CSF-1R signaling in health and disease: A focus on the mammary gland

Journal of Mammary Gland Biology and Neoplasia

Volumn 19, Issue 2, 2014, Pages 149-159

  Sullivan, Amy Renee ^a   Pixley, Fiona Jane ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Breast cancer; CSF 1; CSF 1R; Development; Macrophage; Motility

Indexed keywords

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR 1 RECEPTOR; CYTOKINE; CYTOKINE RECEPTOR; INTERLEUKIN 34; UNCLASSIFIED DRUG; COLONY STIMULATING FACTOR RECEPTOR;

ARTICLE; BREAST CANCER; CANCER RESISTANCE; CELL MOTILITY; HOMEOSTASIS; HUMAN; MACROPHAGE; MAMMARY GLAND; NONHUMAN; ONTOGENY; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; ANIMAL; BREAST TUMOR; DISEASE COURSE; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; METABOLISM; UDDER;

ANIMALS; BREAST NEOPLASMS; DISEASE PROGRESSION; FEMALE; HUMANS; MACROPHAGES; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MAMMARY NEOPLASMS, ANIMAL; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR;

EID: 84905111903     PISSN: 10833021     EISSN: 15737039     Source Type: Journal    
DOI: 10.1007/s10911-014-9320-1     Document Type: Article

References (127)

1. Aharinejad S, Abraham D, Paulus P, et al. Colony-stimulating factor-1 antisense treatment suppresses growth of human tumor xenografts in mice. Cancer Res. 2002;62:5317-24.
2. Aharinejad S, Paulus P, Sioud M, et al. Colony-stimulating factor-1 blockade by antisense oligonucleotides and small interfering RNAs suppresses growth of human mammary tumor xenografts in mice. Cancer Res. 2004;64:5378-84.
3. Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci U S A. 2010;107:8363-8.
4. Arpa L, Valledor AF, Lloberas J, Celada A. IL-4 blocks M-CSF-dependent macrophage proliferation by inducing p21Waf1 in a STAT6-dependent way. Eur J Immunol. 2009;39:514-26.
5. Bartocci A, Mastrogiannis DS, Migliorati G, Stockert RJ, Wolkoff AW, Stanley ER. Macrophages specifically regulate the concentration of their own growth factor in the circulation. Proc Natl Acad Sci U S A. 1987;84:6179-83.
6. Beck AH, Espinosa I, Edris B, et al. The macrophage colony-stimulating factor 1 response signature in breast carcinoma. Clin Cancer Res. 2009;15:778-87.
7. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002;196:254-65.
8. Bingle L, Lewis CE, Corke KP, Reed MW, Brown NJ. Macrophages promote angiogenesis in human breast tumour spheroids in vivo. Br J Cancer. 2006;94:101-7.
9. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol. 2013.
10. Boocock CA, Jones GE, Stanley ER, Pollard JW. Colony-stimulating factor-1 induces rapid behavioural responses in the mouse macrophage cell line, BAC1.2 F5. J Cell Sci. 1989;93:447-56.
11. Burns CJ, Wilks AF. c-FMS inhibitors: a patent review. Expert Opin Ther Pat. 2011;21:147-65.
12. Carey B, Trapnell BC. The molecular basis of pulmonary alveolar proteinosis. Clin Immunol. 2010;135:223-35.
13. Cecchini MG, Dominguez MG, Mocci S, et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development. 1994;120:1357-72.
14. Chihara T, Suzu S, Hassan R, et al. IL-34 and M-CSF share the receptor Fms but are not identical in biological activity and signal activation. Cell Death Differ. 2010;17:1917-27.
15. Chitu V, Stanley ER. Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol. 2006;18:39-48.
16. Chow A, Huggins M, Ahmed J, et al. CD169 (+) macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat Med. 2013;19:429-36.
17. Cohen PE, Zhu L, Nishimura K, Pollard JW. Colony-stimulating factor 1 regulation of neuroendocrine pathways that control gonadal function in mice. Endocrinology. 2002;143:1413-22.
18. Comalada M, Xaus J, Sanchez E, Valledor AF, Celada A. Macrophage colony-stimulating factor-, granulocyte-macrophage colony-stimulating factor-, or IL-3-dependent survival of macrophages, but not proliferation, requires the expression of p21 (Waf1) through the phosphatidylinositol 3-kinase/Akt pathway. Eur J Immunol. 2004;34:2257-67.
19. Dai XM, Ryan GR, Hapel AJ, et al. 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. 2002;99:111-20.
20. Dai XM, Zong XH, Sylvestre V, Stanley ER. 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. 2004;103:1114-23.
21. Davies LC, Jenkins SJ, Allen JE, Taylor PR. Tissue-resident macrophages. Nat Immunol. 2013;14:986-95.
22. De Palma M, Lewis CE. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell. 2013;23:277-86.
23. DeNardo DG, Barreto JB, Andreu P, et al. CD4 (+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell. 2009;16:91-102.
24. DeNardo DG, Brennan DJ, Rexhepaj E, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 2011;1:54-67.
25. Fantin A, Vieira JM, Gestri G, et al. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood. 2010;116:829-40.
26. Feng R, Desbordes SC, Xie H et al. PU.1 and C/EBPalpha/beta convert fibroblasts into macrophage-like cells. Proceedings of the National Academy of Sciences USA. 2008;105:6057-6062.
27. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9:162-74.
28. Gautier EL, Shay T, Miller J, et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol. 2012;13:1118-28.
29. Gemma C, Bachstetter AD. The role of microglia in adult hippocampal neurogenesis. Front Cell Neurosci. 2013;7:229.
30. Ginhoux F, Greter M, Leboeuf M, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 2010;330:841-5.
31. Gomez Perdiguero E, Schulz C, Geissmann F. Development and homeostasis of "resident" myeloid cells: the case of the microglia. Glia. 2013;61:112-20.
32. Gordon S. Alternative activation of macrophages. Nat Rev Immunol. 2003;3:23-35.
33. Goswami S, Sahai E, Wyckoff JB, et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 2005;65:5278-83.
34. Gouon-Evans V, Lin EY, Pollard JW. Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development. Breast Cancer Res. 2002;4:155-64.
35. Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development. 2000;127:2269-82.
36. Guleria I, Pollard JW. Aberrant macrophage and neutrophil population dynamics and impaired Th1 response to Listeria monocytogenes in colony-stimulating factor 1-deficient mice. Infect Immun. 2001;69:1795-807.
37. Guo C, Buranych A, Sarkar D, Fisher PB, Wang XY. The role of tumor-associated macrophages in tumor vascularization. Vasc Cell. 2013;5:20.
38. Hamilton JA. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol. 2008;8:533-44.
39. Hamilton JA, Achuthan A. Colony stimulating factors and myeloid cell biology in health and disease. Trends Immunol. 2013;34:81-9.
40. Hamilton JA, Whitty G, Masendycz P, et al. The critical role of the colony-stimulating factor-1 receptor in the differentiation of myeloblastic leukemia cells. Mol Cancer Res. 2008;6:458-67.
41. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21:309-22.
42. Hashimoto D, Chow A, Noizat C, et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 2013;38:792-804.
43. Herbomel P, Thisse B, Thisse C. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol. 2001;238:274-88.
44. Hume DA, Macdonald KP. Therapeutic applications of macrophage colony-stimulating factor (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood. 2011.
45. Ingman WV, Wyckoff J, Gouon-Evans V, Condeelis J, Pollard JW. Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Dev Dyn. 2006;235:3222-9.
46. Jenkins SJ, Ruckerl D, Cook PC, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science. 2011;332:1284-8.
47. Kacinski BM. CSF-1 and its receptor in breast carcinomas and neoplasms of the female reproductive tract. Mol Reprod Dev. 1997;46:71-4.
48. Kirma N, Luthra R, Jones J, et al. Overexpression of the colony-stimulating factor (CSF-1) and/or its receptor c-fms in mammary glands of transgenic mice results in hyperplasia and tumor formation. Cancer Res. 2004;64:4162-70.
49. Koh TJ, DiPietro LA. Inflammation and wound healing: the role of the macrophage. Expert Rev Mol Med. 2011;13:e23.
50. Koschmieder S, Rosenbauer F, Steidl U, Owens BM, Tenen DG. Role of transcription factors C/EBPalpha and PU.1 in normal hematopoiesis and leukemia. Int J Hematol. 2005;81:368-77.
51. Leek RD, Harris AL. Tumor-associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia. 2002;7:177-89.
52. Lichanska AM, Hume DA. Origins and functions of phagocytes in the embryo. Exp Hematol. 2000;28:601-11.
53. Lin H, Lee E, Hestir K, et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 2008;320:807-11.
54. Lin EY, Li JF, Gnatovskiy L, et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 2006;66:11238-46.
55. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001;193:727-40.
56. MacDonald KP, Palmer JS, Cronau S, et al. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation. Blood. 2010;116:3955-63.
57. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010;22:231-7.
58. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677-86.
59. Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13.
60. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol. 2006;177:7303-11.
61. McDermott RS, Deneux L, Mosseri V, et al. Circulating macrophage colony stimulating factor as a marker of tumour progression. Eur Cytokine Netw. 2002;13:121-7.
62. Medzhitov R. Origin and physiological roles of inflammation. Nature. 2008;454:428-35.
63. Mok S, Koya RC, Tsui C, et al. Inhibition of CSF-1 receptor improves the antitumor efficacy of adoptive cell transfer immunotherapy. Cancer Res. 2014;74:153-61.
64. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8:958-69.
65. Mouchemore KA, Pixley FJ. CSF-1 signaling in macrophages: pleiotrophy through phosphotyrosine-based signaling pathways. Crit Rev Clin Lab Sci. 2012;49:49-61.
66. Mouchemore KA, Sampaio NG, Murrey MW, Stanley ER, Lannutti BJ, Pixley FJ. Specific inhibition of PI3K p110delta inhibits CSF-1-induced macrophage spreading and invasive capacity. FEBS J. 2013;280:5228-36.
67. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723-37.
68. Nakahama K. Cellular communications in bone homeostasis and repair. Cell Mol Life Sci. 2010;67:4001-9.
69. Nandi S, Akhter MP, Seifert MF, Dai XM, Stanley ER. Developmental and functional significance of the CSF-1 proteoglycan chondroitin sulfate chain. Blood. 2006;107:786-95.
70. O'Brien J, Martinson H, Durand-Rougely C, Schedin P. Macrophages are crucial for epithelial cell death and adipocyte repopulation during mammary gland involution. Development. 2012;139:269-75.
71. Ojalvo LS, Whittaker CA, Condeelis JS, Pollard JW. Gene expression analysis of macrophages that facilitate tumor invasion supports a role for Wnt-signaling in mediating their activity in primary mammary tumors. J Immunol. 2010;184:702-12.
72. Paolicelli RC, Bolasco G, Pagani F, et al. Synaptic pruning by microglia is necessary for normal brain development. Science. 2011;333:1456-8.
73. Patsialou A, Wyckoff J, Wang Y, Goswami S, Stanley ER, Condeelis JS. Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor. Cancer Res. 2009;69:9498-506.
74. Paulus P, Stanley ER, Schafer R, Abraham D, Aharinejad S. Colony-stimulating factor-1 antibody reverses chemoresistance in human MCF-7 breast cancer xenografts. Cancer Res. 2006;66:4349-56.
75. Pixley FJ. Macrophage migration and its regulation by CSF-1. International Journal of Cell Biology. 20121-12.
76. Pixley FJ, Lee PS, Condeelis JS, Stanley ER. Protein tyrosine phosphatase phi regulates paxillin tyrosine phosphorylation and mediates colony-stimulating factor 1-induced morphological changes in macrophages. Molecular and Cellular Biology. 2001;21:1795-809.
77. Pixley FJ, Stanley ER. CSF-1 regulation of the wandering macrophage: complexity in action. Trends in Cell Biology. 2004;14:628-38.
78. Pixley FJ, Xiong Y, Yu RY, Sahai EA, Stanley ER, Ye BH. BCL6 suppresses RhoA activity to alter macrophage morphology and motility. Journal of Cell Science. 2005;118:1873-83.
79. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol. 2009;9:259-70.
80. Pollard JW, Hennighausen L. Colony stimulating factor 1 is required for mammary gland development during pregnancy. Proc Natl Acad Sci U S A. 1994;91:9312-6.
81. Pridans C, Sauter KA, Baer K, Kissel H, Hume DA. CSF1R mutations in hereditary diffuse leukoencephalopathy with spheroids are loss of function. Sci Rep. 2013;3:3013.
82. Pyonteck SM, Akkari L, Schuhmacher AJ, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med. 2013;19:1264-72.
83. Qian B, Deng Y, Im JH, et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One. 2009;4:e6562.
84. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010;141:39-51.
85. Rademakers R, Baker M, Nicholson AM, et al. Mutations in the colony stimulating factor 1 receptor (CSF1R) gene cause hereditary diffuse leukoencephalopathy with spheroids. Nat Genet. 2012;44:200-5.
86. Rae F, Woods K, Sasmono T, et al. Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter. Dev Biol. 2007;308:232-46.
87. Ridge SA, Worwood M, Oscier D, Jacobs A, Padua RA. FMS mutations in myelodysplastic, leukemic, and normal subjects. Proc Natl Acad Sci U S A. 1990;87:1377-80.
88. Roussos ET, Condeelis JS, Patsialou A. Chemotaxis in cancer. Nat Rev Cancer. 2011;11:573-87.
89. Ryan GR, Dai XM, Dominguez MG, et al. Rescue of the colony-stimulating factor 1 (CSF-1)-nullizygous mouse (Csf1 (op)/Csf1 (op)) phenotype with a CSF-1 transgene and identification of sites of local CSF-1 synthesis. Blood. 2001;98:74-84.
90. Sampaio NG, Yu W, Cox D, et al. Phosphorylation of CSF-1R Y721 mediates its association with PI3K to regulate macrophage motility and enhancement of tumor cell invasion. J Cell Sci. 2011;124:2021-31.
91. Sasmono RT, Oceandy D, Pollard JW, et al. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood. 2003;101:1155-63.
92. Sauter KA, Pridans C, Sehgal A et al. Pleiotropic effects of extended blockade of CSF1R signaling in adult mice. J Leukoc Biol. 2014.
93. Scholl SM, Bascou CH, Mosseri V, et al. Circulating levels of colony-stimulating factor 1 as a prognostic indicator in 82 patients with epithelial ovarian cancer. Br J Cancer. 1994;69:342-6.
94. Scholl SM, Pallud C, Beuvon F, et al. Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J Natl Cancer Inst. 1994;86:120-6.
95. Schulz C, Gomez Perdiguero E, Chorro L, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 2012;336:86-90.
96. Sharma M, Beck AH, Webster JA, et al. Analysis of stromal signatures in the tumor microenvironment of ductal carcinoma in situ. Breast Cancer Res Treat. 2010;123:397-404.
97. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat Rev Immunol. 2011;11:762-74.
98. Shimada-Hiratsuka M, Naito M, Kaizu C. Shuying, Hasegawa G, LD S. Defective macrophage recruitment and clearance of apoptotic cells in the uterus of osteopetrotic mutant mice lacking macrophage colony-stimulating factor (M-CSF). J Submicrosc Cytol Pathol. 2000;32:297-307.
99. Stanley E, Lieschke GJ, Grail D, et al. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc Natl Acad Sci U S A. 1994;91:5592-6.
100. Stefater JA, Ren S, Lang RA, Duffield JS. Metchnikoff's policemen: macrophages in development, homeostasis and regeneration. Trends Mol Med. 2011.
101. Stein M, Keshav S, Harris N, Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med. 1992;176:287-92.
102. Such E, Cervera J, Valencia A, et al. Absence of mutations in the tyrosine kinase and juxtamembrane domains of C-FMS gene in chronic myelomonocytic leukemia (CMML). Leuk Res. 2009;33:e162-3.
103. Tang R, Beuvon F, Ojeda M, Mosseri V, Pouillart P, Scholl S. M-CSF (monocyte colony stimulating factor) and M-CSF receptor expression by breast tumour cells: M-CSF mediated recruitment of tumour infiltrating monocytes? J Cell Biochem. 1992;50:350-6.
104. Teitelbaum R, Schubert W, Gunther L, et al. The M cell as a portal of entry to the lung for the bacterial pathogen Mycobacterium tuberculosis. Immunity. 1999;10:641-50.
105. Tessem JS, Jensen JN, Pelli H, et al. Critical roles for macrophages in islet angiogenesis and maintenance during pancreatic degeneration. Diabetes. 2008;57:1605-17.
106. Trapnell BC, Whitsett JA. Gm-CSF regulates pulmonary surfactant homeostasis and alveolar macrophage-mediated innate host defense. Annu Rev Physiol. 2002;64:775-802.
107. van Furth R, Cohn ZA. The origin and kinetics of mononuclear phagocytes. J Exp Med. 1968;128:415-35.
108. Van Nguyen A, Pollard JW. Colony stimulating factor-1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth. Dev Biol. 2002;247:11-25.
109. van Ravenswaay Claasen HH, Kluin PM, Fleuren GJ. Tumor infiltrating cells in human cancer. On the possible role of CD16+ macrophages in antitumor cytotoxicity. Lab Invest. 1992;67:166-74.
110. Vereyken EJ, Heijnen PD, Baron W, de Vries EH, Dijkstra CD, Teunissen CE. Classically and alternatively activated bone marrow derived macrophages differ in cytoskeletal functions and migration towards specific CNS cell types. J Neuroinflammation. 2011;8:58.
111. Wang Y, Szretter KJ, Vermi W, et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol. 2012;13:753-60.
112. Wang W, Wyckoff JB, Goswami S, et al. Coordinated regulation of pathways for enhanced cell motility and chemotaxis is conserved in rat and mouse mammary tumors. Cancer Res. 2007;67:3505-11.
113. Wei S, Nandi S, Chitu V, et al. Functional overlap but differential expression of CSF-1 and IL-34 in their CSF-1 receptor-mediated regulation of myeloid cells. J Leukoc Biol. 2010;88:495-505.
114. Weidenbusch M, Anders HJ. Tissue microenvironments define and get reinforced by macrophage phenotypes in homeostasis or during inflammation, repair and fibrosis. J Innate Immun. 2012;4:463-77.
115. Wiktor-Jedrzejczak W, Bartocci A, Ferrante AWJ, et al. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci U S A. 1990;87:4828-32.
116. Wood W, Turmaine M, Weber R, et al. Mesenchymal cells engulf and clear apoptotic footplate cells in macrophageless PU.1 null mouse embryos. Development. 2000;127:5245-52.
117. Wyckoff J, Wang W, Lin EY, et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004;64:7022-9.
118. Wyckoff JB, Wang Y, Lin EY, et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 2007;67:2649-56.
119. Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013;496:445-55.
120. Xu J, Escamilla J, Mok S, et al. CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res. 2013;73:2782-94.
121. Xue J, Schmidt SV, Sander J, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity. 2014;40:274-88.
122. Yasuda H, Shima N, Nakagawa N, et al. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A. 1998;95:3597-602.
123. Yeung YG, Stanley ER. Proteomic approaches to the analysis of early events in colony-stimulating factor-1 signal transduction. Mol Cell Proteomics. 2003;2:1143-55.
124. Yona S, Kim KW, Wolf Y, et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 2013;38:79-91.
125. Yoshida H, Hayashi S, Kunisada T, et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 1990;345:442-4.
126. Yu W, Chen J, Xiong Y, Pixley FJ, Yeung YG, Stanley ER. Macrophage proliferation is regulated through CSF-1 receptor tyrosines 544, 559, and 807. J Biol Chem. 2012;287:13694-704.
127. Yu W, Chen J, Xiong Y, et al. CSF-1 receptor structure/function in MacCsf1r-/- macrophages: regulation of proliferation, differentiation, and morphology. Journal of Leukocyte Biology. 2008;84:852-63.