Combined Wnt/β-Catenin, Met, and CXCL12/CXCR4 Signals Characterize Basal Breast Cancer and Predict Disease Outcome

Cell Reports

Volumn 5, Issue 5, 2013, Pages 1214-1227

  Holland, JaneD ^a   Györffy, Balázs ^b,c   Vogel, Regina ^a   Eckert, Klaus ^d   Valenti, Giovanni ^a   Fang, Liang ^a   Lohneis, Philipp ^c   Elezkurtaj, Sefer ^c   Ziebold, Ulrike ^a   Birchmeier, Walter ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d Experimental Pharmacology and Oncology GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CHEMOKINE RECEPTOR CXCR4; ESTROGEN RECEPTOR; SCATTER FACTOR RECEPTOR; STROMAL CELL DERIVED FACTOR 1; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER PROGNOSIS; CANCER RESISTANCE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; CXCR4 GENE; DRUG TARGETING; GENE; MET 322 GENE; MOLECULAR THERAPY; MOUSE; MOUSE MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; WNT GENE; WNT SIGNALING PATHWAY;

MUS;

ANIMALS; BETA CATENIN; BREAST NEOPLASMS; CHEMOKINE CXCL12; FEMALE; GENETIC THERAPY; HEPATOCYTE GROWTH FACTOR; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MIDDLE AGED; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-MET; RECEPTORS, CXCR4; TUMOR MARKERS, BIOLOGICAL; WNT SIGNALING PATHWAY;

EID: 84890140894     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.11.001     Document Type: Article

References (63)

1. Bouwman P., Aly A., Escandell J.M., Pieterse M., Bartkova J., van der Gulden H., Hiddingh S., Thanasoula M., Kulkarni A., Yang Q., et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 2010, 17:688-695.
2. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. Cancer Genome Atlas Network.
3. Carey L.A., Perou C.M., Livasy C.A., Dressler L.G., Cowan D., Conway K., Karaca G., Troester M.A., Tse C.K., Edmiston S., et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006, 295:2492-2502.
4. Carey L., Winer E., Viale G., Cameron D., Gianni L. Triple-negative breast cancer: disease entity or title of convenience?. Nat Rev Clin Oncol 2010, 7:683-692.
5. Christensen J.G., Schreck R., Burrows J., Kuruganti P., Chan E., Le P., Chen J., Wang X., Ruslim L., Blake R., et al. A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes invitro and exhibits cytoreductive antitumor activity invivo. Cancer Res. 2003, 63:7345-7355.
6. Clevers H. The cancer stem cell: premises, promises and challenges. Nat. Med. 2011, 17:313-319.
7. Deome K.B., Faulkin L.J., Bern H.A., Blair P.B. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 1959, 19:515-520.
8. DiMeo T.A., Anderson K., Phadke P., Fan C., Perou C.M., Naber S., Kuperwasser C. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 2009, 69:5364-5373.
9. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., Wicha M.S. Invitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003, 17:1253-1270.
10. Emami K.H., Nguyen C., Ma H., Kim D.H., Jeong K.W., Eguchi M., Moon R.T., Teo J.L., Kim H.Y., Moon S.H., et al. A small molecule inhibitor ofbeta-catenin/CREB-binding protein transcription [corrected]. Proc. Natl. Acad. Sci. USA 2004, 101:12682-12687.
11. Foulkes W.D., Stefansson I.M., Chappuis P.O., Bégin L.R., Goffin J.R., Wong N., Trudel M., Akslen L.A. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J.Natl. Cancer Inst. 2003, 95:1482-1485.
12. Gallego M.I., Bierie B., Hennighausen L. Targeted expression of HGF/SF in mouse mammary epithelium leads to metastatic adenosquamous carcinomas through the activation of multiple signal transduction pathways. Oncogene 2003, 22:8498-8508.
13. Garcia S., Dalès J.P., Charafe-Jauffret E., Carpentier-Meunier S., Andrac-Meyer L., Jacquemier J., Andonian C., Lavaut M.N., Allasia C., Bonnier P., Charpin C. Poor prognosis in breast carcinomas correlates with increased expression of targetable CD146 and c-Met and with proteomic basal-like phenotype. Hum. Pathol. 2007, 38:830-841.
14. Gastaldi S., Comoglio P.M., Trusolino L. The Met oncogene andbasal-like breast cancer: another culprit to watch out for?. Breast Cancer Res. 2010, 12:208.
15. Geyer F.C., Lacroix-Triki M., Savage K., Arnedos M., Lambros M.B., MacKay A., Natrajan R., Reis-Filho J.S. β-Catenin pathway activation in breast cancer is associated with triple-negative phenotype but not with CTNNB1 mutation. Mod. Pathol. 2011, 24:209-231.
16. Gherardi E., Birchmeier W., Birchmeier C., Vande Woude G. Targeting MET in cancer: rationale and progress. Nat. Rev. Cancer 2012, 12:89-103.
17. Graveel C.R., DeGroot J.D., Su Y., Koeman J., Dykema K., Leung S., Snider J., Davies S.R., Swiatek P.J., Cottingham S., et al. Met induces diverse mammary carcinomas in mice and is associated with human basal breast cancer. Proc. Natl. Acad. Sci. USA 2009, 106:12909-12914.
18. Györffy B., Schäfer R. Meta-analysis of gene expression profiles related to relapse-free survival in 1,079 breast cancer patients. Breast Cancer Res. Treat. 2009, 118:433-441.
19. Harada N., Tamai Y., Ishikawa T., Sauer B., Takaku K., Oshima M., Taketo M.M. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 1999, 18:5931-5942.
20. Hayes M.J., Thomas D., Emmons A., Giordano T.J., Kleer C.G. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin. Cancer Res. 2008, 14:4038-4044.
21. Herschkowitz J.I., Lubet R. Mouse models of triple negative [basal-like/claudin low] breast cancer. Breast Dis. 2010, 32:63-71.
22. Herschkowitz J.I., Simin K., Weigman V.J., Mikaelian I., Usary J., Hu Z., Rasmussen K.E., Jones L.P., Assefnia S., Chandrasekharan S., et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 2007, 8:R76.
23. Holland J.D., Kochetkova M., Akekawatchai C., Dottore M., Lopez A., McColl S.R. Differential functional activation of chemokine receptor CXCR4 is mediated by G proteins in breast cancer cells. Cancer Res. 2006, 66:4117-4124.
24. Holland J.D., Klaus A., Garratt A.N., Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr. Opin. Cell Biol. 2013, 25:254-264.
25. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
26. Huang S., Ouyang N., Lin L., Chen L., Wu W., Su F., Yao Y., Yao H. HGF-induced PKCζ activation increases functional CXCR4 expression in human breast cancer cells. PLoS ONE 2012, 7:e29124.
27. Imbert A., Eelkema R., Jordan S., Feiner H., Cowin P. Delta N89 beta-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J.Cell Biol. 2001, 153:555-568.
28. Keating G.M. Plerixafor: a review of its use in stem-cell mobilization inpatients with lymphoma or multiple myeloma. Drugs 2011, 71:1623-1647.
29. Khramtsov A.I., Khramtsova G.F., Tretiakova M., Huo D., Olopade O.I., Goss K.H. Wnt/beta-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. Am. J. Pathol. 2010, 176:2911-2920.
30. Knight J.F., Lesurf R., Zhao H., Pinnaduwage D., Davis R.R., Saleh S.M., Zuo D., Naujokas M.A., Chughtai N., Herschkowitz J.I., et al. Met synergizes with p53 loss to induce mammary tumors that possess features of claudin-low breast cancer. Proc. Natl. Acad. Sci. USA 2013, 110:E1301-E1310.
31. Lee G.Y., Kenny P.A., Lee E.H., Bissell M.J. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat. Methods 2007, 4:359-365.
32. Lim E., Wu D., Pal B., Bouras T., Asselin-Labat M.L., Vaillant F., Yagita H., Lindeman G.J., Smyth G.K., Visvader J.E. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res. 2010, 12:R21.
33. López-Knowles E., Zardawi S.J., McNeil C.M., Millar E.K., Crea P., Musgrove E.A., Sutherland R.L., O'Toole S.A. Cytoplasmic localization of beta-catenin is a marker of poor outcome in breast cancer patients. Cancer Epidemiol. Biomarkers Prev. 2010, 19:301-309.
34. Malanchi I., Peinado H., Kassen D., Hussenet T., Metzger D., Chambon P., Huber M., Hohl D., Cano A., Birchmeier W., Huelsken J. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008, 452:650-653.
35. Matsuda Y., Schlange T., Oakeley E.J., Boulay A., Hynes N.E. WNT signaling enhances breast cancer cell motility and blockade of the WNT pathway by sFRP1 suppresses MDA-MB-231 xenograft growth. Breast Cancer Res. 2009, 11:R32.
36. Matteucci E., Ridolfi E., Maroni P., Bendinelli P., Desiderio M.A. c-Src/histone deacetylase 3 interaction is crucial for hepatocyte growth factor dependent decrease of CXCR4 expression in highly invasive breast tumor cells. Mol. Cancer Res. 2007, 5:833-845.
37. Maxwell C. Biomarker research in breast cancer. Clin. J. Oncol. Nurs. 2010, 14:771-783.
38. Monteiro J., Gaspar C., Richer W., Franken P.F., Sacchetti A., Joosten R., Idali A., Brandao J., Decraene C., Fodde R. Cancer stemness inWnt-driven mammary tumorigenesis. Carcinogenesis 2013, Published online September 13, 2013.
39. Michaelson J.S., Leder P. beta-catenin is a downstream effector of Wnt-mediated tumorigenesis in the mammary gland. Oncogene 2001, 20:5093-5099.
40. Miyoshi K., Shillingford J.M., Le Provost F., Gounari F., Bronson R., von Boehmer H., Taketo M.M., Cardiff R.D., Hennighausen L., Khazaie K. Activation of beta -catenin signaling in differentiated mammary secretory cells induces transdifferentiation into epidermis and squamous metaplasias. Proc. Natl. Acad. Sci. USA 2002, 99:219-224.
41. Nie Y., Waite J., Brewer F., Sunshine M.J., Littman D.R., Zou Y.R. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J.Exp. Med. 2004, 200:1145-1156.
42. Nimmagadda S., Pullambhatla M., Stone K., Green G., Bhujwalla Z.M., Pomper M.G. Molecular imaging of CXCR4 receptor expression in human cancer xenografts with [64Cu]AMD3100 positron emission tomography. Cancer Res. 2010, 70:3935-3944.
43. Nusse R., Varmus H.E. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982, 31:99-109.
44. Oakman C., Santarpia L., Di Leo A. Breast cancer assessment tools and optimizing adjuvant therapy. Nat Rev Clin Oncol 2010, 7:725-732.
45. Ponzo M.G., Lesurf R., Petkiewicz S., O'Malley F.P., Pinnaduwage D., Andrulis I.L., Bull S.B., Chughtai N., Zuo D., Souleimanova M., et al. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc. Natl. Acad. Sci. USA 2009, 106:12903-12908.
46. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456:593-598.
47. Shackleton M., Vaillant F., Simpson K.J., Stingl J., Smyth G.K., Asselin-Labat M.L., Wu L., Lindeman G.J., Visvader J.E. Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88.
48. Shafee N., Smith C.R., Wei S., Kim Y., Mills G.B., Hortobagyi G.N., Stanbridge E.J., Lee E.Y. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Cancer Res. 2008, 68:3243-3250.
49. Shah S.P., Roth A., Goya R., Oloumi A., Ha G., Zhao Y., Turashvili G., Ding J., Tse K., Haffari G., et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012, 486:395-399.
50. Smolen G.A., Muir B., Mohapatra G., Barmettler A., Kim W.J., Rivera M.N., Haserlat S.M., Okimoto R.A., Kwak E., Dahiya S., et al. Frequent met oncogene amplification in a Brca1/Trp53 mouse model of mammary tumorigenesis. Cancer Res. 2006, 66:3452-3455.
51. Stingl J., Eirew P., Ricketson I., Shackleton M., Vaillant F., Choi D., Li H.I., Eaves C.J. Purification and unique properties of mammary epithelial stem cells. Nature 2006, 439:993-997.
52. Takahashi-Yanaga F., Kahn M. Targeting Wnt signaling: can we safely eradicate cancer stem cells?. Clin. Cancer Res. 2010, 16:3153-3162.
53. Vermeulen L., De Sousa E Melo F., van der Heijden M., Cameron K., de Jong J.H., Borovski T., Tuynman J.B., Todaro M., Merz C., Rodermond H., et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 2010, 12:468-476.
54. 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 2002, 415:530-536.
55. Van Keymeulen A., Rocha A.S., Ousset M., Beck B., Bouvencourt G., Rock J., Sharma N., Dekoninck S., Blanpain C. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011, 479:189-193.
56. Wagner K.U., Wall R.J., St-Onge L., Gruss P., Wynshaw-Boris A., Garrett L., Li M., Furth P.A., Hennighausen L. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res. 1997, 25:4323-4330.
57. Wagner K.U., Boulanger C.A., Henry M.D., Sgagias M., Hennighausen L., Smith G.H. An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 2002, 129:1377-1386.
58. Weigelt B., Reis-Filho J.S. Histological and molecular types of breast cancer: is there a unifying taxonomy?. Nat Rev Clin Oncol 2009, 6:718-730.
59. Wend P., Runke S., Wend K., Anchondo B., Yesayan M., Jardon M., Hardie N., Loddenkemper C., Ulasov I., Lesniak M.S., et al. WNT10B/beta-catenin signalling induces HMGA2 and proliferation in metastatic triple-negative breast cancer. EMBO Mol. Med. 2013, 5:264-279.
60. Yang L., Wu X., Wang Y., Zhang K., Wu J., Yuan Y.C., Deng X., Chen L., Kim C.C., Lau S., et al. FZD7 has a critical role in cell proliferation in triple negative breast cancer. Oncogene 2011, 30:4437-4446.
61. Zeng Y.A., Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 2010, 6:568-577.
62. Zhang M., Atkinson R.L., Rosen J.M. Selective targeting of radiation-resistant tumor-initiating cells. Proc. Natl. Acad. Sci. USA 2010, 107:3522-3527.
63. Zlotnik A., Burkhardt A.M., Homey B. Homeostatic chemokine receptors and organ-specific metastasis. Nat. Rev. Immunol. 2011, 11:597-606.