Autocrine CSF-1R activation promotes Src-dependent disruption of mammary epithelial architecture

Journal of Cell Biology

Volumn 165, Issue 2, 2004, Pages 263-273

  Wrobel, Carolyn N ^a   Debnath, Jayanta ^a,b   Lin, Eva ^a   Beausoleil, Sean ^a   Roussel, Martine F ^c   Brugge, Joan S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Autocrine signaling; Cadherins; CSF 1 receptor; Mammary neoplasms; Src

Indexed keywords

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR 1 RECEPTOR; LIGAND; TYLOXAPOL; UNCLASSIFIED DRUG; UVOMORULIN;

ACINAR CELL; ARTICLE; AUTOCRINE EFFECT; BREAST EPITHELIUM; BREAST TUMOR; CANCER INVASION; CELL PROLIFERATION; COMPLEX FORMATION; CYTOARCHITECTURE; CYTOSKELETON; ENZYME ACTIVITY; EPITHELIUM CELL; EPITHELIUM TUMOR; HUMAN; HUMAN CELL; INFLAMMATORY CELL; INTERNALIZATION; PRIORITY JOURNAL; SRC HOMOLOGY DOMAIN;

AUTOCRINE COMMUNICATION; CADHERINS; CELL ADHESION; CELL LINE, TUMOR; CELL MEMBRANE; CELL SIZE; CYTOSKELETON; ENDOCYTOSIS; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; EPITHELIUM; FEMALE; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MAMMARY GLANDS, HUMAN; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SRC-FAMILY KINASES;

EID: 2142701427     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200309102     Document Type: Article

References (56)

1. Adams, C.L., and W.J. Nelson. 1998. Cytomechanics of cadherin-mediated cell-cell adhesion. Curr. Opin. Cell Biol. 10:572-577.
2. Adams, C.L., Y.T. Chen, S.J. Smith, and W.J. Nelson. 1998. Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J. Cell Biol. 142:1105-1119.
3. Alford, D., and J. Taylor-Papadimitriou. 1996. Cell adhesion molecules in the normal and cancerous mammary gland. J. Mammary Gland Biol. Neoplasia. 1:207-218.
4. Alonso, G., M. Koegl, N. Mazurenko, and S.A. Courtneidge. 1995. Sequence requirements for binding of Src family tyrosine kinases to activated growth factor receptors. J. Biol. Chem. 270:9840-9848.
5. Barcellos-Hoff, M.H., J. Aggeler, T.G. Ram, and M.J. Bissell. 1989. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 105:223-235.
6. Behrens, J., L. Vakaet, R. Friis, E. Winterhager, F. Van Roy, M.M. Mareel, and W. Birchmeier. 1993. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/β-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120:757-766.
7. Blake, R.A., P. Garcia-Paramio, P.J. Parker, and S.A. Courtneidge. 1999. Src promotes PKCdelta degradation. Cell Growth Differ. 10:231-241.
8. Blake, R.A., M.A. Broome, X. Liu, J. Wu, M. Gishizky, L. Sun, and S.A. Courtneidge. 2000. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol. Cell. Biol. 20:9018-9027.
9. Boterberg, T., K.M. Vennekens, M. Thienpont, M.M. Mareel, and M.E. Bracke. 2000. Internalization of the E-cadherin/catenin complex and scattering of human mammary carcinoma cells MCF-7/AZ after treatment with conditioned medium from human skin squamous carcinoma cells COLO 16. Cell Adhes. Commun. 7:299-310.
10. Braga, V.M., L.M. Machesky, A. Hall, and N.A. Hotchin. 1997. The small GTP-ases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 137:1421-1431.
11. Conacci-Sorrell, M., J. Zhurinsky, and A. Ben-Ze'ev. 2002. The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Invest. 109:987-991.
12. Dai, X.M., G.R. Ryan, A.J. Hapel, M.G. Dominguez, R.G. Russell, S. Kapp, V. Sylvestre, and E.R. Stanley. 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.
13. Debnath, J., K.R. Mills, N.L. Collins, M.J. Reginato, S.K. Muthuswamy, and J.S. Brugge. 2002. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell. 111:29-40.
14. Debnath, J., S.K. Muthuswamy, and J.S. Brugge. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 30:256-268.
15. Downing, J.R., and A.B. Reynolds. 1991. PDGF, CSF-1, and EGF induce tyrosine phosphorylation of p120, a pp60src transformation-associated substrate. Oncogene. 6:607-613.
16. Flick, M.B., E. Sapi, and B.M. Kacinski. 2002. Hormonal regulation of the c-fms proto-oncogene in breast cancer cells is mediated by a composite glucocorticoid response element. J. Cell. Biochem. 85:10-23.
17. Fujita, Y., G. Krause, M. Scheffner, D. Zechner, H.E. Leddy, J. Behrens, T. Sommer, and W. Birchmeier. 2002. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4:222-231.
18. Herrenknecht, K., M. Ozawa, C. Eckerskorn, F. Lottspeich, M. Lenter, and R. Kemler. 1991. The uvomorulin-anchorage protein alpha catenin is a vinculin homologue. Proc. Natl. Acad. Sci. USA. 88:9156-9160.
19. Ide, H., D.B. Seligson, S. Memarzadeh, L. Xin, S. Horvath, P. Dubey, M.B. Flick, B.M. Kacinski, A. Palotie, and O.N. Witte. 2002. Expression of colony-stimulating factor 1 receptor during prostate development and prostate cancer progression. Proc. Natl. Acad. Sci. USA. 99:14404-14409.
20. Iyer, A., T.E. Kmiecik, M. Park, I. Daar, D. Blair, K.J. Dunn, P. Sutrave, J.N. Ihle, M. Bodescot, and G.F. Vande Woude. 1990. Structure, tissue-specific expression, and transforming activity of the mouse met protooncogene. Cell Growth Differ. 1:87-95.
21. Kacinski, B.M. 1995. CSF-1 and its receptor in ovarian, endometrial and breast cancer. Ann. Med. 27:79-85.
22. Kacinski, B.M., K.A. Scata, D. Carter, L.D. Yee, E. Sapi, B.L. King, S.K. Chambers, M.A. Jones, M.H. Pirro, E.R. Stanley, and L.R. Rohrschneider. 1991. FMS (CSF-1 receptor) and CSF-1 transcripts and protein are expressed by human breast carcinomas in vivo and in vitro. Oncogene. 6:941-952.
23. Kowalski, P.J., M.A. Rubin, and C.G. Kleer. 2003. E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res. 5:R217-R222.
24. Langer, S.J., D.M. Bortner, M.F. Roussel, C.J. Sherr, and M.C. Ostrowski. 1992. Mitogenic signaling by colony-stimulating factor 1 and ras is suppressed by the ets-2 DNA-binding domain and restored by myc overexpression. Mol. Cell. Biol. 12:5355-5362.
25. Le, T.L., A.S. Yap, and J.L. Stow. 1999. Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146:219-232.
26. Le, T.L., S.R. Joseph, A.S. Yap, and J.L. Stow. 2002. Protein kinase C regulates endocytosis and recycling of E-cadherin. Am. J. Physiol. Cell Physiol. 283: C489-C499.
27. Lipsich, L.A., A.J. Lewis, and J.S. Brugge. 1983. Isolation of monoclonal antibodies that recognize the transforming proteins of avian sarcoma viruses. J. Virol. 48:352-360.
28. Marks, D.C., X.F. Csar, N.J. Wilson, U. Novak, A.C. Ward, V. Kanagasundarum, B.W. Hoffmann, and J.A. Hamilton. 1999. Expression of a Y559F mutant CSF-1 receptor in M1 myeloid cells: a role for Src kinases in CSF-1 receptor-mediated differentiation. Mol. Cell Biol. Res. Commun. 1:144-152.
29. McCrea, P.D., C.W. Turck, and B. Gumbiner. 1991. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science. 254:1359-1361.
30. Mukhopadhyay, D., L. Tsiokas, X.M. Zhou, D. Foster, J.S. Brugge, and V.P. Sukhatme. 1995. Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature. 375:577-581.
31. Muthuswamy, S.K., D. Li, S. Lelievre, M.J. Bissell, and J.S. Brugge. 2001. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 3:785-792.
32. Niemann, C., V. Brinkmann, E. Spitzer, G. Hartmann, M. Sachs, H. Naundorf, and W. Birchmeier. 1998. Reconstitution of mammary gland development in vitro: requirement of c-met and c-erbB2 signaling for branching and alveolar morphogenesis. J. Cell Biol. 143:533-545.
33. Nollet, F., G. Berx, and F. van Roy. 1999. The role of the E-cadherin/catenin adhesion complex in the development and progression of cancer. Mol. Cell Biol. Res. Commun. 2:77-85.
34. Owens, D.W., G.W. McLean, A.W. Wyke, C. Paraskeva, E.K. Parkinson, M.C. Frame, and V.G. Brunton. 2000. The catalytic activity of the Src family kinases is required to disrupt cadherin-dependent cell-cell contacts. Mol. Biol. Cell. 11:51-64.
35. Palacios, F., L. Price, J. Schweitzer, J.G. Collard, and C. D'Souza-Schorey. 2001. An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20:4973-4986.
36. Pollack, A.L., R.B. Runyan, and K.E. Mostov. 1998. Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev. Biol. 204:64-79.
37. Pollard, J.W., and L. Hennighausen. 1994. Colony stimulating factor 1 is required for mammary gland development during pregnancy. Proc. Natl. Acad. Sci. USA. 91:9312-9316.
38. Price, F.V., S.K. Chambers, J.T. Chambers, M.L. Carcangiu, P.E. Schwartz, E.I. Kohorn, E.R. Stanley, and B.M. Kacinski. 1993. Colony-stimulating factor-1 in primary ascites of ovarian cancer is a significant predictor of survival. Am. J. Obstet. Gynecol. 168:520-527.
39. Pujuguet, P., L. Del Maestro, A. Gautreau, D. Louvard, and M. Arpin. 2003. Ezrin regulates E-cadherin-dependent adherens junction assembly through Racl activation. Mol. Biol. Cell. 14:2181-2191.
40. Reynolds, A.B., D.J. Roesel, S.B. Kanner, and J.T. Parsons. 1989. Transformation-specific tyrosine phosphorylation of a novel cellular protein in chicken cells expressing oncogenic variants of the avian cellular src gene. Mol. Cell. Biol. 9:629-638.
41. Reynolds, A.B., J. Daniel, P.D. McCrea, M.J. Wheelock, J. Wu, and Z. Zhang. 1994. Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell. Biol. 14:8333-8342.
42. Roura, S., S. Miravet, J. Piedra, A. Garcia de Herreros, and M. Dunach. 1999. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J. Biol. Chem. 274:36734-36740.
43. Roussel, M.F. 1998. Key effectors of signal transduction and G1 progression. Adv. Cancer Res. 74:1-24.
44. Roussel, M.F., T.J. Dull, C.W. Rettenmier, P. Ralph, A. Ullrich, and C.J. Sherr. 1987. Transforming potential of the c-fms proto-oncogene (CSF-1 receptor). Nature. 325:549-552.
45. Roussel, M.F., J.R. Downing, C.W. Rettenmier, and C.J. Sherr. 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.
46. Sapi, E., M.B. Flick, S. Rodov, M. Gilmore-Hebert, M. Kelley, S. Rockwell, and B.M. Kacinski. 1996. Independent regulation of invasion and anchorage-independent growth by different autophosphorylation sites of the macrophage colony-stimulating factor 1 receptor. Cancer Res. 56:5704-5712.
47. Sapi, E., M.B. Flick, S. Rodov, D. Carter, and B.M. Kacinski. 1998a. Expression of CSF-I and CSF-I receptor by normal lactating mammary epithelial cells. J. Soc. Gynecol. Investig. 5:94-101.
48. Sapi, E., M.B. Flick, S. Rodov, and B.M. Kacinski. 1998b. Ets-2 transdominant mutant abolishes anchorage-independent growth and macrophage colony-stimulating factor-stimulated invasion by BT20 breast carcinoma cells. Cancer Res. 58:1027-1033.
49. Schmeichel, K.L., V.M. Weaver, and M.J. Bissell. 1998. Structural cues from the tissue microenvironment are essential determinants of the human mammary epithelial cell phenotype. J. Mammary Gland Biol. Neoplasia. 3:201-213.
50. Swift, S., J. Lorens, P. Achacoso, and G.P. Nolan. 1999. Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cell-based systems. In Current Protocols in Immunology. Unit 10.28 (Suppl. 31).
51. Takeda, H., A. Nagafuchi, S. Yonemura, S. Tsukita, J. Behrens, and W. Birchmeier. 1995. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J. Cell Biol. 131:1839-1847.
52. Van Nguyen, A., and J.W. Pollard. 2002. Colony stimulating factor-1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth. Dev. Biol. 247:11-25.
53. Warren, S.L., and W.J. Nelson. 1987. Nonmitogenic morphoregulatory action of pp60v-src on multicellular epithelial structures. Mol. Cell. Biol. 7:1326-1337.
54. Watabe, M., A. Nagafuchi, S. Tsukita, and M. Takeichi. 1994. Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line. J. Cell Biol. 127:247-256.
55. Wilhelmsen, K., S. Burkhalter, and P. van der Geer. 2002. C-Cbl binds the CSF-1 receptor at tyrosine 973, a novel phosphorylation site in the receptor's carboxy-terminus. Oncogene. 21:1079-1089.
56. Zhang, Q., J. Calafat, H. Janssen, and S. Greenberg. 1999. ARF6 is required for growth factor- and rac-mediated membrane ruffling in macrophages at a stage distal to rac membrane targeting. Mol. Cell. Biol. 19:8158-8168.