Preponderance of cells with stem cell characteristics in metastasising mouse mammary tumours induced by deregulated EphB4 and ephrin-B2 expression

International Journal of Oncology

Volumn 38, Issue 1, 2011, Pages 151-160

  Kaenel, Philip ^a   Schwab, Caroline ^a   Mülchi, Kathrin ^a   Wotzkow, Carlos ^a   Andres, Anne Catherine ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Carcinogenesis; MMTV NeuT; Progenitor cells; Transgenic mice; Tumour initiating cells

Indexed keywords

ALPHA6 INTEGRIN; ATAXIN 1; CD24 ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYTOKERATIN 19; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; BREAST TUMOR; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; GENE OVEREXPRESSION; HOMEOSTASIS; METASTASIS; MOUSE; NONHUMAN; PARENCHYMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL GROWTH PROCESSES; EPHRIN-B2; FEMALE; IMMUNOHISTOCHEMISTRY; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; RECEPTOR, EPHB4;

EID: 78650943676     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo-00000834     Document Type: Article

References (60)

1. Stockler M, Wilcken NR, Ghersi D and Simes RJ: Systematic reviews of chemotherapy and endocrine therapy in metastatic breast cancer. Cancer Treat Rev 26: 151-168, 2000.
2. Micalizzi D, Farabaugh SM and Ford HL: Epithelial-mesenchymal transition in cancer: parallels between normal development and tumour progression. J Mamm Gland Biol Neoplasia 15: 117-134, 2010.
3. Kaplan RN, Psaila B and Lyden D: Bone marrow cells in the 'pre-metastatic niche': within bone and beyond. Cancer Metastasis Rev 25: 521-529, 2006.
4. Allan AL, Vantyghem SA, Tuck AB and Chambers AF: Tumor dormancy and cancer stem cells: implications for the biology and treatment of breast cancer metastasis. Breast Dis 26: 87-98, 2007.
5. Appelbaum FR, Rowe JM, Radich J and Dick JE: Acute myeloid leukaemia. Hematology (Am Soc Hematol Educ Program) 2001: 62-86, 2001.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988, 2003. (Pubitemid 36418143)
7. 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.
8. Jordan CT, Guzman ML and Noble M: Cancer stem cells. N Engl J Med 355: 1253-1261, 2006.
9. Wicha MS, Liu S and Dontu G: Cancer stem cells: an old idea - a paradigm shift. Cancer Res 66: 1883-1890, 2006.
10. Visvader JE: Keeping abreast of the mammary epithelial hierarchy and breast tumourigenesis. Genes Dev 23: 2563-2577, 2009.
11. Pasquale EB: Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer 10: 165-180, 2010.
12. Prevost N, Woulfe D, Tanaka T and Brass LF: Interactions between Eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-cell contact has occurred. Proc Natl Acad Sci USA 99: 9214-9224, 2002.
13. Suenobu S, Takakura N, Inada T, Yamada Y, Yuasa H, Zhang XQ, Sakakano S, Oike Y and Suda T: A role of the EphB4 receptor and its ligand ephrin-B2 in erythropoiesis. Biochem Biophys Res Com 293: 1124-1131, 2002. (Pubitemid 34694158)
14. Okubo T, Yanai N and Obinata M: Stromal cells modulate ephrin-B2 expression and transmigration of hematopoietic cells. Exp Hematol 34: 330-338, 2006.
15. Zhao C, Irie N, Takada Y, Shimoda K, Miyamoto T, Nishiwaki T, Suda T and Matsuo K: Bidirectional signalling controls bone homeostasis. Cell Metab 4: 111-121, 2006.
16. Munarini N, Jäger R, Abderhalden S, Zürcher G, Rohrbach V, Lörcher 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.
17. Haldimann M, Custer D, Stirnimann C, Munarini N, Weiler S, Zürcher G, Rohrbach V, Djonov V, Ziemiecki A and Andres AC: Deregulated ephrin-B2 expression interferes with the development of both the glandular epithelium and vasculature and promotes metastasis formation. Int J Oncol 35: 525-536, 2009.
18. Battle E, Henderson JT, Benghte H, van den Born MWM, Sancho E, Huls G, et al: ß-catenin and Tcf mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111: 251-263, 2002.
19. Lazarova P, Wu Q, Kvalheim G, Suo Z, Haakenstad KW, Metodiev K and Nesland JM: Growth factor receptors in hematopoietic stem cells: Eph family expression in CD34+ and CD133+ cell populations from mobilised peripheral blood. Int J Immunopathol Pharmacol 19: 49-56, 2006.
20. Stokowski A, Shi S, Sun T, Bartold PM, Koblar SA and Gronthos S: EphB/ephrinB interaction mediates adult stem cell attachment, spreading and migration: implications for dental tissue repair. Stem Cells 25: 156-164, 2007. (Pubitemid 46052986)
21. Picco V, Hudson C and Yassuo H: Ephrin-Eph signalling drives the asymmetric division of notochord/neural precursors in Ciona embryos. Development 134: 1491-1497, 2007.
22. Foubert P, Silvestre JS, Souttou B, Barateau V, Martin C, Ebrahimian TG, et al: PSGL-1 mediated activation of EphB4 increases the proangiogenic potential of endothelial progenitor cells. J Clin Invest 117: 1527-1537, 2007.
23. Pasquale EB: Eph-ephrin bidirectional signalling in physiology and disease. Cell 133: 38-52, 2008.
24. Takai N, Miyazaki T, Fujisawa K, Nasu K and Miyakawa I: Expression of receptor tyrosine kinase EphB4 and its ligand ephrin-B2 is associated with malignant potential in endometrial cancer. Oncol Rep 8: 567-573, 2001. (Pubitemid 33758456)
25. Liu W, Ahmad SA, Jung YD, Reinmuth N, Fan F, Bucana CD, and Ellis LM: Coexpression of ephrin-Bs and their receptors in colon carcinoma. Cancer 94: 934-949, 2002.
26. Sawai Y, Tamura S, Fukui K, Ito N, Imanaka K, Saeki A, Sakuda S, Kiso S and Matsuzawa Y: Expression of ephrin-B1 in hepatocellular carcinoma: possible involvement in neovascularisation. J Hepatol 39: 991-996, 2003.
27. Berclaz G, Altermatt HJ, Rohrbach V, Flütsch B, Djonov V, Ziemiecki A, et al: Loss of EphB4 receptor tyrosine kinse protein expression during carcinogenesis of the human breast. Oncol Rep 9: 25-30, 2002.
28. Wu Q, Suo Z, Risberg B, Karlsson MG, Villman K and Nesland JM: Expression of EphB2 and EphB4 in breast carcinoma. Pathol Oncol Res 10: 26-33, 2004. (Pubitemid 38506609)
29. Noren NK, Lu M, Freeman AL, Koolpe M and Pasquale EB: Interplay between EphB4 on tumor cells and vascular ephrin-B2 regulates tumor growth. Proc Natl Acad Sci USA 101: 5583-5588, 2004.
30. Noren NK, Foos G, Hauser CA and Pasquale EB: The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat Cell Biol 8: 815-825, 2006.
31. Martiny-Baron G, Korff T, Schaffner F, Esser N, Eggstein S, Marme D and Augustin HG: Inhibition of tumor growth and angiogenesis by soluble EphB4. Neoplasia 6: 248-257, 2004. (Pubitemid 38657081)
32. Kumar SR, Singh J, Xia G, Krasnoperov V, Hassanieh L, Ley EJ, et al: Receptor tyrosine kinase EphB4 is a survival factor in breast cancer. Am J Pathol 169: 279-293, 2006.
33. Masood R, Kumar SR, Sinha UK, Crowe DL, Krasnoperov V, Reddy RK, et al: EphB4 provides survival advantage to squamous cell carcinoma of head and neck. Int J Cancer 119: 1236-1248, 2006.
34. Davalos V, Dopeso H, Castano J, Wilson AJ, Vilardell F, Romero-Gimenez J, et al: EphB4 and survival of colorectal cancer patients. Cancer Res 66: 8943-8948, 2006.
35. Kumar SR, Scehnet JS, Ley EJ, Krasnoperov V, Manchanda PK, Ladner RD, et al: Preferential induction of EphB4 over EphB2 and its implication in colorectal cancer. Cancer Res 69: 3736-3745, 2009.
36. Dopeso H, Mateo-Lozano S, Mazzolini R, Rodrigues P, Lagares-Tena L, Ceron J, et al: The receptor tyrosine kinase EphB4 has tumour suppressor activities in intestinal tumorigenesis. Cancer Res 69: 7430-7438, 2009.
37. Nikolova Z, Djonov V, Zürcher 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)
38. Abbas T and Dutta A: p21 in cancer: intricate network and multiple activities. Nat Rev Cancer 9: 400-414, 2009.
39. Stingl J: Detection and analysis of mammary stem cells. J Pathol 217: 229-241, 2009.
40. Grange C, Lanzardo S, Cavallo F, Camussi G and Bussolati B: Sca-1 identifies the tumour-initiating cells in mammary tumours of balb-neuT transgenic mice. Neoplasia 10: 1433-1443, 2008.
41. Smith GH: Stem cells, hormones and mammary cancer. Adv Exp Med Biol 617: 69-78, 2008.
42. Booth BW and Smith GH: Estrogen receptor-α and progesterone receptor are expressed in label-retaining mammary epithelial cells that divide asymmetrically and retain their template DNA. Breast Cancer Res 8: R49, 2006.
43. Lim SC: CD24 and human carcinoma: tumour biological aspects. Biomed Pharmacother 59: 5351-5354, 2005.
44. Cremers N, Deugnier MA and Sleeman J: Loss of CD24 expression promotes ductal branching in the murine mammary gland. Cell Mol Life Sci 67: 2311-2322, 2010.
45. Kristiansen KJ, Winzer E, Mayordomo J, et al: CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res 9: 4906-4913, 2003.
46. Baumann P, Cremers N, Kroese F, Orend G, Chiquet- Ehrismann R, Uede T, Yagita H and Sleeman J: CD24 expression causes the acquisition of multiple cellular properties associated with tumour growth and metastasis. Cancer Res 65: 10783-10793, 2005.
47. Runz S, Mierke CT, Joumaa S, Behrens J, Fabry B and Altevogt P: CD24 induces localization of β1 integrin to lipid rafts. Biochem Biophys Res Comm 365: 35-41, 2007.
48. Friedrichs K, Ruiz P, Franke F, Gille I, Terpe HJ and Imhof BA: High expression level of α6 integrin in human breast carcinoma is correlated with reduced survival. Cancer Res 55: 901-906, 1995.
49. hi defines xenograft-initiating cells in estrogen receptor-negative breast cancer. Cancer Res 70: 4624-4633, 2010.
50. Mercurio AM, Bachelder RE, Chung J, O'Connor KL, Rabinovitz I, Shaw LM and Tani T: Integrin laminin receptors and breast carcinoma progression. J Mamm Gland Biol Neoplasia 6: 299-309, 2001. (Pubitemid 39600489)
51. Rabinovitz I and Mercurio AM: The integrin α6β4 fiuctions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures. J Cell Biol 139: 1873-1884, 1997.
52. Hollier BG, Evans K and Mani SA: The epithelial-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. J Mamm Gland Biol Neoplasia 14: 29-43, 2009.
53. waf/Cip1 functions as a suppressor of malignant skin tumour formation and a determinant of keratinocyte stem cell potential. Proc Natl Acad Sci USA 96: 9089-9094, 1999.
54. waf. Science 287: 1804-1808, 2000.
55. Kippin TE, Martens DJ and van der Kooy D: p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferative capacity. Genes Dev 19: 756-767, 2005.
56. waf/Cip1/Sdi1: association with cell senescence and tumour-promoting activities of stromal fibroblasts. Cancer Lett 179: 1-14, 2002.
57. Cip promotes cyclin D1 nuclear accumulation via direct inhibition of nuclear export. J Biol Chem 277: 8517-8523, 2002.
58. Merlos-Suarez A and Batlle E: Eph-ephrin signalling in adult tissues and cancer. Curr Opin Cell Biol 20: 194-200, 2008.
59. Morel AP, Lièvre M, Thomas C, Hinkal G, Ansieau S and Puisieux A: Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLOS One 3: E2888, 2008.
60. Andres AC and Ziemiecki A: Eph and ephrin signalling in mammary gland morphogenesis and cancer. J Mamm Gland Biol Neopl 8: 475-486, 2003.