CSF-1 receptor signaling in myeloid cells

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 6, 2014, Pages

  Stanley, E Richard ^a   Chitu, Violeta ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR RECEPTOR; LIGAND;

ANIMAL; BONE MARROW CELL; CHEMISTRY; CYTOLOGY; GENETICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

ANIMALS; EVOLUTION, MOLECULAR; HUMANS; LIGANDS; MYELOID CELLS; PROTEIN CONFORMATION; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SIGNAL TRANSDUCTION;

EID: 84903708438     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a021857     Document Type: Review

References (207)

1. Abou-Kheir W, Isaac B, Yamaguchi H, Cox D. 2008. Membrane targeting of WAVE2 is not sufficient for WAVE2- dependent actin polymerization: A role for IRSp53 in mediating the interaction between Rac and WAVE2. J Cell Sci 121: 379-390.
2. Allen WE, Zicha D, Ridley AJ, Jones GE. 1998. A role for Cdc42 in macrophage chemotaxis. J Cell Biol 141: 1147-1157.
3. Baccarini M, Li W, Dello Sbarba P, Stanley ER. 1991. Increased phosphorylation of the colony stimulating factor- 1 receptor following transmembrane signaling. Receptor 1: 243-259.
4. Baran CP, Tridandapani S, Helgason CD, Humphries RK, Krystal G, Marsh CB. 2003. The inositol 50-phosphatase SHIP-1 and the Src kinase Lyn negatively regulate macrophage colony-stimulating factor-induced Akt activity. J Biol Chem 278: 38628-38636.
5. Bartelmez SH, Stanley ER. 1985. Synergism between hemopoietic growth factors (HGFs) detected by their effects on cells bearing receptors for a lineage specific HGF: Assay of hemopoietin-1. J Cell Physiol 122: 370-378.
6. Bartelmez SH, Bradley TR, Bertoncello I, Mochizuki DY, Tushinski RJ, Stanley ER, Hapel AJ, Young IG, Kriegler AB, Hodgson GS. 1989. Interleukin 1 plus interleukin 3 plus colony-stimulating factor 1 are essential for clonal proliferation of primitive myeloid bone marrowcells. Exp Hematol 17: 240-245.
7. Bhavsar PJ, Vigorito E, Turner M, Ridley AJ. 2009. Vav GEFs regulatemacrophage morphologyand adhesion-induced Rac and Rho activation. Exp Cell Res 315: 3345-3358.
8. Bonifer C, Hume DA. 2008. The transcriptional regulation of the colony-stimulating factor 1 receptor (csf1r) gene during hematopoiesis. Front Biosci 13: 549-560.
9. Boocock CA, Jones GE, Stanley ER, Pollard JW. 1989. Colony- stimulating factor-1 induces rapid behavioural re-sponses in the mouse macrophage cell line, BAC1.2F5. J Cell Sci 93: 447-456.
10. Bourette RP, Myles GM, Carlberg K, Chen AR, Rohrschneider LR. 1995. Uncoupling of the proliferation and differentiation signals mediated by the murine macrophage colony-stimulating factor receptor expressed in myeloid FDC-P1 cells. Cell Growth Differ 6: 631-645.
11. Bourette RP, Myles GM, Choi JL, Rohrschneider LR. 1997. Sequential activation of phosphatidylinositol 3-kinase and phospholipase C-g2 by the M-CSF receptor is necessary for differentiation signaling. EMBO J 16: 5880-5893.
12. Bourette RP, De Sepulveda P, Arnaud S, Dubreuil P, Rottapel R, Mouchiroud G. 2001. Suppressor of cytokine signaling 1 interacts with the macrophage colony-stimulating factor receptor and negatively regulates its proliferation signal. J Biol Chem 276: 22133-22139.
13. Bourette RP, Therier J, Mouchiroud G. 2005. Macrophage colony-stimulating factor receptor induces tyrosine phosphorylation of SKAP55R adaptor and its association with actin. Cell Signal 17: 941-949.
14. Bourgin C, Bourette R, Mouchiroud G, Arnaud S. 2000. Expression of Mona (monocytic adapter) in myeloid progenitor cells results in increased and prolonged MAP kinase activation upon macrophage colony-stimulating factor stimulation. FEBS Lett 480: 113-117.
15. Bourgin C, Bourette RP, Arnaud S, Liu Y, Rohrschneider LR, Mouchiroud G. 2002. Induced expression and association of the Mona/Gads adapter and Gab3 scaffolding protein during monocyte/macrophage differentiation. Mol Cell Biol 22: 3744-3756.
16. Braasch I, Salzburger W, Meyer A. 2006. Asymmetric evolution in two fish-specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. Mol Biol Evol 23: 1192-1202.
17. Byrne PV, Guilbert LJ, Stanley ER. 1981. Distribution of cells bearing receptors for a colony-stimulating factor (CSF) in murine tissues. J Cell Biol 91: 848-853.
18. Cammer M, Gevrey JC, Lorenz M, Dovas A, Condeelis J, Cox D. 2009. The mechanism of CSF-1-induced Wiskott-Aldrich syndrome protein activation in vivo: A role for phosphatidylinositol 3-kinase and Cdc42. J Biol Chem 284: 23302-23311.
19. Carlberg K, Rohrschneider LR. 1994. The effect of activating mutations on dimerization, tyrosine phosphorylation and internalization of the macrophage colony stimulating factor receptor. Mol Cell Biol 5: 81-95.
20. Cecchini MG, Dominguez MG, Mocci S, Wetterwald A, Felix R, Fleisch H, Chisholm O, Hofstetter W, Pollard JW, Stanley ER. 1994. Role of colony stimulating factor- 1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120: 1357-1372.
21. Chang M, Hamilton JA, Scholz GM, Masendycz P, Macaulay SL, Elsegood CL. 2009. Phosphatidylinostitol-3 kinase and phospholipase C enhance CSF-1-dependent macrophage survival by controlling glucose uptake. Cell Signal 21: 1361-1369.
22. Chen X, Liu H, Focia PJ, Shim AH, He X. 2008. Structure of macrophage colony stimulating factor bound to FMS: Diverse signaling assemblies of class III receptor tyrosine kinases. Proc Natl Acad Sci 105: 18267-18272.
23. Chihara T, Suzu S, Hassan R, Chutiwitoonchai N, Hiyoshi M, Motoyoshi K, Kimura F, Okada S. 2010. IL-34 and MCSF share the receptor Fms but are not identical in biological activity and signal activation. Cell Death Differ 17: 1917-1927.
24. Chitu V, Stanley ER. 2006. Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol 18: 39-48.
25. Chitu V, Stanley ER. 2007. Pombe Cdc15 homology (PCH) proteins: Coordinators of membrane-cytoskeletal interactions. Trends Cell Biol 17: 145-156.
26. Chitu V, Stanley ER. 2009. PSTPIP1 and PSTPIP2/MAYP. InThePombeCdc15 homology proteins (ed.AspenstromP), pp. 49-61. Landes Bioscience, Austin, Texas.
27. Chitu V, Stanley ER. 2014. CSF-1 receptor. In The receptor tyrosine kinase handbook (ed. Wheeler DL, Yarden Y). Springer, New York (in press).
28. Chitu V, Pixley FJ, Macaluso F, Larson DR, Condeelis J, Yeung YG, Stanley ER. 2005. The PCH family member MAYP/PSTPIP2 directly regulates F-actin bundling and enhances filopodia formation and motility in macrophages. Mol Biol Cell 16: 2947-2959.
29. Chitu V, Ferguson PJ, de Bruijn R, Schlueter AJ, Ochoa LA, Waldschmidt TJ, Yeung YG, Stanley ER. 2009. Primed innate immunity leads to autoinflammatory disease in PSTPIP2-deficient cmo mice. Blood 114: 2497-2505.
30. Chitu V, Nacu V, Charles JF, Henne WM, McMahon HT, Nandi S, Ketchum H, Harris R, Nakamura MC, Stanley ER. 2012. PSTPIP2 deficiency in mice causes osteopenia and increased differentiation of multipotentmyeloid precursors into osteoclasts. Blood 120: 3126-3135.
31. Cote JF, Chung PL, Theberge JF, Halle M, Spencer S, Lasky LA, Tremblay ML. 2002. PSTPIP is a substrate of PTPPESTand serves as a scaffold guiding PTP-PEST toward a specific dephosphorylation of WASP. J Biol Chem 277: 2973-2986.
32. Coussens L, Van Beveren C, Smith D, Chen E, Mitchell RL, Isacke CM, Verma IM, Ullrich A. 1986. Structural alteration of viral homologue of receptor proto-oncogene fms at carboxy-terminus. Nature 32: 277-280.
33. Csar XF, Wilson NJ, McMahon KA, Marks DC, Beecroft TL, Ward AC, Whitty GA, Kanangasundarum V, Hamilton JA. 2001. Proteomic analysis of macrophage differentiation. p46/52(Shc) Tyrosine phosphorylation is required for CSF-1-mediated macrophage differentiation. J Biol Chem 276: 26211-26217.
34. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER. 2002. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99: 111-120.
35. Dai XM, Zong XH, Sylvestre V, Stanley ER. 2004. Incomplete restoration of colony-stimulating factor 1 (CSF-1) function in CSF-1-deficient Csf1op/Csf1op mice by transgenic expression of cell surface CSF-1. Blood 103: 1114-1123.
36. Dauffy J, Mouchiroud G, Bourette RP. 2006. The interferoninducible gene, Ifi204, is transcriptionally activated in response to M-CSF, and its expression favors macrophage differentiation in myeloid progenitor cells. J Leukoc Biol 79: 173-183.
37. DiNitto JP, Deshmukh GD, Zhang Y, Jacques SL, Coli R, Worrall JW, Diehl W, English JM, Wu JC. 2010. Function of activation loop tyrosine phosphorylation in the mechanism of c-Kit auto-activation and its implication in sunitinib resistance. J Biochem 147: 601-609.
38. Dovas A, Gevrey JC, Grossi A, Park H, Abou-Kheir W, Cox D. 2009. Regulation of podosome dynamics by WASp phosphorylation: Implication in matrix degradation and chemotaxis in macrophages. J Cell Sci 122: 3872-3882.
39. Elegheert J, Desfosses A, Shkumatov AV, Wu X, Bracke N, Verstraete K, Van Craenenbroeck K, Brooks BR, Svergun DI, Vergauwen B, et al. 2011. Extracellular complexes of the hematopoietic human and mouse CSF-1 receptor are driven by common assembly principles. Structure 19: 1762-1772.
40. Elegheert J, Bracke N, Pouliot P, Gutsche I, Shkumatov AV, Tarbouriech N, Verstraete K, Bekaert A, Burmeister WP, Svergun DI, et al. 2012. Allosteric competitive inactivation of hematopoietic CSF-1 signaling by the viral decoy receptor BARF1. Nat Struct Mol Biol 19: 938-947.
41. Faccio R, Takeshita S, Colaianni G, Chappel J, Zallone A, Teitelbaum SL, Ross FP. 2007. M-CSF regulates the cytoskeleton via recruitment of a multimeric signaling complex to c-Fms Tyr-559/697/721. J Biol Chem 282: 18991-18999.
42. Felix J, Elegheert J, Gutsche I, Shkumatov AV, Wen YR, Bracke N, Pannecoucke E, Vandenberghe I, Devreese B, Svergun DI, et al. 2013.Human IL-34 and CSF-1 establish structurally similar extracellular assemblies with their common hematopoietic receptor. Structure 21: 528-539.
43. Fleetwood AJ, Lawrence T, Hamilton JA, Cook AD. 2007. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: Implications for CSF blockade in inflammation. J Immunol 178: 5245-5252.
44. Foucher ED, Blanchard S, Preisser L, Garo E, Ifrah N, Guardiola P, Delneste Y, Jeannin P. 2013. IL-34 induces the differentiation of human monocytes into immunosuppressive macrophages. Antagonistic effects of GM-CSF and IFNg. PLoS ONE 8: e56045.
45. Gangoiti P, Granado MH, Wang SW, Kong JY, Steinbrecher UP, Gómez-Muñoz A. 2008.Ceramide 1-phosphate stimulates macrophage proliferation through activation of the PI3-kinase/PKB, JNK and ERK1/2 pathways. Cell Signal 20: 726-736.
46. Gobert Gosse S, Bourgin C, Liu WQ, Garbay C, Mouchiroud G. 2005. M-CSF stimulated differentiation requires persistent MEK activity and MAPK phosphorylation independent of Grb2-Sos association and phosphatidylinositol 3-kinase activity. Cell Signal 17: 1352-1362.
47. Golden LH, Insogna KL. 2004. The expanding role of PI3- kinase in bone. Bone 34: 3-12.
48. Gómez-Muñoz A, Kong JY, Salh B, Steinbrecher UP. 2004. Ceramide-1-phosphate blocks apoptosis through inhibition of acid sphingomyelinase in macrophages. J Lipid Res 45: 99-105.
49. Gómez-Muñ oz A, Kong JY, Parhar K, Wang SW, Gangoiti P, González M, Eivemark S, Salh B, Duronio V, Steinbrecher UP. 2005. Ceramide-1-phosphate promotes cell survival through activation of the phosphatidylinositol 3-kinase/ protein kinase B pathway. FEBS Lett 579: 3744-3750.
50. Gómez-Muñ oz A, Gangoiti P, Granado MH, Arana L, Ouro A. 2010. Ceramide-1-phosphate in cell survival and inflammatory signaling. Adv Exp Med Biol 688: 118-130.
51. Grasset MF, Gobert-Gosse S, Mouchiroud G, Bourette RP. 2010. Macrophage differentiation of myeloid progenitor cells in response to M-CSF is regulated by the dual-specificity phosphatase DUSP5. J Leukoc 87: 127-135.
52. Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, Leboeuf M, Kundig TM, Frei K, Ginhoux F, Merad M, et al. 2012. Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity 37: 1050-1060.
53. Gu J, Gu X. 2003. Natural history and functional divergence of protein tyrosine kinases. Gene 317: 49-57.
54. Gueller S, Goodridge HS, Niebuhr B, Xing H, Koren-Michowitz M, Serve H, Underhill DM, Brandts CH, Koeffler HP. 2010. Adaptor protein Lnk inhibits c-Fms-mediated macrophage function. J Leukoc Biol 88: 699-706.
55. Guery L, Benikhlef N, Gautier T, Paul C, Jego G, Dufour E, Jacquel A, Cally R, Manoury B, Vanden Berghe T, et al. 2011. Fine-tuning nucleophosmin in macrophage differentiation and activation. Blood 118: 4694-4704.
56. Guilbert LJ, Stanley ER. 1980. Specific interaction of murine colony-stimulating factor with mononuclear phagocytic cells. J Cell Biol 85: 153-159.
57. Guilbert LJ, Stanley ER. 1986. The interaction of 125I-colony stimulating factor-1 with bone marrow-derived macrophages. J Biol Chem 261: 4024-4032.
58. Guilbert LJ, Tynan PW, Stanley ER. 1986. Uptake and destruction of 125I-CSF-1 by peritoneal exudate macrophages. J Cell Biochem 31: 203-216.
59. Hampe A, Shamoon BM, Gobet M, Sherr CJ, Galibert F. 1989. Nucleotide sequence and structural organization of the human FMS proto-oncogene. Oncogene Res 4: 9-17.
60. Hanley PJ, Xu Y, Kronlage M, Grobe K, Schon P, Song J, Sorokin L, Schwab A, Bahler M. 2010. Motorized Rho- GAP myosin IXb (Myo9b) controls cell shape and motility. Proc Natl Acad Sci 107: 12145-12150.
61. Himburg HA, Harris JR, Ito T, Daher P, Russell JL, Quarmyne M, Doan PL, Helms K, Nakamura M, Fixsen E, et al. 2012. Pleiotrophin regulates the retention and self-renewal of hematopoietic stem cells in the bone marrow vascular niche. Cell Rep 2: 964-975.
62. Himes SR, Tagoh H, Goonetilleke N, Sasmono T, Oceandy D, Clark R, Bonifer C, Hume DA. 2001. A highly conserved c-fms gene intronic element controls macrophagespecific and regulated expression. J Leukoc Biol 70: 812-820.
63. Hoggan MD, Halden NF, Buckler CE, Kozak CA. 1988. Genetic mapping of the mouse c-fms proto-oncogene to chromosome 18. J Virol 62: 1055-1056.
64. Husson H, Mograbi B, Schmid-Antomarchi H, Fischer S, Rossi B. 1997. CSF-1 stimulation induces the formation of a multiprotein complex including CSF-1 receptor, c-Cbl, PI 3-kinase, Crk-II and Grb2. Oncogene 14: 2331-2338.
65. Huynh D, Dai XM, Nandi S, Lightowler S, Trivett M, Chan CK, Bertoncello I, Ramsay RG, Stanley ER. 2009. Colony stimulating factor-1 dependence of paneth cell development in the mouse small intestine. Gastroenterology 137: 136-144, 144 e131-e133.
66. Huynh J, Kwa MQ, Cook AD, Hamilton JA, Scholz GM. 2012. CSF-1 receptor signalling from endosomes mediates the sustained activation of Erk1/2 and Akt in macrophages. Cell Signal 24: 1753-1761.
67. Hwang SJ, Choi B, Kang SS, Chang JH, Kim YG, Chung YH, Sohn DH, So MW, Lee CK, Robinson WH, et al. 2012. Interleukin-34 produced by human fibroblast-like synovial cells in rheumatoid arthritis supports osteoclastogenesis. Arthritis Res Ther 14: R14.
68. Ikeda O, Sekine Y, Kakisaka M, Tsuji S, Muromoto R, Ohbayashi N, Oritani K, Yoshimura A, Matsuda T. 2007. STAP-2 regulates c-Fms/M-CSF receptor signaling in murine macrophage Raw 264.7 cells. Biochem Biophys Res Commun 358: 931-937.
69. Ishihara D, Dovas A, Park H, Isaac BM, Cox D. 2012. The chemotactic defect inWiskott-Aldrich syndrome macrophages is due to the reduced persistence of directional protrusions. PLoS ONE 7: e30033.
70. Jacquel A, Benikhlef N, Paggetti J, Lalaoui N, Guery L, Dufour EK, Ciudad M, Racoeur C, Micheau O, Delva L, et al. 2009. Colony-stimulating factor-1-induced oscillations in phosphatidylinositol-3 kinase/AKT are required for caspase activation in monocytes undergoing differentiation into macrophages. Blood 114: 3633-3641.
71. Janowska-Wieczorek A, Belch AR, Jacobs A, Bowen D, Padua RA, Paietta E, Stanley ER. 1991. Increased circulating colony-stimulating factor-1 in patients with preleukemia, leukemia, and lymphoid malignancies. Blood 77: 1796-1803.
72. Jones GE, Allen WE, Ridley AJ. 1998. The Rho GTPases in macrophage motility and chemotaxis. Cell Adhes Commun 6: 237-245.
73. Joos H, Trouliaris S, Helftenbein G, Niemann H, Tamura T. 1996. Tyrosine phosphorylation of the juxtamembrane domain of the v-Fms oncogene product is required for its association with a 55-kDa protein. J Biol Chem 271: 24476-24481.
74. Junttila I, Bourette RP, Rohrschneider LR, Silvennoinen O. 2003. M-CSF induced differentiation of myeloid precursor cells involves activation of PKC-d and expression of Pkare. J Leukoc Biol 73: 281-288.
75. Kanagasundaram V, Jaworowski A, Hamilton JA. 1996. Association between phosphatidylinositol-3 kinase, Cbl and other tyrosine phosphorylated proteins in colonystimulating factor-1- stimulated macrophages. Biochem J 320: 69-77.
76. Kelley TW, Graham MM, Doseff AI, Pomerantz RW, Lau SM, Ostrowski MC, Franke TF, Marsh CB. 1999. Macrophage colony-stimulating factor promotes cell survival through Akt/protein kinase B. J Biol Chem 274: 26393-26398.
77. Kheir WA, Gevrey JC, Yamaguchi H, Isaac B, Cox D. 2005. A WAVE2-Abi1 complex mediates CSF-1-induced F-actinrich membrane protrusions and migration in macrophages. J Cell Sci 118: 5369-5379.
78. Krysinska H, Hoogenkamp M, Ingram R, Wilson N, Tagoh H, Laslo P, Singh H, Bonifer C. 2007. A two-step, PU.1- dependent mechanism for developmentally regulated chromatin remodeling and transcription of the c-fms gene. Mol Cell Biol 27: 878-887.
79. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, Gantner BN, Dinner AR, Singh H. 2006. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126: 755-766.
80. Le Beau MM, Pettenati MJ, Lemons RS, Diaz MO, Westbrook CA, Larson RA, Sherr CJ, Rowley JD. 1986. Assignment of the GM-CSF, CSF-1, and FMS genes to human chromosome 5 provides evidence for linkage of a family of genes regulating hematopoiesis and for their involvement in the deletion (5q) in myeloid disorders. Cold Spring Harb Symp Quant Biol 51: 899-909.
81. Lee AW. 2011. The role of atypical protein kinaseCin CSF-1- dependent Erk activation and proliferation in myeloid progenitors and macrophages. PLoS ONE 6: e25580.
82. Lee AW, States DJ. 2000. Both src-dependent and -independent mechanisms mediate phosphatidylinositol 3-kinase regulation of colony-stimulating factor 1-activated mitogen- activated protein kinases in myeloid progenitors. Mol Cell Biol 20: 6779-6798.
83. Lee PS, Wang Y, Dominguez MG, Yeung YG, Murphy MA, Bowtell DD, Stanley ER. 1999. The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J 18: 3616-3628.
84. Lee AW, Mao Y, Penninger JM, Yu S. 2011. Gab2 promotes colony-stimulating factor 1-regulated macrophage expansion via alternate effectors at different stages of development. Mol Cell Biol 31: 4563-4581.
85. Leveugle M, Prat K, Popovici C, Birnbaum D, Coulier F. 2004. Phylogenetic analysis of Ciona intestinalis gene superfamilies supports the hypothesis of successive gene expansions. J Mol Evol 58: 168-181.
86. Li W, Stanley ER. 1991. Role of dimerization and modification of the CSF-1 receptor in its activation and internalization during the CSF-1 response. EMBO J 10: 277-288.
87. LiW, Yeung YG, Stanley ER. 1991. Tyrosine phosphorylation of acommon 57-kDa protein in growth factor-stimulated and -transformed cells. J Biol Chem 266: 6808-6814.
88. Li ZH, Spektor A, Varlamova O, Bresnick AR. 2003. Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 42: 14258-14266.
89. Li ZH, Dulyaninova NG, House RP, Almo SC, Bresnick AR. 2010. S100A4 regulates macrophage chemotaxis. Mol Biol Cell 21: 2598-2610.
90. Lin H, Lee E, Hestir K, Leo C, Huang M, Bosch E, Halenbeck R, Wu G, Zhou A, Behrens D, et al. 2008. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 320: 807-811.
91. Liu Y, Jenkins B, Shin JL, Rohrschneider LR. 2001. Scaffolding protein Gab2 mediates differentiation signaling downstream of Fms receptor tyrosine kinase. Mol Cell Biol 21: 3047-3056.
92. Liu H, Leo C, Chen X, Wong BR, Williams LT, Lin H, He X. 2012. The mechanism of shared but distinct CSF-1R signaling by the non-homologous cytokines IL-34 and CSF- 1. Biochim Biophys Acta 1824: 938-945.
93. Luo J, Elwood F, Britschgi M, Villeda S, Zhang H, Ding Z, Zhu L, Alabsi H, Getachew R, Narasimhan R, et al. 2013. Colony-stimulating factor 1 receptor (CSF1R) signaling in injured neurons facilitates protection and survival. J Exp Med 210: 157-172.
94. Ma X, Lin WY, Chen Y, Stawicki S, Mukhyala K, Wu Y, Martin F, Bazan JF, Starovasnik MA. 2012. Structural basis for the dual recognition of helical cytokines IL-34 and CSF-1 by CSF-1R. Structure 20: 676-687.
95. MacDonald KP, Rowe V, Bofinger HM, Thomas R, Sasmono T, Hume DA, Hill GR. 2005. The colony-stimulating factor 1 receptor is expressed on dendritic cells during differentiation and regulates their expansion. J Immunol 175: 1399-1405.
96. Mahankali M, Peng HJ, Cox D, Gomez-Cambronero J. 2011a. The mechanism of cell membrane ruffling relies on a phospholipase D2 (PLD2), Grb2 and Rac2 association. Cell Signal 23: 1291-1298.
97. Mahankali M, Peng HJ, Henkels KM, Dinauer MC, Gomez- Cambronero J. 2011b. Phospholipase D2 (PLD2) is a guanine nucleotide exchange factor (GEF) for the GTPase Rac2. Proc Natl Acad Sci 108: 19617-19622.
98. Mancini A, Koch A, Whetton AD, Tamura T. 2004. The MCSF receptor substrate and interacting protein FMIP is governed in its subcellular localization by protein kinase C-mediated phosphorylation, and thereby potentiates M-CSF-mediated differentiation. Oncogene 23: 6581-6589.
99. Marks DC, Csar XF, Wilson NJ, Novak U, Ward AC, Kanagasundarum V, Hoffmann BW, Hamilton JA. 1999. Expression of a Y559F mutant CSF-1 receptor in M1 myeloid cells: A role for Src kinases in CSF-1 receptormediated differentiation. Mol Cell Biol Res Commun 1: 144-152.
100. McMahon KA, Wilson NJ, Marks DC, Beecroft TL, Whitty GA, Hamilton JA, Csar XF. 2001. Colony-stimulating factor-1 (CSF-1) receptor-mediated macrophage differentiation in myeloid cells: A role for tyrosine 559-dependent protein phosphatase 2A (PP2A) activity. Biochemical J 358: 431-436.
101. Meng S, Chen Z, Munoz-Antonia T, Wu J. 2005. Participation of both Gab1 and Gab2 in the activation of the ERK/ MAPK pathway by epidermal growth factor. Biochem J 391: 143-151.
102. Morgan CJ, Stanley ER. 1984. Chemical crosslinking of the mononuclear phagocyte specific growth factor CSF-1 to its receptor at the cell surface. Biochem Biophys Res Commun 119: 35-41.
103. Mossadegh-Keller N, Sarrazin S, Prashanth KK, Espinoza L, Stanley ER, Nutt SL, Moore J, Sieweke MH. 2013. M-CSF instructs myeloid lineage fate in single hematopoietic stem cells. Nature 497: 239-243.
104. Mouchemore KA, Sampaio NG, Murrey MW, Stanley ER, Lannutti BJ, Pixley FJ. 2013. Specific inhibition of PI3K p110d inhibits CSF-1-induced macrophage spreading and invasive capacity. FEBS J 280: 5228-5236.
105. Munugalavadla V, Borneo J, Ingram DA, Kapur R. 2005. p85a subunit of class IA PI-3 kinase is crucial for macrophage growth and migration. Blood 106: 103-109.
106. Murray JT, Craggs G, Wilson L, Kellie S. 2000.Mechanism of phosphatidylinositol 3-kinase-dependent increases in BAC1.2F5 macrophage-like cell density in response to M-CSF: Phosphatidylinositol 3-kinase inhibitors increase the rate of apoptosis rather than inhibit DNA synthesis. Inflamm Res 49: 610-618.
107. Nandi S, Akhter MP, Seifert MF, Dai XM, Stanley ER. 2006. Developmental and functional significance of the CSF-1 proteoglycan chondroitin sulfate chain. Blood 107: 786-795.
108. Nandi S, Gokhan S, Dai XM, Wei S, Enikolopov G, Lin H, Mehler MF, Stanley ER. 2012. The CSF-1 receptor ligands IL-34 and CSF-1 exhibit distinct developmental brain expression patterns and regulate neural progenitor cell maintenance and maturation. Dev Biol 367: 100-113.
109. Nandi S, Cioce M, Yeung YG, Nieves E, Tesfa L, Lin H, Hsu AW, Halenbeck R, Cheng HY, Gokhan S, et al. 2013. Receptor- type protein-tyrosine phosphatase z is a functional receptor for interleukin-34. J Biol Chem 288: 21972-21986.
110. Nataf S, Anginot A, Vuaillat C, Malaval L, Fodil N, Chereul E, Langlois JB, Dumontel C, Cavillon G, Confavreux C, et al. 2005. Brain and bone damage in KARAP/DAP12 loss-of-function mice correlate with alterations in microglia and osteoclast lineages. Am J Pathol 166: 275-286.
111. Nicholson AM, Baker MC, Finch NA, Rutherford NJ, Wider C, Graff-Radford NR, Nelson PT, Clark HB, Wszolek ZK, Dickson DW, et al. 2013. CSF1R mutations link POLD and HDLS as a single disease entity. Neurology 80: 1033-1040.
112. Nishida K, Yoshida Y, Itoh M, Fukada T, Ohtani T, Shirogane T, Atsumi T, Takahashi-Tezuka M, Ishihara K, Hibi M, et al. 1999. Gab-family adapter proteins act downstream of cytokine and growth factor receptors and T- and B-cell antigen receptors. Blood 93: 1809-1816.
113. Otero K, Turnbull IR, Poliani PL, Vermi W, Cerutti E, Aoshi T, Tassi I, Takai T, Stanley SL, Miller M, et al. 2009. Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and b-catenin. Nat Immunol 10: 734-743.
114. Ovchinnikov DA, DeBats CE, Sester DP, Sweet MJ, Hume DA. 2010. A conserved distal segment of the mouse CSF- 1 receptor promoter is required for maximal expression of a reporter gene in macrophages and osteoclasts of transgenic mice. J Leukoc Biol 87: 815-822.
115. Owen KA, Pixley FJ, Thomas KS, Vicente-Manzanares M, Ray BJ, Horwitz AF, Parsons JT, Beggs HE, Stanley ER, Bouton AH. 2007. Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol 179: 1275-1287.
116. Pandit J, Bohm A, Jancarik J, Halenbeck R, Koths K, Kim S-H. 1992. Three-dimensional structure of dimeric human recombinant macrophage colony-stimulating factor. Science 258: 1358-1362.
117. Papakonstanti EA, Ridley AJ, Vanhaesebroeck B. 2007. The p110d isoform of PI 3-kinase negatively controls RhoA and PTEN. EMBO J 26: 3050-3061.
118. Papakonstanti EA, Zwaenepoel O, Bilancio A, Burns E, Nock GE, Houseman B, Shokat K, Ridley AJ, Vanhaesebroeck B. 2008. Distinct roles of class IA PI3K isoforms in primary and immortalised macrophages. J Cell Sci 121: 4124-4133.
119. Parichy DM, Turner JM. 2003. Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130: 817-833.
120. Parichy DM, Rawls JF, Pratt SJ, Whitfield TT, Johnson SL. 1999. Zebrafish sparse corresponds to an orthologue of ckit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development 126: 3425-3436.
121. Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL. 2000. An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 127: 3031-3044.
122. Park H, Ishihara D, Cox D. 2011. Regulation of tyrosine phosphorylation in macrophage phagocytosis and chemotaxis. Arch Biochem Biophys 510: 101-111.
123. Peng HJ, Henkels KM, Mahankali M, Marchal C, Bubulya P, Dinauer MC, Gomez-Cambronero J. 2011. The dual effect of Rac2 on phospholipase D2 regulation that explains both the onset and termination of chemotaxis. Mol Cell Biol 31: 2227-2240.
124. Pixley FJ. 2012.Macrophage migration and its regulation by CSF-1. Int J Cell Biol 2012: 501962.
125. Pixley FJ, Stanley ER. 2004. CSF-1 regulation of the wandering macrophage: Complexity in action. Trends Cell Biol 14: 628-638.
126. Pixley FJ, Lee PS, Condeelis JS, Stanley ER. 2001. Protein tyrosine phosphatase w regulates paxillin tyrosine phosphorylation and mediates colony-stimulating factor 1- induced morphological changes in macrophages. Mol Cell Biol 21: 1795-1809.
127. Pollard JW. 2009. Trophic macrophages in development and disease. Nat Rev Immunol 9: 259-270.
128. Pollard JW, Stanley ER. 1996. Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic. Adv Dev Biochem 4: 153-193.
129. Price LKH, Choi HU, Rosenberg L, Stanley ER. 1992. The predominant form of secreted colony stimulating factor- 1 is a proteoglycan. J Biol Chem 267: 2190-2199.
130. Rademakers R, Baker M, Nicholson AM, Rutherford NJ, Finch N, Soto-Ortolaza A, Lash J, Wider C, Wojtas A, DeJesus-Hernandez M, et al. 2011. Mutations in the colony stimulating factor 1 receptor (CSF1R) gene cause hereditary diffuse leukoencephalopathy with spheroids. Nat Genet 44: 200-205.
131. Rettenmier CW, Chen JH, Roussel MF, Sherr CJ. 1985. The product of the c-fms proto-oncogene: A glycoprotein with associated tyrosine kinase activity. Science 228: 320-322.
132. Rettenmier CW, Roussel MF, Ashmun RA, Ralph P, Price K, Sherr CJ. 1987. Synthesis of membrane-bound colonystimulating factor 1 (CSF-1) and downmodulation of CSF-1 receptors in NIH 3T3 cells transformed by cotransfection of the human CSF-1 and c-fms (CSF-1 receptor) genes. Mol Cell Biol 7: 2378-2387.
133. Ridley AJ. 2008. Regulation of macrophage adhesion and migration by Rho GTP-binding proteins. J Microsc 231: 518-523.
134. Rieger MA, Hoppe PS, Smejkal BM, Eitelhuber AC, Schroeder T. 2009. Hematopoietic cytokines can instruct lineage choice. Science 325: 217-218.
135. Roberts WM, Look AT, Roussel MF, Sherr CJ. 1988. Tandem linkage of human CSF-1 receptor (c-fms) and PDGF receptor genes. Cell 55: 655-661.
136. Roberts WM, Shapiro LH, Ashmun RA, Look AT. 1992. Transcription of the human colony-stimulating factor-1 receptor gene is regulated by separate tissue-specific promoters. Blood 79: 586-593.
137. Rohde CM, Schrum J, Lee AW. 2004. A juxtamembrane tyrosine in the colony stimulating factor-1 receptor regulates ligand-induced Src association, receptor kinase function, and down-regulation. J Biol Chem 279: 43448-43461.
138. Rohrschneider LR, Bourette RP, Lioubin MN, Algate PA, Myles GM, Carlberg K. 1997. Growth and differentiation signals regulated by the M-CSF receptor.Mol Reprod Dev 46: 96-103.
139. Rothwell VM, Rohrschneider LR. 1987. Murine c-fms cDNA: Cloning, sequence analysis and retroviral expression. Oncogene Res 1: 311-324.
140. Roussel MF, Downing JR, Rettenmier CW, Sherr CJ. 1988. A point mutation in the extracellular domain of the human CSF-1 receptor (c-fms proto-oncogene product) activates its transforming potential. Cell 55: 979-988.
141. Rousset D, Agnes F, Lachaume P, Andre C, Galibert F. 1995. Molecular evolution of the genes encoding receptor tyrosine kinase with immunoglobulinlike domains. J Mol Evol 41: 421-429.
142. Rovida E, Baccarini M, Olivotto M, Sbarba PD. 2002. Opposite effects of different doses of MCSF on ERK phosphorylation and cell proliferation in macrophages. Oncogene 21: 3670-3676.
143. Rovida E, Spinelli E, Sdelci S, Barbetti V, Morandi A, Giuntoli S, Dello Sbarba P. 2008. ERK5/BMK1 is indispensable for optimal colony-stimulating factor 1 (CSF-1)-induced proliferation in macrophages in a Src-dependent fashion. J Immunol 180: 4166-4172.
144. Salzburger W, Niederstatter H, Brandstatter A, Berger B, Parson W, Snoeks J, Sturmbauer C. 2006. Colour-assortative mating among populations of Tropheus moorii, a cichlid fish from Lake Tanganyika, East Africa. Proc Biol Sci 273: 257-266.
145. Sampaio NG, Yu W, Cox D, Wyckoff J, Condeelis J, Stanley ER, Pixley FJ. 2011. Phosphorylation of CSF-1R Y721 mediates its association with PI3K to regulate macrophage motility and enhancement of tumor cell invasion. J Cell Sci 124: 2021-2031.
146. Sarrazin S, Mossadegh-Keller N, Fukao T, Aziz A, Mourcin F, Vanhille L, Kelly Modis L, Kastner P, Chan S, Duprez E, et al. 2009. MafB restricts M-CSF-dependent myeloid commitment divisions of hematopoietic stem cells. Cell 138: 300-313.
147. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, Ostrowski MC, Himes SR, Hume DA. 2003. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101: 1155-1163.
148. Sauter KA, Bouhlel MA, O'Neal J, Sester DP, Tagoh H, Ingram RM, Pridans C, Bonifer C, Hume DA. 2013. The function of the conserved regulatory element within the second intron of the mammalian Csf1r locus. PLoS ONE 8: e54935.
149. Schubert C, Schalk-Hihi C, Struble GT, Ma HC, Petrounia IP, Brandt B, Deckman IC, Patch RJ, Player MR, Spurlino JC, et al. 2007. Crystal structure of the tyrosine kinase domain of colony-stimulating factor-1 receptor (cFMS) in complex with two inhibitors. J Biol Chem 282: 4094-4101.
150. Seiffert M, Custodio JM, Wolf I, Harkey M, Liu Y, Blattman JN, Greenberg PD, Rohrschneider LR. 2003. Gab3-deficient mice exhibit normal development and hematopoiesis and are immunocompetent. Mol Cell Biol 23: 2415-2424.
151. Sherr CJ. 1990. Colony-stimulating factor-1 receptor. Blood 75: 1-12.
152. Sherr CJ. 1991. Mitogenic response to colony-stimulating factor 1. Trends Genet 7: 398-402.
153. Sherr CJ, Rettenmier CW, Sacca R, Roussel MF, Look AT, Stanley ER. 1985. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell 41: 665-676.
154. Shim AH, Chang RA, Chen X, Longnecker R, He X. 2012. Multipronged attenuation of macrophage-colony stimulating factor signaling by Epstein-Barr virus BARF1. Proc Natl Acad Sci 109: 12962-12967.
155. Simoncic PD, Bourdeau A, Lee-Loy A, Rohrschneider LR, Tremblay ML, Stanley ER, McGlade CJ. 2006. T-cell protein tyrosine phosphatase (Tcptp) is a negative regulator of colony-stimulating factor 1 signaling and macrophage differentiation. Mol Cell Biol 26: 4149-4160.
156. Stanley ER. 1979. Colony-stimulating factor (CSF) radioimmunoassay: Detection of a CSF subclass stimulating macrophage production. Proc Natl Acad Sci 76: 2969-2973.
157. Stanley ER, Heard PM. 1977. Factors regulating macrophage production and growth. Purification and some properties of the colony stimulating factor from medium conditioned by mouse L cells. J Biol Chem 252: 4305-4312.
158. Stanley ER, Chen DM, Lin H-S. 1978. Induction of macrophage production and proliferation by a purified colony stimulating factor. Nature 274: 168-170.
159. Steinbrecher UP, Gómez-Muñ oz A, Duronio V. 2004. Acid sphingomyelinase in macrophage apoptosis. Curr Opin Lipidol 15: 531-537.
160. Strockbine LD, Cohen JI, Farrah T, Lyman SD, Wagener F, DuBose RF, Armitage RJ, Spriggs MK.1998. TheEpstein-Barr virus BARF1 gene encodes a novel, soluble colonystimulating factor-1 receptor. J Virol 72: 4015-4021.
161. Sundquist KT, Cecchini MG, Marks SC Jr, 1995. Colonystimulating factor-1 injections improve but do not cure skeletal sclerosis in osteopetrotic (op) mice. Bone 16: 39.
162. Suzu S, Ohtsuki T, Yanai N, Takatsu Z, Kawashima T, Takaku F, Nagata N, Motoyoshi K. 1992. Identification of a high molecular weight macrophage colony-stimulating factor as a glycosaminoglycan-containing species. J Biol Chem 267: 4345-4348.
163. Tagoh H, Himes R, Clarke D, Leenen PJ, Riggs AD, Hume D, Bonifer C. 2002. Transcription factor complex formation and chromatin fine structure alterations at the murine cfms (CSF-1 receptor) locus during maturation of myeloid precursor cells. Genes Dev 16: 1721-1737.
164. Tagoh H, Schebesta A, Lefevre P, Wilson N, Hume D, Busslinger M, Bonifer C. 2004. Epigenetic silencing of the cfms locus during B-lymphopoiesis occurs in discrete steps and is reversible. EMBO J 23: 4275-4285.
165. Tagoh H, Ingram R, Wilson N, Salvagiotto G, Warren AJ, Clarke D, Busslinger M, Bonifer C. 2006. The mechanism of repression of the myeloid-specific c-fms gene by Pax5 during B lineage restriction. EMBO J 25: 1070-1080.
166. Takeshita S, Faccio R, Chappel J, Zheng L, Feng X, Weber JD, Teitelbaum SL, Ross FP. 2007. c-Fms tyrosine 559 is a major mediator of M-CSF-induced proliferation of primary macrophages. J Biol Chem 282: 18980-18990.
167. Tian Y, Shen H, Xia L, Lu J. 2013. Elevated serum and synovial fluid levels of Interleukin-34 in rheumatoid arthritis: Possible associationwith disease progression via interleukin- 17 production. J InterferonCytokine Res 33: 398-401.
168. Tsujita K, Kondo A, Kurisu S, Hasegawa J, Itoh T, Takenawa T. 2013. Antagonistic regulation of F-BAR protein assemblies controls actin polymerization during podosome formation. J Cell Sci 126: 2267-2278.
169. Tushinski RJ, Stanley ER. 1983. The regulation of macrophage protein turnover by a colony stimulating factor (CSF-1). J Cell Physiol 116: 67-75.
170. Tushinski RJ, Stanley ER. 1985. The regulation of mononuclear phagocyte entry into S phase by the colony stimulating factor CSF-1. J Cell Physiol 122: 221-228.
171. Tushinski RJ, Oliver IT, Guilbert LJ, Tynan PW, Warner JR, Stanley ER. 1982. Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell 28: 71-81.
172. Valledor AF, Xaus J, Marques L, Celada A. 1999.Macrophage colony-stimulating factor induces the expression of mitogen- activated protein kinase phosphatase-1 through a protein kinase C-dependent pathway. J Immunol 163: 2452-2462.
173. Van Nguyen A, Pollard JW. 2002. Colony stimulating factor- 1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth. Dev Biol 247: 11-25.
174. VedhamV, Phee H, Coggeshall KM. 2005.Vav activation and function as a rac guanine nucleotide exchange factor in macrophage colony-stimulating factor-induced macrophage chemotaxis. Mol Cell Biol 25: 4211-4220.
175. Verstraete K, Savvides SN. 2012. Extracellular assembly and activation principles of oncogenic class III receptor tyrosine kinases. Nat Rev Cancer 12: 753-766.
176. Visvader J, Verma IM. 1989. Differential transcription of exon 1 of the human c-fms gene in placental trophoblasts and monocytes. Mol Cell Biol 9: 1336-1341.
177. von Holst A, Sirko S, Faissner A. 2006. The unique 473HDChondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci 26: 4082-4094.
178. Walsh JC, DeKoter RP, Lee HJ, Smith ED, Lancki DW, Gurish MF, Friend DS, Stevens RL, Anastasi J, Singh H. 2002. Cooperative and antagonistic interplay betweenPU.1 and GATA-2 in the specification of myeloid cell fates. Immunity 17: 665-676.
179. Walter M, Lucet IS, Patel O, Broughton SE, Bamert R, Williams NK, Fantino E, Wilks AF, Rossjohn J. 2007. The 2.7 A ° crystal structure of the autoinhibited human c-Fms kinase domain. J Mol Biol 367: 839-847.
180. Wang ZE, Myles GM, Brandt CS, Lioubin MN, Rohrschneider L. 1993. Identification of the ligand-binding regions in the macrophage colony-stimulating factor receptor extracellular domain. Mol Cell Biol 13: 5348-5359.
181. Wang Y, Yeung YG, Langdon WY, Stanley ER. 1996. c-Cbl is transiently tyrosine-phosphorylated, ubiquitinated, and membrane-targeted following CSF-1 stimulation of macrophages. J Biol Chem 271: 17-20.
182. Wang Y, Berezovska O, Fedoroff S. 1999a. Expression of colony stimulating factor-1 receptor (CSF-1R) by CNS neurons in mice. J Neurosci Res 57: 616-632.
183. Wang Y, Yeung YG, Stanley ER. 1999b. CSF-1 stimulated multiubiquitination of the CSF-1 receptor and of Cbl follows their tyrosine phosphorylation and association with other signaling proteins. J Cell Biochem 72: 119-134.
184. Wang Y, Szretter KJ, Vermi W, Gilfillan S, Rossini C, Cella M, Barrow AD, Diamond MS, Colonna M. 2012. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 13: 753-760.
185. Webb SE, Pollard JW, Jones GE. 1996. Direct observation and quantification of macrophage chemoattraction to the growth factor CSF-1. J Cell Sci 109: 793-803.
186. Wei S, Nandi S, Chitu V, Yeung YG, Yu W, Huang M, Williams LT, Lin H, Stanley ER. 2010. Functional overlap but differential expression of CSF-1 and IL-34 in their CSF-1 receptor-mediated regulation of myeloid cells. J Leukoc Biol 88: 495-505.
187. Wells CM, Walmsley M, Ooi S, Tybulewicz V, Ridley AJ. 2004. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J Cell Sci 117: 1259-1268.
188. Wells CM, Bhavsar PJ, Evans IR, Vigorito E, Turner M, Tybulewicz V, Ridley AJ. 2005. Vav1 and Vav2 play different roles in macrophage migration and cytoskeletal organization. Exp Cell Res 310: 303-310.
189. Wheeler AP, Wells CM, Smith SD, Vega FM, Henderson RB, Tybulewicz VL, Ridley AJ. 2006. Rac1 and Rac2 regulate macrophage morphology but are not essential for migration. J Cell Sci 119: 2749-2757.
190. Wiktor-Jedrzejczak W, Urbanowska E, Aukerman SL, Pollard JW, Stanley ER, Ralph P, Ansari AA, Sell KW, Szperl M. 1991. Correction by CSF-1 of defects in the osteopetrotic op/op mouse suggests local, developmental, and humoral requirements for this growth factor. Exp Hematol 19: 1049-1054.
191. Williams N, Bertoncello I, Kavnoudias H, Zsebo K, McNiece I. 1992. Recombinant rat stem cell factor stimulates the amplification and differentiation of fractionated mouse stem cell populations. Blood 79: 58-64.
192. Wilson NJ, Cross M, Nguyen T, Hamilton JA. 2005. cAMP inhibits CSF-1-stimulated tyrosine phosphorylation but augments CSF-1R-mediated macrophage differentiation and ERK activation. Febs J 272: 4141-4152.
193. Wolf I, Jenkins BJ, Liu Y, Seiffert M, Custodio JM, Young P, Rohrschneider LR. 2002. Gab3, a new DOS/Gab family member, facilitates macrophage differentiation. Mol Cell Biol 22: 231-244.
194. Woolford J, McAuliffe A, Rohrschneider LR. 1988. Activation of the feline c-fms proto-oncogene: Multiple alterations are required to generate a fully transformed phenotype. Cell 55: 965-977.
195. Wu Y, Dowbenko D, Lasky LK. 1998. PSTPIP 2, a second tyrosine phosphorylated, cytoskeletal associated protein that binds a PEST-type protein-tyrosine phosphatase. J Biol Chem 273: 30487-30496.
196. Xiong Y, Song D, Cai Y, Yu W, Yeung YG, Stanley ER. 2011. A CSF-1 receptor phosphotyrosine 559 signaling pathway regulates receptor ubiquitination and tyrosine phosphorylation. J Biol Chem 286: 952-960.
197. Xu X-X, Tessner TG, Rock CO, Jackowski S. 1993. Phosphatidylcholine hydrolysis and c-myc expression are in collaborating mitogenic pathways activated by colony-stimulating factor 1. Mol Cell Biol 13: 1522-1533.
198. Yang H, Reinherz EL. 2006. CD2BP1 modulates CD2-dependent T cell activation via linkage to protein tyrosine phosphatase (PTP)-PEST. J Immunol 176: 5898-5907.
199. Yang Y, Yuzawa S, Schlessinger J. 2008. Contacts between membrane proximal regions of the PDGF receptor ectodomain are required for receptor activation but not for receptor dimerization. Proc Natl Acad Sci 105: 7681-7686.
200. Yarden Y, Escobedo JA, Kuang WJ, Yang-Fang TL, Daniel TO, Tremble PM, Chen EY, Ando ME, Harkins RN, Francke U, et al. 1986. Structure of the receptor for platelet- derived growth factor helps define a family of closely related growth factor receptors. Nature 323: 226-232.
201. Yeung YG, Stanley ER. 2003. Proteomic approaches to the analysis of early events in CSF-1 signal transduction. Mol Cell Proteomics 2: 1143-1155.
202. Yeung Y-G, Jubinsky PT, Sengupta A, Yeung DC-Y, Stanley ER. 1987. Purification of the colony-stimulating factor 1 receptor and demonstration of its tyrosine kinase activity. Proc Natl Acad Sci 84: 1268-1271.
203. Yeung Y-G, Wang Y, Einstein DB, Lee PSW, Stanley ER. 1998. Colony-stimulating factor-1 stimulates the formation of multimeric cytosolic complexes of signaling proteins and cytoskeletal components in macrophages. J Biol Chem 273: 17128-17137.
204. Yu W, Chen J, Xiong Y, Pixley FJ, Dai XM, Yeung YG, Stanley ER. 2008. CSF-1 receptor structure/function in MacCsf1r2/2 macrophages: Regulation of proliferation, differentiation, and morphology. J Leukoc Biol 84: 852-863.
205. Yu W, Chen J, Xiong Y, Pixley FJ, Yeung YG, Stanley ER. 2012. Macrophage proliferation is regulated through CSF-1 receptor tyrosines 544, 559, and 807. J Biol Chem 287: 13694-13704.
206. Yuzawa S, Opatowsky Y, Zhang Z, Mandiyan V, Lax I, Schlessinger J. 2007. Structural basis for activation of the receptor tyrosine kinase KIT by stem cell factor. Cell 130: 323-334.
207. Zhang B, Ma Y, Guo H, Sun B, Niu R, Ying G, Zhang N. 2009. Akt2 is required for macrophage chemotaxis. Eur J Immunol 39: 894-901.