Fes tyrosine kinase expression in the tumor niche correlates with enhanced tumor growth, angiogenesis, circulating tumor cells, metastasis, and infiltrating macrophages

Cancer Research

Volumn 71, Issue 4, 2011, Pages 1465-1473

  Zhang, Shengnan ^a   Chitu, Violeta ^b   Stanley, E Richard ^b   Elliott, Bruce E ^a   Greer, Peter A ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE FES;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CARCINOGENESIS; CELL FUNCTION; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; VASCULAR ENDOTHELIUM;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; HUMANS; MACROPHAGES; MICE; MICE, KNOCKOUT; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-FES; STEM CELL NICHE; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 79951830119     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3757     Document Type: Article

References (47)

1. Greer P. Closing in on the biological functions of Fps/Fes and Fer. Nat Rev Mol Cell Biol 2002;3:278-89. (Pubitemid 34619263)
2. Smithgall TE, Rogers JA, Peters KL, Li J, Briggs SD, Lionberger JM, et al. The c-Fes family of protein-tyrosine kinases. Crit Rev Oncog 1998;9:43-62. (Pubitemid 28436457)
3. Haigh J, McVeigh J, Greer P. The fps/fes tyrosine kinase is expressed in myeloid, vascular endothelial, epithelial, and neuronal cells and is localized in the trans-golgi network. Cell Growth Differ 1996;7:931-44. (Pubitemid 26360733)
4. Truesdell PF, Zirngibl RA, Francis S, Sangrar W, Greer PA. fps/fes knockout mice display a lactation defect and the fps/fes tyrosine kinase is a component of E-cadherin-based adherens junctions in breast epithelial cells during lactation. Exp Cell Res 2009;315:2929-40.
5. Shibuya M, Hanafusa T, Hanafusa H, Stephenson JR. Homology exists among the transforming sequences of avian and feline sarcoma viruses. Proc Natl Acad Sci U S A 1980;77:6536-40. (Pubitemid 11219163)
6. Sherr CJ, Fedele LA, Oskarsson M, Maizel J, Woude GV. Molecular cloning of Snyder-Theilen feline leukemia and sarcoma viruses: comparative studies of feline sarcoma virus with its natural helper virus and with Moloney murine sarcoma virus. J Virol 1980;34:200-12. (Pubitemid 10149396)
7. Yee SP, Mock D, Greer P, Maltby V, Rossant J, Bernstein A, et al. Lymphoid and mesenchymal tumors in transgenic mice expressing the v-fps protein-tyrosine kinase. Mol Cell Biol 1989;9:5491-9. (Pubitemid 20004367)
8. Bardelli A, Parsons DW, Silliman N, Ptak J, Szabo S, Saha S, et al. Mutational analysis of the tyrosine kinome in colorectal cancers. Science 2003;300:949. (Pubitemid 36548874)
9. Sangrar W, Zirgnibl RA, Gao Y, Muller WJ, Jia Z, Greer PA. An identity crisis for fps/fes:oncogene or tumor suppressor?Cancer Res 2005;65:3518-22.
10. Shaffer JM, Smithgall TE. Promoter methylation blocks FES protein-tyrosine kinase gene expression in colorectal cancer. Genes Chromosomes Cancer 2009;48:272-84.
11. Greer P, Haigh J, Mbamalu G, Khoo W, Bernstein A, Pawson T. The Fps/Fes protein-tyrosine kinase promotes angiogenesis in transgenic mice. Mol Cell Biol 1994;14:6755-63. (Pubitemid 24299745)
12. Haigh JJ, Ema M, Haigh K, Gertsenstein M, Greer P, Rossant J, et al. Activated Fps/Fes partially rescues the in vivo developmental potential of Flk1-deficient vascular progenitor cells. Blood 2004;103:912-20. (Pubitemid 38129550)
13. Zirngibl RA, Senis Y, Greer PA. Enhanced endotoxin sensitivity in fps/ fes-null mice with minimal defects in hematopoietic homeostasis. Mol Cell Biol 2002;22:2472-86. (Pubitemid 34262970)
14. Parsons SA, Greer PA. The Fps/Fes kinase regulates the inflammatory response to endotoxin through down-regulation of TLR4, NF-kappaB activation, and TNF-alpha secretion in macrophages. J Leukoc Biol 2006;80:1522-8. (Pubitemid 44904991)
15. Elliott BE, Tam SP, Dexter D, Chen ZQ. Capacity of adipose tissue to promote growth and metastasis of a murine mammary carcinoma: effect of estrogen and progesterone. Int J Cancer 1992;51:416-24.
16. Senis Y, Zirngibl R, McVeigh J, Haman A, Hoang T, Greer PA. Targeted disruption of the murine fps/fes proto-oncogene reveals that Fps/Fes kinase activity is dispensable for hematopoiesis. Mol Cell Biol 1999;19:7436-46. (Pubitemid 29493407)
17. Ellis C, Moran M, McCormick F, Pawson T. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature 1990;343:377-81.
18. Udell CM, Samayawardhena LA, Kawakami Y, Kawakami T, Craig AW. Fer and Fps/Fes participate in a Lyn-dependent pathway from Fcep-silonRI to platelet-endothelial cell adhesion molecule 1 to limit mast cell activation. J Biol Chem 2006;281:20949-57. (Pubitemid 44115436)
19. Stanley ER. Murine bone marrow-derived macrophages. Methods Mol Biol 1997;75:301-4.
20. Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, Pixley FJ, 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. (Pubitemid 40827339)
21. Kanda S, Naba A, Miyata Y. Inhibition of endothelial cell chemotaxis toward FGF-2 by gefitinib associates with downregulation of Fes activity. Int J Oncol 2009;35:1305-12.
22. Kanda S, Kanetake H, Miyata Y. Downregulation of Fes inhibits VEGFA- induced chemotaxis and capillary-like morphogenesis by cultured endothelial cells. J Cell Mol Med 2007;11:495-501. (Pubitemid 47153459)
23. Sangrar W, Mewburn JD, Vincent SG, Fisher JT, Greer PA. Vascular defects in gain-of-function fps/fes transgenic mice correlate with PDGF- and VEGF-induced activation of mutant Fps/Fes kinase in endothelial cells. J Thromb Haemost 2004;2:820-32. (Pubitemid 40185720)
24. 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.
25. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
26. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007;117:1155-66. (Pubitemid 46718400)
27. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996;56:4625-9. (Pubitemid 26338061)
28. 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.
29. Aharinejad S, Abraham D, Paulus P, Abri H, Hofmann M, Grossschmidt K, et al. Colony-stimulating factor-1 antisense treatment suppresses growth of human tumor xenografts in mice. Cancer Res 2002;62:5317-24. (Pubitemid 35024608)
30. Aharinejad S, Paulus P, Sioud M, Hofmann M, Zins K, Schäfer R, 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. (Pubitemid 39006559)
31. Hernandez L, Smirnova T, Kedrin D, Wyckoff J, Zhu L, Stanley ER, et al. The EGF/CSF-1 paracrine invasion loop can be triggered by heregulin beta1 and CXCL12. Cancer Res 2009;69:3221-7.
32. Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, 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. (Pubitemid 39331012)
33. Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 2007;67:2649-56. (Pubitemid 46548952)
34. Senis YA, Sangrar W, Zirngibl RA, Craig AW, Lee DH, Greer PA. Fps/ Fes and Fer non-receptor protein-tyrosine kinases regulate collagen- and ADP-induced platelet aggregation. J Thromb Haemost 2003;1:1062-70.
35. Craig AW, Greer PA. Fer kinase is required for sustained p38 kinase activation and maximal chemotaxis of activated mast cells. Mol Cell Biol 2002;22:6363-74.
36. Smithgall TE, Yu G, Glazer RI. Identification of the differentiation- associated p93 tyrosine protein kinase of HL-60 leukemia cells as the product of the human c-fes locus and its expression in myelomono-cytic cells. J Biol Chem 1988;263:15050-5.
37. Condeelis J, Pollard JW. Macrophages:obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006;124:263-6. (Pubitemid 43121975)
38. 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.
39. Robinson BD, Sica GL, Liu YF, Rohan TE, Gertler FB, Condeelis JS, et al. Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination. Clin Cancer Res 2009;15:2433-41.
40. 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. (Pubitemid 44715100)
41. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005;7:211-7. (Pubitemid 40568680)
42. Kim J, Feldman RA. Activated Fes protein tyrosine kinase induces terminal macrophage differentiation of myeloid progenitors (U937 cells) and activation of the transcription factor PU.1. Mol Cell Biol 2002;22:1903-18. (Pubitemid 34175005)
43. Kim J, Ogata Y, Feldman RA. Fes tyrosine kinase promotes survival and terminal granulocyte differentiation of factor-dependent myeloid progenitors (32D) and activates lineage-specific transcription factors. J Biol Chem 2003;278:14978-84. (Pubitemid 36799829)
44. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009;27:451-83.
45. Izuhara K, Feldman RA, Greer P, Harada N. Interleukin-4 induces association of the c-fes proto-oncogene product with phosphatidylinositol- 3 kinase. Blood 1996;88:3910-8. (Pubitemid 26383115)
46. Jiang H, Foltenyi K, Kashiwada M, Donahue L, Vuong B, Hehn B, et al. Fes mediates the IL-4 activation of insulin receptor substrate-2 and cellular proliferation. J Immunol 2001;166:2627-34. (Pubitemid 32173501)
47. Parsons SA, Mewburn JD, Truesdell P, Greer PA. The Fps/Fes kinase regulates leucocyte recruitment and extravasation during inflammation. Immunology 2007;122:542-50. (Pubitemid 350075950)