Deregulated ephrin-B2 signaling in mammary epithelial cells alters the stem cell compartment and interferes with the epithelial differentiation pathway

International Journal of Oncology

Volumn 40, Issue 2, 2012, Pages 357-369

  Kaenel, Philip ^a   Antonijevic, Milica ^a   Richter, Stefanie ^a   Küchler, Samuel ^a   Sutter, Nora ^a   Wotzkow, Carlos ^a   Strange, Robert ^a   Andres, Anne Catherine ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

CD49f CD24; Estrogen receptor; Mammary gland; Repopulation assay; Transgenic mice

Indexed keywords

EPHRIN B2; ESTROGEN RECEPTOR; MUTANT PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL CELL; BREAST EPITHELIUM; CARCINOGENESIS; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; LASER SCANNING CYTOMETRY; LUNG ALVEOLUS CELL; METASTASIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; STEM CELL; TRANSGENIC MOUSE;

ADIPOSE TISSUE; ANIMALS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL POLARITY; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; EPHRIN-B2; EPITHELIAL CELLS; FEMALE; HOMEOSTASIS; HUMANS; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHOPROTEINS; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELLS;

EID: 84855708539     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2011.1238     Document Type: Article

References (60)

1. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC and Dirks PB: Tumour initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Disc 8: 806-823, 2009.
2. Brisken C and Duss S: Stem cells and the stem cell niche in the breast: an integrated hormonal and developmental perspective. Stem Cell Rev 3: 147-156, 2007. (Pubitemid 350129717)
3. Kaenel P, Schwab C, Mulchi K, Wotzkow C and Andres AC: Preponderance of cells with stem cell characteristics in metastasising mouse mammary tumours induced by deregulated EphB4 and ephrin-B2 expression. Int J Oncol 38: 151-160, 2011.
4. Haldimann M, Custer D, Munarini N, Stirnimann C, Zurcher G, Rohrbach V, Djonov V, Ziemiecki A and Andres AC: Deregulated ephrin-B2 expression in the mammary gland interferes with the development of both the glandular epithelium and vasculature and promotes metastasis formation. Int J Oncol 35: 525-536, 2009.
5. Munarini N, Jager R, Abderhalden S, Zuercher G, Rohrbach V, Loercher S, Pfanner-Meyer B, Andres AC and Ziemiecki A: Altered mammary epithelial development, pattern formation and involution in transgenic mice expressing the EphB4 receptor tyrosine kinase. J Cell Sci 115: 25-37, 2002. (Pubitemid 34105526)
6. Sternlicht MD: Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Res 8: 201, 2006.
7. McDaniel SM, Rumer, KK, Biroc SL, Metz RP, Singh M, Porter W and Schedin P: Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathol 168: 608-620, 2006. (Pubitemid 43271158)
8. Howlin J, McBryan J and Martin F: Pubertal mammary gland development: insights from mouse models. J Mammary Gland Biol Neoplasia 11: 283-297, 2006. (Pubitemid 44869922)
9. Silberstein GB: Postnatal mammary gland morphogenesis. Microsc Res Tech 52: 155-162, 2001.
10. Kametani Y and Takeichi M: Basal-to-apical cadherin flow at cell junctions. Nat Cell Biol 9: 92-98, 2007. (Pubitemid 46024202)
11. Schwertfeger KL, Rosen JM and Cohen DA: Mammary gland macrophages: pleiotropic functions in mammary development. J Mammary Gland Biol Neoplasia 11: 229-238, 2006. (Pubitemid 44869918)
12. Dunbar ME and Wysolmerski JJ: Parathyroid hormone-related protein: a developmental regulatory molecule necessary for mammary gland development. J Mammary Gland Biol Neoplasia 4: 21-34, 1999.
13. Hens JR, Dann P, Zhang JP, Harris S, Robinson GW and Wysolmerski J: BMP4 and PTHrP interact to stimulate ductal outgrowth during embryonic mammary development and to inhibit hair follicle induction. Development 134: 1221-1230, 2007. (Pubitemid 46630089)
14. Chu EY, Hens J, Andl T, Kairo A, Yamaguchi TP, Brisken C, Glick A, Wysolmerski JJ and Millar SE: Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 131: 4819-4829, 2004. (Pubitemid 39433468)
15. Mailleux AA, Spencer-Dene B, Dillon C, Ndiaye D, Savona-Baron C, Itoh N, Kato S, Dickson C, Thiery JP and Bellusci S: Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development 129: 53-60, 1998.
16. Brisken C, Park S, Vass T, Lydon JP, O'Malley BW and Weinberg RA: A paracrine role for the epithelial progesterone receptor in mammary gland development. Proc Natl Acad Sci USA 95: 5076-5081, 1998. (Pubitemid 28208553)
17. Joshi PA, Jackson HW, Beristain AG, Di Grappa MA, Mote PA, Clarke CL, Stingl J, Waterhouse PD and Khokha R: Progesterone induces adult mammary stem cell expansion. Nature 465: 803-807, 2010.
18. Mallepell S, Krust A, Chambon P and Brisken C: Paracrine signaling through the epithelial estrogen receptor alpha is required for proliferation and morphogenesis in the mammary gland. Proc Natl Acad Sci USA 103: 2196-2201, 2006. (Pubitemid 43271646)
19. Brisken C, Heineman A, Chavarria T, Elenbaas B, Tan J, Dey SK, McMahon JA, McMahon AP and Weinberg RA: Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev 14: 650-654, 2000. (Pubitemid 30176819)
20. Cao Y, Bonizzi G, Seagroves TN, Greten FR, Johnson R, Schmidt EV and Karin M: IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107: 763-775, 2001. (Pubitemid 34033669)
21. Ciarloni L, Mallepell S and Brisken C: Amphiregulin is an essential mediator of estrogen receptor alpha function in mammary gland development. Proc Natl Acad Sci USA 104: 5455-5460, 2007. (Pubitemid 47175701)
22. Rudland PS, Platt-Higgins AM, Wilkinson MC and Fernig DG: Immunocytochemical identification of basic fibroblast growth factor in the developing rat mammary gland: variations in location are dependent on glandular structure and differentiation. J Histochem Cytochem 41: 887-898, 1993. (Pubitemid 23147729)
23. Hinck L and Silberstein GB: Key stages in mammary gland development: the mammary end bud as a motile organ. Breast Cancer Res 7: 245-251, 2005.
24. Muschler J and Streuli CH: Cell-matrix interactions in mammary gland development and breast cancer. Cold Spring Harb Perspect Biol 2: a003202, 2010.
25. Ewan KB, Shyamala G, Ravani SA, Tang Y, Akhurst R, Wakefield L and Barcellos-Hoff MH: Latent transforming growth factor-beta activation in mammary gland: regulation by ovarian hormones affects ductal and alveolar proliferation. Am J Pathol 160: 2081-2093, 2002. (Pubitemid 34663401)
26. Fata JE, Werb Z and Bissell MJ: Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res 6: 1-11, 2004. (Pubitemid 38195555)
27. Bruno RD and Smith GH: Functional characterization of stem cell activity in the mouse mammary gland. Stem Cell Rev 7: 238-247, 2011.
28. Visvader JE and Smith GH: Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harb Perspect Biol: doi: 10.1101/cshperspect.a004879, 2011.
29. Stingl J: Detection and analysis of mammary gland stem cells. J Pathol 217: 229-241, 2009.
30. Pasquale EB: Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer 10: 165-180, 2010.
31. Clevers H and Batlle E: EphB/EphrinB receptors and Wnt signaling in colorectal cancer. Cancer Res 66: 2-5, 2006. (Pubitemid 43165998)
32. Orsulic S and Kemler R: Expression of Eph receptors and ephrins is differentially regulated by E-cadherin. J Cell Sci 113: 1793-1802, 2000. (Pubitemid 30333128)
33. Cortina C, Palomo-Ponce S, Iglesias M, et al: EphB-ephrin-B interactions suppress colorectal cancer progression by compartmentalizing tumor cells. Nat Genet 39: 1376-1383, 2007. (Pubitemid 350034995)
34. Andres A-C and Ziemiecki A: Eph and ephrin signaling in mammary gland morphogenesis and cancer. J Mammary Gland Biol Neoplasia 8: 475-485, 2003. (Pubitemid 39137508)
35. Weiler S, Rohrbach V, Pulvirenti T, Adams R, Ziemiecki A and Andres AC: Mammary epithelial-specific knockout of the ephrin-B2 gene leads to precocious epithelial cell death at lactation. Dev Growth Differ 51: 809-819, 2009.
36. Deome KB, Faulkin LJ Jr, Bern HA and Blair PB: Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 19: 515-520, 1959.
37. McCaffrey LM and Macara IG: The Par3/aPKC interaction is essential for end bud remodeling and progenitor differentiation during mammary gland morphogenesis. Genes Dev 23: 1450.1460, 2009.
38. Sleeman KE, Kendrick H, Robertson D, Isacke CM, Ashworth A and Smalley MJ: Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol 176: 19-26, 2007. (Pubitemid 46041676)
39. Lee HS, Nishanian TG, Mood K, Bong YS and Daar IO: EphrinB1 controls cell-cell junctions through the Par polarity complex. Nat Cell Biol 10: 979-986, 2008.
40. Asselin-Labat ML, Vaillant F, Shackleton M, Bouras T, Lindeman GJ and Visvader JE: Delineating the epithelial hierarchy in the mouse mammary gland. Cold Spring Harb Symp Quant Biol 73: 469-478, 2008.
41. Boulanger CA and Smith GH: Reprogramming cell fates in the mammary microenvironment. Cell Cycle 8: 1127-1132, 2009.
42. Sleeman KE, Kendrick H, Ashworth A, Isacke CM and Smalley MJ: CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res 8: R7, 2006.
43. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI and Eaves CJ: Purification and unique properties of mammary epithelial stem cells. Nature 439: 993-997, 2006. (Pubitemid 43292419)
44. Vaillant F, Asselin-Labat ML, Shackleton M, Lindeman GJ and Visvader JE: The emerging picture of the mouse mammary stem cell. Stem Cell Rev 3: 114-123, 2007. (Pubitemid 350129714)
45. Visvader JE: Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 23: 2563-2577, 2009.
46. Battle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T and Clevers H: Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111: 251-263, 2002. (Pubitemid 35292445)
47. Picco V, Hudson C and Yasuo H: Ephrin-Eph signalling drives the asymmetric division of notochord/neural precursors in Ciona embryos. Development 134: 1491-1497, 2007. (Pubitemid 46746301)
48. Stokowski A, Shi S, Sun T, Bartold PM, Koblar SA and Gronthos S: EphB/ephrin-B interaction mediates adult stem cell attachment, spreading, and migration: implications for dental tissue repair. Stem Cells 25: 156-164, 2007. (Pubitemid 46052986)
49. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, Suda T and Matsuo K: Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 4: 111-121, 2006. (Pubitemid 44138718)
50. Faraldo MM, Teuliere J, Deugnier MA, Taddei-De La Hosseraye I, Thiery JP and Glukhova MA: Myoepithelial cells in the control of mammary development and tumorigenesis: data from genetically modified mice. J Mammary Gland Biol Neoplasia 10: 211-219, 2005.
51. Gudjonsson T, Ronnov-Jessen L, Villadsen R, Rank F, Bissell MJ and Petersen OW: Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J Cell Sci 115: 39-50, 2001. (Pubitemid 34105527)
52. Andrew DJ and Ewald AJ: Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration. Dev Biol 341: 34-55, 2010.
53. Lin D, Gish GD, Songyang Z and Pawson T: The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J Biol Chem 274: 3726-3733, 1999. (Pubitemid 29077220)
54. Dravis C and Henkemeyer M: Ephrin-B reverse signaling controls septation events at the embryonic midline through separate tyrosine phosphorylation- independent signaling avenues. Dev Biol 355: 138-151, 2011.
55. Nikolova Z, Djonov V, Zuercher G, Andres AC and Ziemiecki A: Cell-type specific and estrogen dependent expression of the receptor tyrosine kinase EphB4 and its ligand ephrin-B2 during mammary gland morphogenesis. J Cell Sci 111: 2741-2751, 1998. (Pubitemid 28479198)
56. Asselin-Labat ML, Vaillant F, Sheridan JM, Pal B, Wu D, Simpson ER, Yasuda H, Smyth GK, Martin TJ, Lindeman GJ and Visvader JE: Control of mammary stem cell function by steroid hormone signalling. Nature 465: 798-802, 2011.
57. Shoker BS, Jarvis C, Clarke RB, Anderson E, Hewlett J, Davies MP, Sibson DR and Sloane JP: Estrogen receptor-positive proliferating cells in the normal and precancerous breast. Am J Pathol 155: 1811-1815, 1999.
58. Shoker BS, Jarvis C, Sibson DR, Walker C and Sloane JP: Oestrogen receptor expression in the normal and pre-cancerous breast. J Pathol 188: 237-244, 1999. (Pubitemid 29317764)
59. Clarke RB, Howell A, Potten CS and Anderson E: Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res 57: 4987-4991, 1997. (Pubitemid 27498105)
60. Bissell MJ and Labarge MA: Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 7: 17-23, 2005. (Pubitemid 40126379)