Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis

Cancer Cell

Volumn 10, Issue 5, 2006, Pages 437-449

  Derksen, Patrick W B ^a   Liu, Xiaoling ^a   Saridin, Francis ^a   van der Gulden, Hanneke ^a   Zevenhoven, John ^a   Evers, Bastiaan ^a   van Beijnum, Judy R ^c   Griffioen, Arjan W ^c   Vink, Jacqueline ^a   Krimpenfort, Paul ^a   Peterse, Johannes L ^a   Cardiff, Robert D ^b   Berns, Anton ^a   Jonkers, Jos ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

CELLCYCLE

Indexed keywords

PROTEIN P53; UVOMORULIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOIKIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST CARCINOMA; CANCER INVASION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM; GENE MUTATION; KNOCKOUT GENE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; VASCULAR TUMOR;

EID: 33750614651     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2006.09.013     Document Type: Article

References (58)

1. Adams D.J., and Bradley A. Induced mitotic recombination: A switch in time. Nat. Genet. 30 (2002) 6-7
2. Althuis M.D., Dozier J.M., Anderson W.F., Devesa S.S., and Brinton L.A. Global trends in breast cancer incidence and mortality 1973-1997. Int. J. Epidemiol. 34 (2005) 405-412
3. Arpino G., Bardou V.J., Clark G.M., and Elledge R.M. Infiltrating lobular carcinoma of the breast: Tumor characteristics and clinical outcome. Breast Cancer Res. 6 (2004) R149-R156
4. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., and Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2 (2000) 84-89
5. Bernards R., and Weinberg R.A. A progression puzzle. Nature 418 (2002) 823
6. Berx G., and van Roy F. The E-cadherin/catenin complex: An important gatekeeper in breast cancer tumorigenesis and malignant progression. Breast Cancer Res. 3 (2001) 289-293
7. Berx G., Cleton-Jansen A.M., Nollet F., de Leeuw W.J., van de Vijver M., Cornelisse C., and van Roy F. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 14 (1995) 6107-6115
8. Berx G., Becker K.F., Hofler H., and van Roy F. Mutations of the human E-cadherin (CDH1) gene. Hum. Mutat. 12 (1998) 226-237
9. Boussadia O., Kutsch S., Hierholzer A., Delmas V., and Kemler R. E-cadherin is a survival factor for the lactating mouse mammary gland. Mech. Dev. 115 (2002) 53-62
10. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., and Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2 (2000) 76-83
11. Cavallaro U., and Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat. Rev. Cancer 4 (2004) 118-132
12. Cleton-Jansen A.M., Moerland E.W., Kuipers-Dijkshoorn N.J., Callen D.F., Sutherland G.R., Hansen B., Devilee P., and Cornelisse C.J. At least two different regions are involved in allelic imbalance on chromosome arm 16q in breast cancer. Genes Chromosomes Cancer 9 (1994) 101-107
13. Comijn J., Berx G., Vermassen P., Verschueren K., van Grunsven L., Bruyneel E., Mareel M., Huylebroeck D., and van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7 (2001) 1267-1278
14. Conacci-Sorrell M., Zhurinsky J., and Ben Ze'ev A. The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Invest. 109 (2002) 987-991
15. Coradini D., Pellizzaro C., Veneroni S., Ventura L., and Daidone M.G. Infiltrating ductal and lobular breast carcinomas are characterised by different interrelationships among markers related to angiogenesis and hormone dependence. Br. J. Cancer 87 (2002) 1105-1111
16. Derksen P.W., de Gorter D.J., Meijer H.P., Bende R.J., van Dijk M., Lokhorst H.M., Bloem A.C., Spaargaren M., and Pals S.T. The hepatocyte growth factor/Met pathway controls proliferation and apoptosis in multiple myeloma. Leukemia 17 (2003) 764-774
17. Drubin D.G., and Nelson W.J. Origins of cell polarity. Cell 84 (1996) 335-344
18. Dull T., Zufferey R., Kelly M., Mandel R.J., Nguyen M., Trono D., and Naldini L. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72 (1998) 8463-8471
19. Frixen U.H., Behrens J., Sachs M., Eberle G., Voss B., Warda A., Lochner D., and Birchmeier W. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J. Cell Biol. 113 (1991) 173-185
20. Fujita N., Jaye D.L., Kajita M., Geigerman C., Moreno C.S., and Wade P.A. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113 (2003) 207-219
21. -/- mice: Functional inactivation of p53 in developing T cells. Blood 104 (2004) 3886-3893
22. Graff J.R., Herman J.G., Lapidus R.G., Chopra H., Xu R., Jarrard D.F., Isaacs W.B., Pitha P.M., Davidson N.E., and Baylin S.B. E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res. 55 (1995) 5195-5199
23. Hajra K.M., Chen D.Y., and Fearon E.R. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 62 (2002) 1613-1618
24. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
25. Hulsken J., Birchmeier W., and Behrens J. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J. Cell Biol. 127 (1994) 2061-2069
26. Jonkers J., Meuwissen R., Van Der Gulden H., Peterse H., van der Valk M., and Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29 (2001) 418-425
27. Korkola J.E., DeVries S., Fridlyand J., Hwang E.S., Estep A.L., Chen Y.Y., Chew K.L., Dairkee S.H., Jensen R.M., and Waldman F.M. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 63 (2003) 7167-7175
28. Lehr H.A., Folpe A., Yaziji H., Kommoss F., and Gown A.M. Cytokeratin 8 immunostaining pattern and E-cadherin expression distinguish lobular from ductal breast carcinoma. Am. J. Clin. Pathol. 114 (2000) 190-196
29. Marchetti A., Buttitta F., Pellegrini S., Campani D., Diella F., Cecchetti D., Callahan R., and Bistocchi M. p53 mutations and histological type of invasive breast carcinoma. Cancer Res. 53 (1993) 4665-4669
30. Miyoshi H., Blomer U., Takahashi M., Gage F.H., and Verma I.M. Development of a self-inactivating lentivirus vector. J. Virol. 72 (1998) 8150-8157
31. Mohsin S.K., O'Connell P., Allred D.C., and Libby A.L. Biomarker profile and genetic abnormalities in lobular carcinoma in situ. Breast Cancer Res. Treat. 90 (2005) 249-256
32. Moody S.E., Perez D., Pan T.C., Sarkisian C.J., Portocarrero C.P., Sterner C.J., Notorfrancesco K.L., Cardiff R.D., and Chodosh L.A. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8 (2005) 197-209
33. Nandi S., Guzman R.C., and Yang J. Hormones and mammary carcinogenesis in mice, rats, and humans: A unifying hypothesis. Proc. Natl. Acad. Sci. USA 92 (1995) 3650-3657
34. Oda T., Kanai Y., Oyama T., Yoshiura K., Shimoyama Y., Birchmeier W., Sugimura T., and Hirohashi S. E-cadherin gene mutations in human gastric carcinoma cell lines. Proc. Natl. Acad. Sci. USA 91 (1994) 1858-1862
35. Perez-Moreno M., Jamora C., and Fuchs E. Sticky business: Orchestrating cellular signals at adherens junctions. Cell 112 (2003) 535-548
36. Perl A.K., Wilgenbus P., Dahl U., Semb H., and Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392 (1998) 190-193
37. Robanus-Maandag E., Dekker M., van der Valk M., Carrozza M.L., Jeanny J.C., Dannenberg J.H., Berns A., and te Riele H. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev. 12 (1998) 1599-1609
38. Rosen P.P., Lesser M.L., Arroyo C.D., Cranor M., Borgen P., and Norton L. p53 in node-negative breast carcinoma: An immunohistochemical study of epidemiologic risk factors, histologic features, and prognosis. J. Clin. Oncol. 13 (1995) 821-830
39. Savagner P., Yamada K.M., and Thiery J.P. The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J. Cell Biol. 137 (1997) 1403-1419
40. Shackleton M., Vaillant F., Simpson K.J., Stingl J., Smyth G.K., Asselin-Labat M.L., Wu L., Lindeman G.J., and Visvader J.E. Generation of a functional mammary gland from a single stem cell. Nature 439 (2006) 84-88
41. Simpson P.T., Gale T., Fulford L.G., Reis-Filho J.S., and Lakhani S.R. The diagnosis and management of pre-invasive breast disease: Pathology of atypical lobular hyperplasia and lobular carcinoma in situ. Breast Cancer Res. 5 (2003) 258-262
42. Smalley M., and Ashworth A. Stem cells and breast cancer: A field in transit. Nat. Rev. Cancer 3 (2003) 832-844
43. Soslow R.A., Carlson D.L., Horenstein M.G., and Osborne M.P. A comparison of cell cycle markers in well-differentiated lobular and ductal carcinomas. Breast Cancer Res. Treat. 61 (2000) 161-170
44. Stange D.E., Radlwimmer B., Schubert F., Traub F., Pich A., Toedt G., Mendrzyk F., Lehmann U., Eils R., Kreipe H., and Lichter P. High-resolution genomic profiling reveals association of chromosomal aberrations on 1q and 16p with histologic and genetic subgroups of invasive breast cancer. Clin. Cancer Res. 12 (2006) 345-352
45. Stingl J., Eirew P., Ricketson I., Shackleton M., Vaillant F., Choi D., Li H.I., and Eaves C.J. Purification and unique properties of mammary epithelial stem cells. Nature 439 (2006) 993-997
46. Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7 (1995) 619-627
47. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2 (2002) 442-454
48. Tinkle C.L., Lechler T., Pasolli H.A., and Fuchs E. Conditional targeting of E-cadherin in skin: Insights into hyperproliferative and degenerative responses. Proc. Natl. Acad. Sci. USA 101 (2004) 552-557
49. Tunggal J.A., Helfrich I., Schmitz A., Schwarz H., Gunzel D., Fromm M., Kemler R., Krieg T., and Niessen C.M. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J. 24 (2005) 1146-1156
50. Van 't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., Peterse H.L., van der Kooy K., Marton M.J., Witteveen A.T., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415 (2002) 530-536
51. Vleminckx K., Vakaet Jr. L., Mareel M., Fiers W., and van Roy F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66 (1991) 107-119
52. Vos C.B., Cleton-Jansen A.M., Berx G., de Leeuw W.J., ter Haar N.T., van Roy F., Cornelisse C.J., Peterse J.L., and van de Vijver M.J. E-cadherin inactivation in lobular carcinoma in situ of the breast: An early event in tumorigenesis. Br. J. Cancer 76 (1997) 1131-1133
53. Wellings S.R. Development of human breast cancer. Adv. Cancer Res. 31 (1980) 287-314
54. Wellings S.R., Jensen H.M., and Marcum R.G. An atlas of subgross pathology of the human breast with special reference to possible precancerous lesions. J. Natl. Cancer Inst. 55 (1975) 231-273
55. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., and Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117 (2004) 927-939
56. Yoshiura K., Kanai Y., Ochiai A., Shimoyama Y., Sugimura T., and Hirohashi S. Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc. Natl. Acad. Sci. USA 92 (1995) 7416-7419
57. Young P., Boussadia O., Halfter H., Grose R., Berger P., Leone D.P., Robenek H., Charnay P., Kemler R., and Suter U. E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles. EMBO J. 22 (2003) 5723-5733
58. Zhao H., Langerod A., Ji Y., Nowels K.W., Nesland J.M., Tibshirani R., Bukholm I.K., Karesen R., Botstein D., Borresen-Dale A.L., and Jeffrey S.S. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol. Biol. Cell 15 (2004) 2523-2536