Control of breast cancer growth and initiation by the stem cell-associated transcription factor TCF3

Cancer Research

Volumn 72, Issue 21, 2012, Pages 5613-5624

  Slyper, Michal ^a   Shahar, Amit ^a   Bar Ziv, Anat ^a   Granit, Roy Z ^a   Hamburger, Tamar ^b   Maly, Bella ^c   Peretz, Tamar ^b   Ben Porath, Ittai ^a  

^a HEBREW UNIVERSITY   (Israel)

^b Sharett Institute for Oncology   (Israel)

^c HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR 7 LIKE 1; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST DUCT; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CANCER PREVENTION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL RENEWAL; COLONY FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; MAMMARY GLAND; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BREAST NEOPLASMS; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, SCID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

EID: 84868224872     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0119     Document Type: Article

References (48)

1. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancerstem cells. Nature 2001;414:105-11.
2. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cel biology to cancer. Nat Rev Cancer 2003;3:895-902.
3. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40:499-507.
4. Arce L, Yokoyama NN, Waterman ML. Diversity of LEF/TCF action in development and disease. Oncogene 2006;25:7492-504.
5. Merrill BJ, Pasolli HA, Polak L, Rendl M, Garcia-Garcia MJ, Anderson KV, et al. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 2004;131:263-74.
6. Merrill BJ, Gat U, Das Gupta R, Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev 2001;15: 1688-705.
7. Nguyen H, Rendl M, Fuchs E. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 2006;127:171-83.
8. Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, Shaver TM, et al. Tcf3 and Tcf4 are essential for long-term homeostasis of skinepithelia. Nat Genet 2009;41:1068-75.
9. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA. Tcf3 is an integral component of thecore regulatory circuitry ofembryonic stem cells. Genes Dev 2008;22:746-55.
10. Tam WL, Lim CY, Han J, Zhang J, Ang YS, Ng HH, et al.T-cellfactor3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 2008;26:2019-31.
11. Pereira L, Yi F, Merrill BJ. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 2006;26: 7479-91.
12. Yi F, Pereira L, Merrill BJ. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 2008;26:1951-60.
13. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, et al. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cel self-renewal. Nat Cell Biol 2011;13:762-70.
14. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, Kemler R, et al. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resis-tanceto differentiation. Nat Cell Biol 2011;13:838-45.
15. Kim CH, Oda T, Itoh M, Jiang D, Artinger KB, Chandrasekharappa SC, et al. Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 2000;407:913-6.
16. Andoniadou CL, Signore M, Young RM, Gaston-Massuet C, Wilson SW, Fuchs E, et al. HESX1- and TCF3-mediated repression of Wnt/ beta-catenin targets is required for normal development of the anterior forebrain. Development 2011;138:4931-42.
17. Wu CI, Hoffman JA, Shy BR, Ford EM, Fuchs E, Nguyen H, et al. Function of Wnt/beta-catenin in counteracting Tcf3 repression through the Tcf3-beta-catenin interaction. Development 2012;139: 2118-29.
18. vande Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, et al. Agene-expression signatureas a predictorof survival in breast cancer. N Engl J Med 2002;347:1999-2009.
19. Harrell JC, Prat A, Parker JS, Fan C, He X, Carey L, et al. Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse. Breast Cancer Res Treat 2012;132:523-35.
20. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253-70.
21. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and sox9 cooperatively determine the mammary stem cel state. Cell 2012;148:1015-28.
22. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003; 30:256-68.
23. Hu Y, Smyth GK. ELDA: extremelimiting dilution analysisforcompar-ing depleted and enriched populations in stem cell and otherassays. J Immunol Methods 2009;347:70-8.
24. Diamond I, Owolabi T, Marco M, Lam C, Glick A. Conditional gene expression in the epidermis oftransgenic mice using thetetracycline-regulated transactivators t TA and r TA linked to the keratin 5 promoter. J Invest Dermatol 2000;115:788-94.
25. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-8.
26. Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol 2007;9: 201-9.
27. Welm BE, Dijkgraaf GJ, Bledau AS, Welm AL, Werb Z. Lentiviral transduction of mammary stem cells for analysis of gene function during development and cancer. Cell Stem Cell 2008;2:90-102.
28. Rakha EA, El-Sayed ME, Reis-Filho J, Ellis IO. Patho-biological aspects of basal-like breast cancer. Breast Cancer Res Treat 2008; 113:411-22.
29. Visvader JE. Keepingabreastofthemammaryepithelial hierarchyand breast tumorigenesis. Genes Dev 2009;23:2563-77.
30. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med 2010;363:1938-48.
31. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009; 15:907-13.
32. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010;140: 62-73.
33. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, et al. Phenotypicand molecularcharacterizationoftheclaudin-lowintrinsic subtype of breast cancer. Breast Cancer Res 2010;12:R68.
34. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, et al. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 2001;15:50-65.
35. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
36. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011;145:926-40.
37. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification oftumorigenic breast cancercells. Proc Natl Acad Sci U S A 2003;100:3983-8.
38. Yang J, Weinberg RA. Epithelial-mesenchymaltransition:atthecross-roads of development and tumor metastasis. Dev Cell 2008;14: 818-29.
39. Brabletz S, Brabletz T. The ZEB/mi R-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep 2010;11: 670-7.
40. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammarycancersfrom progenitorcells. Proc Natl Acad Sci U S A 2003;100:15853-8.
41. Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cellsand promotetheir long-term expansion in culture. Cell Stem Cell 2010;6:568-77.
42. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/ beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002;22: 1172-83.
43. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-7.
44. Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P. Delta N89 beta-catenin induces precocious development, differentiation, and neopla-sia in mammary gland. J Cell Biol 2001;153:555-68.
45. Teuliere J, Faraldo MM, Deugnier MA, Shtutman M, Ben-Ze'ev A, Thiery JP, et al. Targeted activation of beta-catenin signaling in basal mammary epithelial cells affects mammary development and leads to hyperplasia. Development 2005;132: 267-77.
46. Livasy CA, Karaca G, Nanda R, Tretiakova MS, Olopade OI, Moore DT, et al. Phenotypicevaluation of the basal-like subtype of invasive breast carcinoma. Mod Pathol 2006;19:264-71.
47. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008;68:989-97.
48. Prat A, Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol 2011;5:5-23.