The Epithelial-Mesenchymal Transition Generates Cells with Properties of Stem Cells

Cell

Volumn 133, Issue 4, 2008, Pages 704-715

  Mani, Sendurai A ^a,c   Guo, Wenjun ^a   Liao, Mai Jing ^a   Eaton, Elinor Ng ^a   Ayyanan, Ayyakkannu ^d   Zhou, Alicia Y ^a,b   Brooks, Mary ^a   Reinhard, Ferenc ^a   Zhang, Cheng Cheng ^a   Shipitsin, Michail ^e,f   Campbell, Lauren L ^e,f   Polyak, Kornelia ^e,f   Brisken, Cathrin ^d   Yang, Jing ^g   Weinberg, Robert A ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d EPFL   (Switzerland)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CELLBIO; HUMDISEASE; STEMCELL

Indexed keywords

ANIMAL CELL; ARTICLE; BREAST CARCINOMA; BREAST EPITHELIUM; CANCER CELL; CELL IMMORTALIZATION; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; MAMMARY GLAND; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ADULT STEM CELLS; ANIMALS; ANTIGENS, CD24; ANTIGENS, CD44; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MESODERM; MICE; NEOPLASTIC STEM CELLS; SPHEROIDS, CELLULAR; STEM CELLS; TUMOR CELLS, CULTURED;

EID: 43049165453     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.03.027     Document Type: Article

References (42)

1. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., and Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100 (2003) 3983-3988
2. 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
3. Bonnet D., and Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3 (1997) 730-737
4. Brabletz T., Jung A., Spaderna S., Hlubek F., and Kirchner T. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5 (2005) 744-749
5. Briegel K.J. Embryonic transcription factors in human breast cancer. IUBMB Life 58 (2006) 123-132
6. 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
7. Cheng G.Z., Chan J., Wang Q., Zhang W., Sun C.D., and Wang L.H. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res. 67 (2007) 1979-1987
8. Cifone M.A., and Fidler I.J. Correlation of patterns of anchorage-independent growth with in vivo behavior of cells from a murine fibrosarcoma. Proc. Natl. Acad. Sci. USA 77 (1980) 1039-1043
9. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., Visvader J., Weissman I.L., and Wahl G.M. Cancer stem cells-Perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 66 (2006) 9339-9344
10. 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
11. Davies J.A. Mesenchyme to epithelium transition during development of the mammalian kidney tubule. Acta Anat. (Basel) 156 (1996) 187-201
12. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., and Wicha M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17 (2003) 1253-1270
13. Eisen M.B., Spellman P.T., Brown P.O., and Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95 (1998) 14863-14868
14. Elenbaas B., Spirio L., Koerner F., Fleming M.D., Zimonjic D.B., Donaher J.L., Popescu N.C., Hahn W.C., and Weinberg R.A. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 15 (2001) 50-65
15. Gudjonsson T., Villadsen R., Nielsen H.L., Ronnov-Jessen L., Bissell M.J., and Petersen O.W. Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev. 16 (2002) 693-706
16. Hahn W.C., Counter C.M., Lundberg A.S., Beijersbergen R.L., Brooks M.W., and Weinberg R.A. Creation of human tumour cells with defined genetic elements. Nature 400 (1999) 464-468
17. Hartwell K.A., Muir B., Reinhardt F., Carpenter A.E., Sgroi D.C., and Weinberg R.A. The Spemann organizer gene, Goosecoid, promotes tumor metastasis. Proc. Natl. Acad. Sci. USA 103 (2006) 18969-18974
18. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat. (Basel) 154 (1995) 8-20
19. Hay E.D. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev. Dyn. 233 (2005) 706-720
20. Huber M.A., Kraut N., and Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17 (2005) 548-558
21. Kondo M., Wagers A.J., Manz M.G., Prohaska S.S., Scherer D.C., Beilhack G.F., Shizuru J.A., and Weissman I.L. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu. Rev. Immunol. 21 (2003) 759-806
22. Liao M.J., Zhang C.C., Zhou B., Zimonjic D.B., Mani S.A., Kaba M., Gifford A., Reinhardt F., Popescu N.C., Guo W.G., et al. Enrichment of a population of mammary gland cells that forms mammospheres and has in vivo repopulating activity. Cancer Res. (2007) in press
23. Liu S., Dontu G., Mantle I.D., Patel S., Ahn N.S., Jackson K.W., Suri P., and Wicha M.S. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66 (2006) 6063-6071
24. Mani S.A., Yang J., Brooks M., Schwaninger G., Zhou A., Miura N., Kutok J.L., Hartwell K., Richardson A.L., and Weinberg R.A. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc. Natl. Acad. Sci. USA 104 (2007) 10069-10074
25. Moraes R.C., Zhang X., Harrington N., Fung J.Y., Wu M.F., Hilsenbeck S.G., Allred D.C., and Lewis M.T. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development 134 (2007) 1231-1242
26. O'Brien C.A., Pollett A., Gallinger S., and Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 (2007) 106-110
27. Oft M., Akhurst R.J., and Balmain A. Metastasis is driven by sequential elevation of H-ras and Smad2 levels. Nat. Cell Biol. 4 (2002) 487-494
28. Peinado H., Olmeda D., and Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 7 (2007) 415-428
29. Perez-Pomares J.M., and Munoz-Chapuli R. Epithelial-mesenchymal transitions: a mesodermal cell strategy for evolutive innovation in Metazoans. Anat. Rec. 268 (2002) 343-351
30. Reya T., Morrison S.J., Clarke M.F., and Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 414 (2001) 105-111
31. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., and De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 445 (2007) 111-115
32. Savagner P., Kusewitt D.F., Carver E.A., Magnino F., Choi C., Gridley T., and Hudson L.G. Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes. J. Cell. Physiol. 202 (2005) 858-866
33. 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
34. Shipitsin M., Campbell L.L., Argani P., Weremowicz S., Bloushtain-Qimron N., Yao J., Nikolskaya T., Serebryiskaya T., Beroukhim R., Hu M., et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 11 (2007) 259-273
35. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., and Dirks P.B. Identification of human brain tumour initiating cells. Nature 432 (2004) 396-401
36. Sleeman K.E., Kendrick H., Ashworth A., Isacke C.M., and Smalley M.J. CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res. 8 (2006) R7
37. 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
38. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15 (2003) 740-746
39. Thiery J.P., and Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7 (2006) 131-142
40. Weaver V.M., and Bissell M.J. Functional culture models to study mechanisms governing apoptosis in normal and malignant mammary epithelial cells. J. Mammary Gland Biol. Neoplasia 4 (1999) 193-201
41. 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
42. Yang J., Mani S.A., and Weinberg R.A. Exploring a new twist on tumor metastasis. Cancer Res. 66 (2006) 4549-4552