EMT in breast cancer stem cell generation

Cancer Letters

Volumn 338, Issue 1, 2013, Pages 63-68

  Ansieau, Stéphane ^a,b,c  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b CENTRE LÉON BÉRARD   (France)

^c LabEx DEVweCAN   (France)

Author keywords

Breast; Cancer stem cells; Cell plasticity; Embryonic EMT inducers; Epithelial to mesenchymal transition

Indexed keywords

BMI1 PROTEIN; CD24 ANTIGEN; CELL PROTEIN; HERMES ANTIGEN; PROTEIN ALDH1; PROTEIN P53; SNAIL1 PROTEIN; SNAIL2 PROTEIN; TRANSCRIPTION FACTOR ZEB1; TWIST1 PROTEIN; UNCLASSIFIED DRUG;

BIOTYPOLOGY; BREAST CANCER; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STAGING; CANCER STEM CELL; CARCINOGENESIS; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL FUNCTION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION; HUMAN; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHORT SURVEY; TUMOR SUPPRESSOR GENE;

EID: 84882849193     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.05.014     Document Type: Review

References (67)

1. Bernards R., Weinberg R.A. A progression puzzle. Nature 2002, 418:823.
2. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
3. 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.
4. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 2007, 7:415-428.
5. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
6. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
7. Maestro R., Dei Tos A.P., Hamamori Y., Krasnokutsky S., Sartorelli V., Kedes L., Doglioni C., Beach D.H., Hannon G.J. Twist is a potential oncogene that inhibits apoptosis. Genes Dev. 1999, 13:2207-2217.
8. Valsesia-Wittmann S., Magdeleine M., Dupasquier S., Garin E., Jallas A.C., Combaret V., Krause A., Leissner P., Puisieux A. Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell 2004, 6:625-630.
9. Wu W.S., Heinrichs S., Xu D., Garrison S.P., Zambetti G.P., Adams J.M., Look A.T. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 2005, 123:641-653.
10. Ansieau S., Bastid J., Doreau A., Morel A.P., Bouchet B.P., Thomas C., Fauvet F., Puisieux I., Doglioni C., Piccinin S., Maestro R., Voeltzel T., Selmi A., Valsesia-Wittmann S., Caron de F.C., Puisieux A. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008, 14:79-89.
11. Perez-Caro M., Bermejo-Rodriguez C., Gonzalez-Herrero I., Sanchez-Beato M., Piris M.A., Sanchez-Garcia I. Transcriptomal profiling of the cellular response to DNA damage mediated by Slug (Snai2). Br. J. Cancer 2008, 98:480-488.
12. Lee S.H., Lee S.J., Jung Y.S., Xu Y., Kang H.S., Ha N.C., Park B.J. Blocking of p53-Snail binding, promoted by oncogenic K-Ras, recovers p53 expression and function. Neoplasia 2009, 11:22-31. 6p.
13. Sayan A.E., Griffiths T.R., Pal R., Browne G.J., Ruddick A., Yagci T., Edwards R., Mayer N.J., Qazi H., Goyal S., Fernandez S., Straatman K., Jones G.D., Bowman K.J., Colquhoun A., Mellon J.K., Kriajevska M., Tulchinsky E. SIP1 protein protects cells from DNA damage-induced apoptosis and has independent prognostic value in bladder cancer. Proc. Natl. Acad. Sci. USA 2009, 106:14884-14889.
14. Ohashi S., Natsuizaka M., Wong G.S., Michaylira C.Z., Grugan K.D., Stairs D.B., Kalabis J., Vega M.E., Kalman R.A., Nakagawa M., Klein-Szanto A.J., Herlyn M., Diehl J.A., Rustgi A.K., Nakagawa H. Epidermal growth factor receptor and mutant p53 expand an esophageal cellular subpopulation capable of epithelial-to-mesenchymal transition through ZEB transcription factors. Cancer Res. 2010, 70:4174-4184.
15. Ansieau S., Morel A.P., Hinkal G., Bastid J., Puisieux A. TWISTing an embryonic transcription factor into an oncoprotein. Oncogene 2010, 29:3173-3184.
16. Elenbaas B., Spirio L., Koerner F., Fleming M.D., Zimonjic D.B., Donaher J.L., Popescu N.C., Hahn W.C., Weinberg R.A. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 2001, 15:50-65.
17. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., Campbell L.L., Polyak K., Brisken C., Yang J., Weinberg R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
18. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008, 3:e2888.
19. Vesuna F., Lisok A., Kimble B., Raman V. Twist modulates breast cancer stem cells by transcriptional regulation of CD24 expression. Neoplasia 2009, 11:1318-1328.
20. Battula V.L., Evans K.W., Hollier B.G., Shi Y., Marini F.C., Ayyanan A., Wang R.Y., Brisken C., Guerra R., Andreeff M., Mani S.A. Epithelial-mesenchymal transition-derived cells exhibit multilineage differentiation potential similar to mesenchymal stem cells. Stem Cells 2010, 28:1435-1445.
21. Yang M.H., Hsu D.S., Wang H.W., Wang H.J., Lan H.Y., Yang W.H., Huang C.H., Kao S.Y., Tzeng C.H., Tai S.K., Chang S.Y., Lee O.K., Wu K.J. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat. Cell Biol. 2010, 12:982-992.
22. Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., Waldvogel B., Vannier C., Darling D., Zur H.A., Brunton V.G., Morton J., Sansom O., Schuler J., Stemmler M.P., Herzberger C., Hopt U., Keck T., Brabletz S., Brabletz T. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 2009, 11:1487-1495.
23. Guo W., Keckesova Z., Donaher J.L., Shibue T., Tischler V., Reinhardt F., Itzkovitz S., Noske A., Zurrer-Härdy U., Bell G., Tam W.L., Mani S.A., van Oudenaarden A., Weinberg R.A. Slug and sox9 cooperatively determine the mammary stem cell state. Cell 2012, 148:1015-1028.
24. Gupta P.B., Chaffer C.L., Weinberg R.A. Cancer stem cells: mirage or reality?. Nat. Med. 2009, 15:1010-1012.
25. Watson M.A., Ylagan L.R., Trinkaus K.M., Gillanders W.E., Naughton M.J., Weilbaecher K.N., Fleming T.P., Aft R.L. Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients. Clin. Cancer Res. 2007, 13:5001-5009.
26. Creighton C.J., Li X., Landis M., Dixon J.M., Neumeister V.M., Sjolund A., Rimm D.L., Wong H., Rodriguez A., Herschkowitz J.I., Fan C., Zhang X., He X., Pavlick A., Gutierrez M.C., Renshaw L., Larionov A.A., Faratian D., Hilsenbeck S.G., Perou C.M., Lewis M.T., Rosen J.M., Chang J.C. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl. Acad. Sci. USA 2009, 106:13820-13825.
27. Lin T., Ambasudhan R., Yuan X., Li W., Hilcove S., Abujarour R., Lin X., Hahm H.S., Hao E., Hayek A., Ding S. A chemical platform for improved induction of human iPSCs. Nat. Methods 2009, 6:805-808.
28. Geradts J., de Herreros A.G., Su Z., Burchette J., Broadwater G., Bachelder R.E. Nuclear Snail1 and nuclear ZEB1 protein expression in invasive and intraductal human breast carcinomas. Hum. Pathol. 2011, 42:1125-1131.
29. Morel A.-P., Hinkal G.W., Thomas C., Fauvet F., Courtois-cox S., Wierinckx A., Devouassoux-Shisheboran M., Treilleux I., Tissier A., Gras B., Pourchet J., Puisieux I., Browne G., Spicer D.B., Lachuer J., Ansieau S., Puisieux A. EMT inducers catalyze malignant transformation of mammary epithelial cells and drive tumorigenesis towards claudin-low tumors in transgenic mice. PLoS Genetics 2012, 8:e1002723.
30. Hu Z., Fan C., Oh D.S., Marron J.S., He X., Qaqish B.F., Livasy C., Carey L.A., Reynolds E., Dressler L., Nobel A., Parker J., Ewend M.G., Sawyer L.R., Wu J., Liu Y., Nanda R., Tretiakova M., Ruiz O.A., Dreher D., Palazzo J.P., Perreard L., Nelson E., Mone M., Hansen H., Mullins M., Quackenbush J.F., Ellis M.J., Olopade O.I., Bernard P.S., Perou C.M. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genom. 2006, 7:96.
31. Neve R.M., Chin K., Fridlyand J., Yeh J., Baehner F.L., Fevr T., Clark L., Bayani N., Coppe J.P., Tong F., Speed T., Spellman P.T., DeVries S., Lapuk A., Wang N.J., Kuo W.L., Stilwell J.L., Pinkel D., Albertson D.G., Waldman F.M., McCormick F., Dickson R.B., Johnson M.D., Lippman M., Ethier S., Gazdar A., Gray J.W. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515-527.
32. Herschkowitz J.I., Simin K., Weigman V.J., Mikaelian I., Usary J., Hu Z., Rasmussen K.E., Jones L.P., Assefnia S., Chandrasekharan S., Backlund M.G., Yin Y., Khramtsov A.I., Bastein R., Quackenbush J., Glazer R.I., Brown P.H., Green J.E., Kopelovich L., Furth P.A., Palazzo J.P., Olopade O.I., Bernard P.S., Churchill G.A., Van Dyke T., Perou C.M. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 2007, 8:R76.
33. Hennessy B.T., Gonzalez-Angulo A.M., Stemke-Hale K., Gilcrease M.Z., Krishnamurthy S., Lee J.S., Fridlyand J., Sahin A., Agarwal R., Joy C., Liu W., Stivers D., Baggerly K., Carey M., Lluch A., Monteagudo C., He X., Weigman V., Fan C., Palazzo J., Hortobagyi G.N., Nolden L.K., Wang N.J., Valero V., Gray J.W., Perou C.M., Mills G.B. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res. 2009, 69:4116-4124.
34. 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.
35. Molyneux G., Geyer F.C., Magnay F.A., McCarthy A., Kendrick H., Natrajan R., Mackay A., Grigoriadis A., Tutt A., Ashworth A., Reis-Filho J.S., Smalley M.J. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010, 7:403-417.
36. Liu X., Holstege H., van der Gulden H., Treur-Mulder M., Zevenhoven J., Velds A., Kerkhoven R.M., van Vliet M.H., Wessels L.F., Peterse J.L., Berns A., Jonkers J. Somatic loss of BRCA1 and p53 in mice induces mammary tumors with features of human BRCA1-mutated basal-like breast cancer. Proc. Natl. Acad. Sci. USA 2007, 104:12111-12116.
37. Lim E., Vaillant F., Wu D., Forrest N.C., Pal B., Hart A.H., Asselin-Labat M.L., Gyorki D.E., Ward T., Partanen A., Feleppa F., Huschtscha L.I., Thorne H.J., Fox S.B., Yan M., French J.D., Brown M.A., Smyth G.K., Visvader J.E., Lindeman G.J. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat. Med. 2009, 15:907-913.
38. Prat A., Perou C.M. Mammary development meets cancer genomics. Nat. Med. 2009, 15:842-844.
39. 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.
40. Visvader J.E. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev. 2009, 23:2563-2577.
41. Sarrio D., Franklin C.K., Mackay A., Reis-Filho J.S., Isacke C.M. Epithelial and mesenchymal subpopulations within normal Basal breast cell lines exhibit distinct stem cell/progenitor properties. Stem Cells 2012, 30:292-303.
42. Keller P.J., Arendt L.M., Skibinski A., Logvinenko T., Klebba I., Dong S., Smith A.E., Prat A., Perou C.M., Gilmore H., Schnitt S., Naber S.P., Garlick J.A., Kuperwasser C. Defining the cellular precursors to human breast cancer. Proc. Natl. Acad. Sci. USA 2012, 109:2772-2777.
43. Prat A., Parker J.S., Karginova O., Fan C., Livasy C., Herschkowitz J.I., He X., Perou C.M. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res. 2010, 12:R68.
44. Spike B.T., Engle D.D., Lin J.C., Cheung S.K., La J., Wahl G.M. A mammary stem cell population identified and characterized in late embryogenesis reveals similarities to human breast cancer. Cell Stem Cell 2012, 10:183-197.
45. Fillmore C.M., Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 2008, 10:R25.
46. Taube J.H., Herschkowitz J.I., Komurov K., Zhou A.Y., Gupta S., Yang J., Hartwell K., Onder T.T., Gupta P.B., Evans K.W., Hollier B.G., Ram P.T., Lander E.S., Rosen J.M., Weinberg R.A., Mani S.A. Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc. Natl. Acad. Sci. USA 2010, 107:15449-15454.
47. Asiedu M.K., Ingle J.N., Behrens M.D., Radisky D.C., Knutson K.L. TGFbeta/TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Res. 2011, 71:4707-4719.
48. Scheel C., Eaton E.N., Li S.H., Chaffer C.L., Reinhardt F., Kah K.J., Bell G., Guo W., Rubin J., Richardson A.L., Weinberg R.A. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011, 145:926-940.
49. Paranjape A.N., Mandal T., Mukherjee G., Kumar M.V., Sengupta K., Rangarajan A. Introduction of SV40ER and hTERT into mammospheres generates breast cancer cells with stem cell properties. Oncogene 2012, 31:1896-1909.
50. Proia T.A., Keller P.J., Gupta P.B., Klebba I., Jones A.D., Sedic M., Gilmore H., Tung N., Naber S.P., Schnitt S., Lander E.S., Kuperwasser C. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011, 8:149-163.
51. Derksen P.W., Braumuller T.M., van der Burg E., Hornsveld M., Mesman E., Wesseling J., Krimpenfort P., Jonkers J. Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice. Dis. Model. Mech. 2011, 4:347-358.
52. Chang C.J., Chao C.H., Xia W., Yang J.Y., Xiong Y., Li C.W., Yu W.H., Rehman S.K., Hsu J.L., Lee H.H., Liu M., Chen C.T., Yu D., Hung M.C. P53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat. Cell Biol. 2011, 13:317-323.
53. Gilbertson R.J. Mapping cancer origins. Cell 2011, 145:25-29.
54. Fang X., Cai Y., Liu J., Wang Z., Wu Q., Zhang Z., Yang C.J., Yuan L., Ouyang G. Twist2 contributes to breast cancer progression by promoting an epithelial-mesenchymal transition and cancer stem-like cell self-renewal. Oncogene 2011, 30:4707-4720.
55. Dang H., Ding W., Emerson D., Rountree C.B. Snail1 induces epithelial-to-mesenchymal transition and tumor initiating stem cell characteristics. BMC Cancer 2011, 11:396.
56. Xie G., Yao Q., Liu Y., Du S., Liu A., Guo Z., Sun A., Ruan J., Chen L., Ye C., Yuan Y. IL-6-induced epithelial-mesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int. J. Oncol. 2012, 40:1171-1179.
57. Potten C.S., Kellett M., Rew D.A., Roberts S.A. Proliferation in human gastrointestinal epithelium using bromodeoxyuridine in vivo: data for different sites, proximity to a tumour, and polyposis coli. Gut 1992, 33:524-529.
58. Bjerknes M., Cheng H., Hay K., Gallinger S. APC mutation and the crypt cycle in murine and human intestine. Am. J. Pathol. 1997, 150:833-839.
59. Wasan H.S., Park H.S., Liu K.C., Mandir N.K., Winnett A., Sasieni P., Bodmer W.F., Goodlad R.A., Wright N.A. APC in the regulation of intestinal crypt fission. J. Pathol. 1998, 185:246-255.
60. Brabletz T., Jung A., Reu S., Porzner M., Hlubek F., Kunz-Schughart L.A., Knuechel R., Kirchner T. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc. Natl. Acad. Sci. USA 2001, 98:10356-10361.
61. Walker F., Zhang H.H., Odorizzi A., Burgess A.W. LGR5 is a negative regulator of tumourigenicity, antagonizes Wnt signalling and regulates cell adhesion in colorectal cancer cell lines. PLoS ONE 2011, 6:e22733.
62. Vermeulen L., Melo De Sousa E, van der Heijden M., Cameron K., de Jong J.H., Borovski T., Tuynman J.B., Todaro M., Merz C., Rodermond H., Sprick M.R., Kemper K., Richel D.J., Stassi G., Medema J.P. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 2010, 12:468-476.
63. Sánchez-Tilló E., de Barrios O., Siles L., Cuatrecasas M., Castells A., Postigo A. Beta-catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness. Proc. Natl. Acad. Sci. USA 2011, 108:19204-19209.
64. Valcz G., Sipos F., Krenacs T., Molnar J., Patai A.V., Leiszter K., Toth K., Wichmann B., Molnar B., Tulassay Z. Increase of alpha-SMA(+) and CK (+) Cells as an Early Sign of Epithelial-Mesenchymal Transition during Colorectal Carcinogenesis. Pathol. Oncol. Res. 2012, 18:371-376.
65. Loboda A., Nebozhyn M.V., Watters J.W., Buser C.A., Shaw P.M., Huang P.S., Van't Veer L., Tollenaar R.A., Jackson D.B., Agrawal D., Dai H., Yeatman T.J. EMT is the dominant program in human colon cancer. BMC Med. Genomics 2011, 4:9.
66. Singh A., Greninger P., Rhodes D., Koopman L., Violette S., Bardeesy N., Settleman J. A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 2009, 15:489-500.
67. Liu Y., Dean D.C. Tumor initiation via loss of cell contact inhibition versus Ras mutation: do all roads lead to EMT?. Cell Cycle 2010, 9:897-900.