Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor

Cancer Research

Volumn 69, Issue 24, 2009, Pages 9498-9506

  Patsialou, Antonia ^a   Wyckoff, Jeffrey ^a   Wang, Yarong ^a   Goswami, Sumanta ^b   Stanley, E Richard ^a   Condeelis, John S ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b YESHIVA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; BREAST CANCER; CANCER INVASION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCID MOUSE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, SCID; NEOPLASM INVASIVENESS; RATS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS;

EID: 73649122504     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-1868     Document Type: Article

References (40)

1. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006;124:263-6.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. Paulus P, Stanley ER, Schafer R, Abraham D, Aharinejad S. Colony-stimulating factor-1 antibody reverses chemo-resistance in human MCF-7 breast cancer xenografts. Cancer Res 2006;66:4349-56.
8. Kacinski BM, Carter D, Mittal K, et al. High level expression of fms proto-oncogene mRNA is observed in clinically aggressive human endometrial adenocarcinomas. Int J Radiat Oncol Biol Phys 1988;15:823-9.
9. Kacinski BM, Carter D, Mittal K, et al. Ovarian adenocarcinomas express fms-complementary transcripts and fms antigen, often with coexpression of CSF-1. Am J Pathol 1990;137:135-47.
10. Kacinski BM, Scata KA, Carter D, et al. FMS (CSF-1 receptor) and CSF-1 transcripts and protein are expressed by human breast carcinomas in vivo and in vitro. Oncogene 1991;6:941-52.
11. Ide H, Seligson DB, Memarzadeh S, et al. Expression of colony-stimulating factor 1 receptor during prostate development and prostate cancer progression. Proc Natl Acad Sci U S A 2002;99:14404-9.
12. Kacinski BM, Chambers SK, Stanley ER, et al. The cytokine CSF-1 (M-CSF) expressed by endometrial carcinomas in vivo and in vitro, may also be a circulating tumor marker of neoplastic disease activity in endometrial carcinoma patients. Int J Radiat Oncol Biol Phys 1990;19:619-26.
13. 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.
14. Kacinski BM. CSF-1 and its receptor in breast carcinomas and neoplasms of the female reproductive tract. Mol Reprod Dev 1997;46:71-4.
15. Kacinski BM, Stanley ER, Carter D, et al. Circulating levels of CSF-1 (M-CSF) a lymphohematopoietic cytokine may be a useful marker of disease status in patients with malignant ovarian neoplasms. Int J Radiat Oncol Biol Phys 1989;17:159-64.
16. 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.
17. Smith HO, Anderson PS, Kuo DY, et al. The role of colony-stimulating factor 1 and its receptor in the etiopathogenesis of endometrial adenocarcinoma. Clin Cancer Res 1995;1:313-25.
18. Filderman AE, Bruckner A, Kacinski BM, Deng N, Remold HG. Macrophage colony-stimulating factor (CSF-1) enhances invasiveness in CSF-1 receptorpositive carcinoma cell lines. Cancer Res 1992;52: 3661-6.
19. Sapi E, Flick MB, Rodov S, et al. Independent regulation of invasion and anchorage-independent growth by different autophosphorylation sites of the macrophage colony-stimulating factor 1 receptor. Cancer Res 1996; 56:5704-12.
20. Wrobel CN, Debnath J, Lin E, Beausoleil S, Roussel MF, Brugge JS. Autocrine CSF-1R activation promotes Src-dependent disruption of mammary epithelial architecture. J Cell Biol 2004;165:263-73.
21. Flick MB, Sapi E, Kacinski BM. Hormonal regulation of the c-fms proto-oncogene in breast cancer cells is mediated by a composite glucocorticoid response element. J Cell Biochem 2002;85:10-23.
22. Brenton JD, Carey LA, Ahmed AA, Caldas C. Molecular classification and molecular forecasting of breast cancer: ready for clinical application? J Clin Oncol 2005;23:7350-60.
23. Morgan C, Pollard JW, Stanley ER. Isolation and characterization of a cloned growth factor dependent macrophage cell line, BAC1.2F5. J Cell Physiol 1987; 130:420-7.
24. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
25. Wyckoff JB, Segall JE, Condeelis JS. The collection of the motile population of cells from a living tumor. Cancer Res 2000;60:5401-4.
26. Sudo T, Nishikawa S, Ogawa M, et al. Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M. Oncogene 1995;11:2469-76.
27. Austyn JM, Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 1981;11:805-15.
28. Wang W, Wyckoff JB, Wang Y, Bottinger EP, Segall JE, Condeelis JS. Gene expression analysis on small numbers of invasive cells collected by chemotaxis from primary mammary tumors of the mouse. BMC Biotechnol 2003;3:13.
29. Wang W, Goswami S, Lapidus K, et al. Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res 2004;64:8585-94.
30. Das SK, Stanley ER, Guilbert LJ, Forman LW. Human colony-stimulating factor (CSF-1) radioimmunoassay: resolution of three subclasses of human colony-stimulating factors. Blood 1981;58:630-41.
31. Inaba T, Ishibashi S, Harada K, et al. Synergistic effects of transforming growth factor-β on the expression of c-fms, macrophage colony-stimulating factor receptor gene, in vascular smooth muscle cells. FEBS Lett 1996;399:207-10.
32. Kirma N, Hammes LS, Liu YG, et al. Elevated expression of the oncogene c-fms and its ligand, the macrophage colony-stimulating factor-1, in cervical cancer and the role of transforming growth factor-β1 in inducing c-fms expression. Cancer Res 2007;67: 1918-26.
33. Farina AR, Coppa A, Tiberio A, et al. Transforming growth factor-β1 enhances the invasiveness of human MDA-MB-231 breast cancer cells by up-regulating urokinase activity. Int J Cancer 1998;75:721-30.
34. Yang L, Moses HL. Transforming growth factor β: tumor suppressor or promoter? Are host immune cells the answer? Cancer Res 2008;68:9107-11.
35. Massague J. TGFβ in cancer. Cell 2008;134:215-30.
36. Halder SK, Beauchamp RD, Datta PK. A specific inhibitor of TGF-β receptor kinase, SB-431542, as a potent anti-tumor agent for human cancers. Neoplasia 2005;7:509-21.
37. 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.
38. 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.
39. Yang L, Huang J, Ren X, et al. Abrogation of TGF β signaling in mammary carcinomas recruits Gr-1+CD11b+myeloid cells that promote metastasis. Cancer Cell 2008; 13:23-35.
40. Dalal BI, Keown PA, Greenberg AH. Immunocyto-chemical localization of secreted transforming growth factor-β1 to the advancing edges of primary tumors and to lymph node metastases of human mammary carcinoma. Am J Pathol 1993;143:381-9.