deconstructing the peptide-MHC specificity of T cell recognition, Cell, 157, 1073, 10.1016/j.cell.2014.03.047 Blechman, 1995, The fourth immunoglobulin domain of the stem cell factor receptor couples ligand binding to signal transduction, Cell, 80, 103, 10.1016/0092-8674(95)90455-7 Boder, 1997, Yeast surface display for screening combinatorial polypeptide libraries, Nat. Biotechnol., 15, 553, 10.1038/nbt0697-553 Briddell, 1993, Recombinant rat stem cell factor synergizes with recombinant human granulocyte colony-stimulating factor in vivo in mice to mobilize peripheral blood progenitor cells that have enhanced repopulating potential, Blood, 82, 1720, 10.1182/blood.V82.6.1720.1720 Costa, 1996, Recombinant human stem cell factor (kit ligand) promotes human mast cell and melanocyte hyperplasia and functional activation in vivo, J. Exp. Med., 183, 2681, 10.1084/jem.183.6.2681 da Silva, 2004, Ancestim (recombinant human stem cell factor, SCF) in association with filgrastim does not enhance chemotherapy and/or growth factor-induced peripheral blood progenitor cell (PBPC) mobilization in patients with a prior insufficient PBPC collection, Bone Marrow Transplant., 34, 683, 10.1038/sj.bmt.1704602 Ding, 2012, Endothelial and perivascular cells maintain haematopoietic stem cells, Nature, 481, 457, 10.1038/nature10783 Floros, 2015, Anticancer cytokines: biology and clinical effects of interferon-α2, interleukin (IL)-2, IL-15, IL-21, and IL-12, Semin. Oncol., 42, 539, 10.1053/j.seminoncol.2015.05.015 Gagari, 1997, Differential release of mast cell interleukin-6 via c-kit, Blood, 89, 2654, 10.1182/blood.V89.8.2654 Galli, 1993, Reversible expansion of primate mast cell populations in vivo by stem cell factor, J. Clin. Invest., 91, 148, 10.1172/JCI116164 Gardner, 1998, Stem cell factor improves the repopulating ability of primitive hematopoietic stem cells after sublethal irradiation (and, to a lesser extent) after bone marrow transplantation in mice, Stem Cells, 16, 112, 10.1002/stem.160112 Gaudenzio, 2015, Analyzing the functions of Mast cells in vivo using ‘Mast cell knock-in’ mice, J. Vis. Exp., e52753 Gaudenzio, 2016, Different activation signals induce distinct mast cell degranulation strategies, J. Clin. Invest., 126, 3981, 10.1172/JCI85538 Gilfillan, 2009, Amplification mechanisms for the enhancement of antigen-mediated mast cell activation, Immunol. Res., 43, 15, 10.1007/s12026-008-8046-9 Gudkov, 2003, The role of p53 in determining sensitivity to radiotherapy, Nat. Rev. Cancer, 3, 117, 10.1038/nrc992 Hart, 2014, Paradoxical signaling by a secreted molecule leads to homeostasis of cell levels, Cell, 158, 1022, 10.1016/j.cell.2014.07.033 Hill, 1996, Stem cell factor enhances immunoglobulin E-dependent mediator release from cultured rat bone marrow-derived mast cells: activation of previously unresponsive cells demonstrated by a novel ELISPOT assay, Immunology, 87, 326, 10.1046/j.1365-2567.1996.455545.x Hsu, 1997, The majority of stem cell factor exists as monomer under physiological conditions. Implications for dimerization mediating biological activity, J. Biol. Chem., 272, 6406, 10.1074/jbc.272.10.6406 Jaqaman, 2008, Robust single-particle tracking in live-cell time-lapse sequences, Nat. Methods, 5, 695, 10.1038/nmeth.1237 Jiang, 2000, Structure of the active core of human stem cell factor and analysis of binding to its receptor kit, EMBO J., 19, 3192, 10.1093/emboj/19.13.3192 Kalesnikoff, 2011, Antiinflammatory and immunosuppressive functions of mast cells, Methods Mol. Biol., 677, 207, 10.1007/978-1-60761-869-0_15 Kirchhofer, 2010, Modulation of protein properties in living cells using nanobodies, Nat. Struct. Mol. Biol., 17, 133, 10.1038/nsmb.1727 Klemm, 1998, Dimerization as a regulatory mechanism in signal transduction, Annu. Rev. Immunol., 16, 569, 10.1146/annurev.immunol.16.1.569 Krieg, 2010, Improved IL-2 immunotherapy by selective stimulation of IL-2 receptors on lymphocytes and endothelial cells, Proc. Natl. Acad. Sci. USA, 107, 11906, 10.1073/pnas.1002569107 Krutzik, 2003, Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events, Cytometry A, 55, 61, 10.1002/cyto.a.10072 Leibowitz, 2014, Ionizing irradiation induces acute haematopoietic syndrome and gastrointestinal syndrome independently in mice, Nat. Commun., 5, 3494, 10.1038/ncomms4494 Leigh, 1995, Stem cell factor enhances the survival of murine intestinal stem cells after photon irradiation, Radiat. Res., 142, 12, 10.2307/3578961 Levin, 2014, Multifaceted activities of type I interferon are revealed by a receptor antagonist, Sci. Signal., 7, ra50, 10.1126/scisignal.2004998 Li, 1994, Stem cell factor enhances the survival but not the self-renewal of murine hematopoietic long-term repopulating cells, Blood, 84, 408, 10.1182/blood.V84.2.408.408 Lilla, 2011, Reduced mast cell and basophil numbers and function in Cpa3-Cre; Mcl-1fl/fl mice, Blood, 118, 6930, 10.1182/blood-2011-03-343962 Lin, 1995, The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15, Immunity, 2, 331, 10.1016/1074-7613(95)90141-8 Liu, 2007, Structural basis for stem cell factor-KIT signaling and activation of class III receptor tyrosine kinases, EMBO J., 26, 891, 10.1038/sj.emboj.7601545 Macdonald-Obermann, 2014, Different epidermal growth factor (EGF) receptor ligands show distinct kinetics and biased or partial agonism for homodimer and heterodimer formation, J. Biol. Chem., 289, 26178, 10.1074/jbc.M114.586826 Mitra, 2015, Interleukin-2 activity can be fine tuned with engineered receptor signaling clamps, Immunity, 42, 826, 10.1016/j.immuni.2015.04.018 Molineux, 1991, The effects on hematopoiesis of recombinant stem cell factor (ligand for c-kit) administered in vivo to mice either alone or in combination with granulocyte colony-stimulating factor, Blood, 78, 961, 10.1182/blood.V78.4.961.961 Moraga, 2014, Multifarious determinants of cytokine receptor signaling specificity, Adv. Immunol., 121, 1, 10.1016/B978-0-12-800100-4.00001-5 Moraga, 2015, Instructive roles for cytokine-receptor binding parameters in determining signaling and functional potency, Sci. Signal., 8, ra114, 10.1126/scisignal.aab2677 Moraga, 2015, Tuning cytokine receptor signaling by re-orienting dimer geometry with surrogate ligands, Cell, 160, 1196, 10.1016/j.cell.2015.02.011 Moskowitz, 1997, Recombinant methionyl human stem cell factor and filgrastim for peripheral blood progenitor cell mobilization and transplantation in non-Hodgkin’s lymphoma patients--results of a phase I/II trial, Blood, 89, 3136, 10.1182/blood.V89.9.3136 Nepom, 2013, Anti-cytokine therapies in T1D: Concepts and strategies, Clin. Immunol., 149, 279, 10.1016/j.clim.2013.02.003 Nicola, 1994, Cytokine pleiotropy and redundancy: a view from the receptor, Stem Cells, 12, 3 Reshetnyak, 2015, The strength and cooperativity of KIT ectodomain contacts determine normal ligand-dependent stimulation or oncogenic activation in cancer, Mol. Cell, 57, 191, 10.1016/j.molcel.2014.11.021 Riese, 2011, Ligand-based receptor tyrosine kinase partial agonists: new paradigm for cancer drug discovery?, Expert Opin. Drug Discov., 6, 185, 10.1517/17460441.2011.547468 Roder, 2014, Rapid transfer of transmembrane proteins for single molecule dimerization assays in polymer-supported membranes, ACS Chem. Biol., 9, 2479, 10.1021/cb5005806 Rönnstrand, 2004, Signal transduction via the stem cell factor receptor/c-Kit, Cell. Mol. Life Sci., 61, 2535, 10.1007/s00018-004-4189-6 Schlessinger, 1992, Growth factor signaling by receptor tyrosine kinases, Neuron, 9, 383, 10.1016/0896-6273(92)90177-F Sergé, 2008, Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes, Nat. Methods, 5, 687, 10.1038/nmeth.1233 Stroud, 2004, Mechanistic diversity of cytokine receptor signaling across cell membranes, Sci. STKE, 2004, re7, 10.1126/stke.2312004re7 Taketomi, 2007, Impaired mast cell maturation and degranulation and attenuated allergic responses in Ndrg1-deficient mice, J. Immunol., 178, 7042, 10.4049/jimmunol.178.11.7042 Taylor, 1995, Stem-cell factor, the kit ligand, induces direct degranulation of rat peritoneal mast cells in vitro and in vivo: dependence of the in vitro effect on period of culture and comparisons of stem-cell factor with other mast cell-activating agents, Immunology, 86, 427 Thomas, 2004, Regulation of haematopoiesis by growth factors - emerging insights and therapies, Expert Opin. Biol. Ther., 4, 869, 10.1517/14712598.4.6.869 Tong, 1993, In vivo administration of recombinant methionyl human stem cell factor expands the number of human marrow hematopoietic stem cells, Blood, 82, 784, 10.1182/blood.V82.3.784.784 Vogelsang, 2008, A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes, Angew. Chem. Int. Ed. Engl., 47, 5465, 10.1002/anie.200801518 Wada, 2010, Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks, J. Clin. Invest., 120, 2867, 10.1172/JCI42680 Wang, 2009, Structural biology of shared cytokine receptors, Annu. Rev. Immunol., 27, 29, 10.1146/annurev.immunol.24.021605.090616 Weiskopf, 2013, Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies, Science, 341, 88, 10.1126/science.1238856 Williams, 1992, Recombinant murine steel factor stimulates in vitro production of granulocyte-macrophage progenitor cells, J. Cell. Biochem., 50, 221, 10.1002/jcb.240500302 Wilmes, 2015, Receptor dimerization dynamics as a regulatory valve for plasticity of type I interferon signaling, J. Cell Biol., 209, 579, 10.1083/jcb.201412049 Yea, 2015, Selection of multiple agonist antibodies from intracellular combinatorial libraries reveals that cellular receptors are functionally pleiotropic, Curr. Opin. Chem. Biol., 26, 1, 10.1016/j.cbpa.2015.01.002 Yee, 1994, Mechanism of down-regulation of c-kit receptor. Roles of receptor tyrosine kinase, phosphatidylinositol 3′-kinase, and protein kinase C, J. Biol. Chem., 269, 31991, 10.1016/S0021-9258(18)31793-9 You, 2014, Dynamic submicroscopic signaling zones revealed by pair correlation tracking and localization microscopy, Anal. Chem., 86, 8593, 10.1021/ac501127r Yuzawa, 2007, Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor, Cell, 130, 323, 10.1016/j.cell.2007.05.055 Zhang, 2000, Crystal structure of human stem cell factor: implication for stem cell factor receptor dimerization and activation, Proc. Natl. Acad. Sci. USA, 97, 7732, 10.1073/pnas.97.14.7732 Zsebo, 1992, Radioprotection of mice by recombinant rat stem cell factor, Proc. Natl. Acad. Sci. USA, 89, 9464, 10.1073/pnas.89.20.9464