Oncogenic transformation of mammary epithelial cells by transforming growth factor beta independent of mammary stem cell regulation

Cancer Cell International

Volumn 13, Issue 1, 2013, Pages

  Dunphy, Karen A ^a   Seo, Jae Hong ^b   Kim, Daniel J ^a   Roberts, Amy L ^a   Tao, Luwei ^a   DiRenzo, James ^c   Balboni, Amanda L ^c   Crisi, Giovanna M ^d   Hagen, Mary J ^a   Chandrasekaran, Thiruppavai ^a   Gauger, Kelly J ^e   Schneider, Sallie Smith ^e   Jerry, D Joseph ^a,e  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b Korea University   (South Korea)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d BAYSTATE MEDICAL CENTER   (United States)

^e Pioneer Valley Life Sciences Institute   (United States)

Author keywords

EMT; Epithelial to mesenchymal transition; TGF ; Transdifferentiation; Transforming growth factor beta

Indexed keywords

GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST EPITHELIUM; CANCER STEM CELL; CELL DEDIFFERENTIATION; CELL POPULATION; CELL TRANSDIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE EXPRESSION PROFILING; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; INVOLUTION; LATENT PERIOD; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; SOLID TUMOR; TUMOR DIFFERENTIATION;

EID: 84880912288     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-13-74     Document Type: Article

References (64)

1. Padua D, Massague J. Roles of TGFbeta in metastasis. Cell Res 2009, 19:89-102. 10.1038/cr.2008.316, 19050696.
2. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005, 24:5764-5774. 10.1038/sj.onc.1208927, 16123809.
3. Muraoka-Cook RS, Dumont N, Arteaga CL. Dual role of transforming growth factor beta in mammary tumorigenesis and metastatic progression. Clin Cancer Res 2005, 11:937s-943s.
4. Bierie B, Moses HL. Gain or loss of TGFbeta signaling in mammary carcinoma cells can promote metastasis. Cell Cycle 2009, 8:3319-3327. 10.4161/cc.8.20.9727, 19806012.
5. Ewan KB, Oketch-Rabah HA, Ravani SA, Shyamala G, Moses HL, Barcellos-Hoff MH. Proliferation of estrogen receptor-alpha-positive mammary epithelial cells is restrained by transforming growth factor-beta1 in adult mice. Am J Pathol 2005, 167:409-417. 10.1016/S0002-9440(10)62985-9, 1603552, 16049327.
6. Becker KA, Lu S, Dickinson ES, Dunphy KA, Mathews L, Schneider SS, et al. Estrogen and progesterone regulate radiation-induced p53 activity in mammary epithelium through TGF-beta-dependent pathways. Oncogene 2005, 24:6345-6353.
7. Bierie B, Gorska AE, Stover DG, Moses HL. TGF-beta promotes cell death and suppresses lactation during the second stage of mammary involution. J Cell Physiol 2009, 219:57-68. 10.1002/jcp.21646, 3038423, 19086032.
8. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia 2010, 15:117-134. 10.1007/s10911-010-9178-9, 2886089, 20490631.
9. Joseph H, Gorska AE, Sohn P, Moses HL, Serra R. Overexpression of a kinase-deficient transforming growth factor-beta type II receptor in mouse mammary stroma results in increased epithelial branching. Mol Biol Cell 1999, 10:1221-1234. 10.1091/mbc.10.4.1221, 25256, 10198068.
10. Dunphy KA, Schneyer AL, Hagen MJ, Jerry DJ. The role of activin in mammary gland development and oncogenesis. J Mammary Gland Biol Neoplasia 2011, 16:117-126. 10.1007/s10911-011-9214-4, 21475961.
11. Faure E, Heisterkamp N, Groffen J, Kaartinen V. Differential expression of TGF-beta isoforms during postlactational mammary gland involution. Cell Tissue Res 2000, 300:89-95.
12. Robinson SD, Silberstein GB, Roberts AB, Flanders KC, Daniel CW. Regulated expression and growth inhibitory effects of transforming growth factor-beta isoforms in mouse mammary gland development. Development 1991, 113:867-878.
13. Strange R, Li F, Saurer S, Burkhardt A, Friis RR. Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development 1992, 115:49-58.
14. Flanders KC, Wakefield LM. Transforming growth factor-(beta)s and mammary gland involution; functional roles and implications for cancer progression. J Mammary Gland Biol Neoplasia 2009, 14:131-144. 10.1007/s10911-009-9122-z, 2797127, 19396528.
15. Barcellos-Hoff MH, Derynck R, Tsang ML, Weatherbee JA. Transforming growth factor-beta activation in irradiated murine mammary gland. J Clin Invest 1994, 93:892-899. 10.1172/JCI117045, 293960, 8113421.
16. Biswas S, Guix M, Rinehart C, Dugger TC, Chytil A, Moses HL, et al. Inhibition of TGF-beta with neutralizing antibodies prevents radiation-induced acceleration of metastatic cancer progression. J Clin Invest 2007, 117:1305-1313. 10.1172/JCI30740, 1838926, 17415413.
17. Andarawewa KL, Erickson AC, Chou WS, Costes SV, Gascard P, Mott JD, et al. Ionizing radiation predisposes nonmalignant human mammary epithelial cells to undergo transforming growth factor beta induced epithelial to mesenchymal transition. Cancer Res 2007, 67:8662-8670. 10.1158/0008-5472.CAN-07-1294, 17875706.
18. Brown KA, Aakre ME, Gorska AE, Price JO, Eltom SE, Pietenpol JA, et al. Induction by transforming growth factor-beta1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Res 2004, 6:R215-R231. 10.1186/bcr778, 400675, 15084245.
19. Dumont N, Wilson MB, Crawford YG, Reynolds PA, Sigaroudinia M, Tlsty TD. Sustained induction of epithelial to mesenchymal transition activates DNA methylation of genes silenced in basal-like breast cancers. Proc Natl Acad Sci USA 2008, 105:14867-14872. 10.1073/pnas.0807146105, 2567459, 18806226.
20. Morel AP, 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. 10.1371/journal.pone.0002888, 2492808, 18682804.
21. Oft M, Peli J, Rudaz C, Schwarz H, Beug H, Reichmann E. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev 1996, 10:2462-2477. 10.1101/gad.10.19.2462, 8843198.
22. Oft M, Heider KH, Beug H. TGFbeta signaling is necessary for carcinoma cell invasiveness and metastasis. Curr Biol 1998, 8:1243-1252. 10.1016/S0960-9822(07)00533-7, 9822576.
23. Miettinen PJ, Ebner R, Lopez AR, Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994, 127:2021-2036. 10.1083/jcb.127.6.2021, 2120317, 7806579.
24. Gal A, Sjoblom T, Fedorova L, Imreh S, Beug H, Moustakas A. Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 2008, 27:1218-1230. 10.1038/sj.onc.1210741, 17724470.
25. 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, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
26. Lindley LE, Briegel KJ. Molecular characterization of TGFbeta-induced epithelial-mesenchymal transition in normal finite lifespan human mammary epithelial cells. Biochem Biophys Res Commun 2010, 399:659-664. 10.1016/j.bbrc.2010.07.138, 20691661.
27. Asiedu MK, Ingle JN, Behrens MD, Radisky DC, Knutson KL. TGFbeta/TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Res 2011, 71:4707-4719. 10.1158/0008-5472.CAN-10-4554, 3129359, 21555371.
28. Santisteban M, Reiman JM, Asiedu MK, Behrens MD, Nassar A, Kalli KR, et al. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 2009, 69:2887-2895. 10.1158/0008-5472.CAN-08-3343, 2664865, 19276366.
29. Lim E, Wu D, Pal B, Bouras T, Asselin-Labat ML, Vaillant F, et al. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res 2010, 12:R21. 10.1186/bcr2560, 2879567, 20346151.
30. Blick T, Hugo H, Widodo E, Waltham M, Pinto C, Mani SA, et al. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia 2010, 15:235-252. 10.1007/s10911-010-9175-z, 20521089.
31. Gauger KJ, Hugh JM, Troester MA, Schneider SS. Down-regulation of sfrp1 in a mammary epithelial cell line promotes the development of a cd44high/cd24low population which is invasive and resistant to anoikis. Cancer Cell Int 2009, 9:11. 10.1186/1475-2867-9-11, 2687411, 19422694.
32. 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, 145:926-940. 10.1016/j.cell.2011.04.029, 21663795.
33. Deugnier MA, Faraldo MM, Teuliere J, Thiery JP, Medina D, Glukhova MA. Isolation of mouse mammary epithelial progenitor cells with basal characteristics from the Comma-Dbeta cell line. Dev Biol 2006, 293:414-425. 10.1016/j.ydbio.2006.02.007, 16545360.
34. Jerry DJ, Medina D, Butel JS. p53 mutations in COMMA-D cells. In Vitro Cell Dev Biol Anim 1994, 30A:87-89.
35. Kittrell FS, Carletti MZ, Kerbawy S, Heestand J, Xian W, Zhang M, et al. Prospective isolation and characterization of committed and multipotent progenitors from immortalized mouse mammary epithelial cells with morphogenic potential. Breast Cancer Res 2011, 13:R41. 10.1186/bcr2863, 3219204, 21466693.
36. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc 2009, 4:44-45.
37. Huang DW, Sherman BT, Lempi RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13. 10.1093/nar/gkn923, 2615629, 19033363.
38. Tao L, Roberts AL, Dunphy KA, Bigelow C, Yan H, Jerry DJ. Repression of mammary stem/progenitor cells by p53 is mediated by Notch and separable from apoptotic activity. Stem Cells 2011, 29:119-127. 10.1002/stem.552, 3404152, 21280161.
39. Katoh Y, Katoh M. Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA (review). Int J Mol Med 2008, 22:271-275.
40. Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, Roslan S, et al. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell 2011, 22:1686-1698. 10.1091/mbc.E11-02-0103, 3093321, 21411626.
41. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, et al. 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. 10.1073/pnas.1004900107, 2932589, 20713713.
42. Nguyen DH, Oketch-Rabah HA, Illa-Bochaca I, Geyer FC, Reis-Filho JS, Mao JH, et al. Radiation acts on the microenvironment to affect breast carcinogenesis by distinct mechanisms that decrease cancer latency and affect tumor type. Cancer Cell 2011, 19:640-651. 10.1016/j.ccr.2011.03.011, 3110779, 21575864.
43. Battula VL, Evans KW, Hollier BG, Shi Y, Marini FC, Ayyanan A, et al. Epithelial-mesenchymal transition-derived cells exhibit multilineage differentiation potential similar to mesenchymal stem cells. Stem Cells 2010, 28:1435-1445. 10.1002/stem.467, 3523728, 20572012.
44. Booth BW, Boulanger CA, Anderson LH, Jimenez-Rojo L, Brisken C, Smith GH. Amphiregulin mediates self-renewal in an immortal mammary epithelial cell line with stem cell characteristics. Exp Cell Res 2010, 316:422-432. 10.1016/j.yexcr.2009.11.006, 2812656, 19913532.
45. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644. 10.1016/j.cell.2011.07.026, 21854987.
46. Scheel C, Weinberg RA. Phenotypic plasticity and epithelial-mesenchymal transitions in cancer and normal stem cells?. Int J Cancer 2011, 129:2310-2314. 10.1002/ijc.26311, 3357895, 21792896.
47. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988. 10.1073/pnas.0530291100, 153034, 12629218.
48. Mafi R, Hindocha S, Mafi P, Griffin M, Khan WS. Sources of adult mesenchymal stem cells applicable for musculoskeletal applications - a systematic review of the literature. Open Orthop J 2011, 5(Suppl 2):242-248. 3149887, 21886689.
49. Shipitsin M, Polyak K. The cancer stem cell hypothesis: in search of definitions, markers, and relevance. Lab Invest 2008, 88:459-463. 10.1038/labinvest.2008.14, 3702270, 18379567.
50. Chang CJ, Chao CH, Xia W, Yang JY, Xiong Y, Li CW, et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol 2011, 13:1467.
51. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 1995, 92:5545-5549. 10.1073/pnas.92.12.5545, 41732, 7777546.
52. Levrero M, De LV, Costanzo A, Gong J, Wang JY, Melino G. The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci 2000, 113(Pt 10):1661-1670.
53. Yin X, Wolford CC, Chang YS, McConoughey SJ, Ramsey SA, Aderem A, et al. ATF3, an adaptive-response gene, enhances TGF{beta} signaling and cancer-initiating cell features in breast cancer cells. J Cell Sci 2010, 123:3558-3565. 10.1242/jcs.064915, 2951469, 20930144.
54. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1420-1428. 10.1172/JCI39104, 2689101, 19487818.
55. Dunphy KA, Tao L, Jerry DJ. Mammary epithelial transplant procedure. J Vis Exp 2010, 10(40).
56. Dunphy KA, Blackburn AC, Yan H, O'Connell LR, Jerry DJ. Estrogen and progesterone induce persistent increases in p53-dependent apoptosis and suppress mammary tumors in BALB/c-Trp53+/- mice. Breast Cancer Res 2008, 10:R43. 10.1186/bcr2094, 2481490, 18471300.
57. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
58. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193. 10.1093/bioinformatics/19.2.185, 12538238.
59. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003, 31:e15. 10.1093/nar/gng015, 150247, 12582260.
60. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
61. Saeed AL, Sarov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
62. Kendrick H, Regan JL, Magnay FA, Grigoriadis A, Mitsopoulos C, Zvelebil M, et al. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics 2008, 9:591. 10.1186/1471-2164-9-591, 2629782, 19063729.
63. Bloushtain-Qimron N, Yao J, Snyder EL, Shipitsin M, Campbell LL, Mani SA, et al. Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci USA 2008, 105:14076-14081. 10.1073/pnas.0805206105, 2532972, 18780791.
64. Wansbury O, Mackay A, Kogata N, Mitsopoulos C, Kendrick H, Davidson K, et al. Transcriptome analysis of embryonic mammary cells reveals insights into mammary lineage establishment. Breast Cancer Res 2011, 13:R79. 10.1186/bcr2928, 3236343, 21834968.