The origin of breast tumor heterogeneity

Oncogene

Volumn 34, Issue 42, 2015, Pages 5309-5316

  Skibinski, A ^a,b   Kuperwasser, C ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN;

BASAL LIKE BREAST CANCER; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER RESEARCH; GENETIC HETEROGENEITY; HEREDITY; HUMAN; MAMMARY GLAND; NONHUMAN; PHENOTYPE; PLASTICITY; PRECURSOR; PRIORITY JOURNAL; REVIEW; ANIMAL; BREAST; BREAST TUMOR; CELL PLASTICITY; CYTOLOGY; EPITHELIUM CELL; FEMALE; PATHOLOGY; PHYSIOLOGY; STEM CELL; TUMOR SUPPRESSOR GENE; WNT SIGNALING PATHWAY;

ANIMALS; BREAST; BREAST NEOPLASMS; CELL PLASTICITY; EPITHELIAL CELLS; FEMALE; GENES, BRCA1; GENES, P53; HUMANS; RECEPTOR, ERBB-2; STEM CELLS; WNT SIGNALING PATHWAY;

EID: 84945487572     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.475     Document Type: Review

References (87)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
3. Perouklk CM, Sørile T, Eisen MB, Van De Rijn M, Jeffrey SS, Ress CA et al. Molecular portraits of human breast tumours. Nature 2000; 406: 747-752.
4. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001; 98: 10869-10874.
5. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007; 8: R76.
6. Prat A, Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol 2011; 5: 5-23.
7. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12: R68.
8. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004; 10: 5367-5374.
9. Cheang MCU, Chia SK, Voduc D, Gao D, Leung S, Snider J et al. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 2009; 101: 736-750.
10. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF et al. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 2006; 7: 96.
11. Weigelt B, Hu Z, He X, Livasy C, Carey LA, Ewend MG et al. Molecular portraits and 70-gene prognosis signature are preserved throughout the metastatic process of breast cancer. Cancer Res 2005; 65: 9155-9158.
12. Visvader JE, Stingl J. Mammary stem cells and the differentiation hierarchy: Current status and perspectives. Gene Dev 2014; 28: 1143-1158.
13. Macias H, Hinck L. Mammary gland development. Wiley Interdisciplinary Reviews. Dev Biol 2012; 1: 533-557.
14. Hoshino K, Gardner WU. Transplantability and life span of mammary gland during serial transplantation in mice. Nature 1967; 213: 193-194.
15. Daniel CW, De Ome KB, Young JT, Blair PB, Faulkin Jr LJ. The in vivo life span of normal and preneoplastic mouse mammary glands: a serial transplantation study. Proc Natl Acad Sci USA 1968; 61: 53-60.
16. DeOme KB, Faulklin LJ, Bern HA, Blair PB. Development of mammary tumors from hyperplastic alveolar nodules. Cancer Res 1959; 19: 515-520.
17. 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: 993-997.
18. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat M et al. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439: 84-88.
19. Tsai YC, Lu Y, Nichols PW, Zlotnikov G, Jones PS, Smith HS. Contiguous patches of normal human mammary epithelium derived from a single stem cell: Implications for breast carcinogenesis. Cancer Res 1996; 56: 402-404.
20. Stingl J, Eaves CJ, Zandieh I, Emerman JT. Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res Treat 2001; 67: 93-109.
21. Stingl J, Raouf A, Emerman JT, Eaves CJ. Epithelial progenitors in the normal human mammary gland. J Mammary Gland Biol Neoplasia 2005; 10: 49-59.
22. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci USA 2004; 101: 4966-4971.
23. 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: 907-913.
24. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007; 1: 555-567.
25. Sleeman KE, Kendrick H, Robertson D, Isacke CM, Ashworth A, Smalley MJ. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol 2007; 176: 19-26.
26. Asselin-Labat M-, Vaillant F, Shackleton M, Bouras T, Lindeman GJ, Visvader JE. Delineating the epithelial hierarchy in the mouse mammary gland. Cold Spring Harbor Symp Quant Biol 2008; 73: 469-478.
27. Van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/ß-catenin-responsive stem cells in the mammary gland. Cell Stem Cell 2012; 11: 387-400.
28. Tao L, Van Bragt MPA, Laudadio E, Li Z. Lineage tracing of mammary epithelial cells using cell-type-specific cre-expressing adenoviruses. Stem Cell Rep 2014; 2: 770-779.
29. Rios AC, Fu NY, Lindeman GJ, Visvader JE. In situ identification of bipotent stem cells in the mammary gland. Nature 2014; 506: 322-327.
30. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011; 479: 189-193.
31. Prater MD, Petit V, Alasdair RI, Giraddi RR, Shehata M, Menon S et al. Mammary stem cells have myoepithelial cell properties. Nat Cell Biol 2014; 16: 942-950.
32. Visvader JE. Cells of origin in cancer. Nature 2011; 469: 314-322.
33. Banerji S, Cibulskis K, Rangel-Escareno C, Brown KK, Carter SL, Frederick AM et al. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 2012; 486: 405-409.
34. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012; 486: 395-399.
35. Koboldt DC, Fulton RS, McLellan MD, Schmidt H, Kalicki-Veizer J, McMichael JF et al. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490: 61-70.
36. Smalley M, Ashworth A. Stem cells and breast cancer: a field in transit. Nat Rev Cancer 2003; 3: 832-844.
37. Polyak K. Breast cancer: Origins and evolution. J Clin Invest 2007; 117: 3155-3163.
38. 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 mammary cancers from progenitor cells. Proc Natl Acad Sci USA 2003; 100: 15853-15858.
39. Cleary AS, Leonard TL, Gestl SA, Gunther EJ. Tumour cell heterogeneity maintained by cooperating subclones in Wnt-driven mammary cancers. Nature 2014; 508: 113-117.
40. Liu BY, McDermott SP, Khwaja SS, Alexander CM. The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells. Proc Natl Acad Sci USA 2004; 101: 4158-4163.
41. Liu BY, Kim YC, Leatherberry V, Cowin P, Alexander CM. Mammary gland development requires syndecan-1 to create a ?-catenin/TCF-responsive mammary epithelial subpopulation. Oncogene 2003; 22: 9243-9253.
42. Vaillant F, Asselin-Labat M-, Shackleton M, Forrest NC, Lindeman GJ, Visvader JE. The mammary progenitor marker CD61/?3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res 2008; 68: 7711-7717.
43. Lim E, Wu D, Pal B, Bouras T, Asselin-Labat M, 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.
44. Imbert A, Eelkema R, Jordan S, Feiner H, Cowin P. ?N89?-catenin induces precocious development, differentiation, neoplasia in mammary gland. J Cell Biol 2001; 152: 555-568.
45. Moser AR, Mattes EM, Dove WF, Lindstrom MJ, Haag JD, Gould MN. Apc(Min), a mutation in the murine APC gene, predisposes to mammary carcinomas and focal alveolar hyperplasias. Proc Natl Acad Sci USA 1993; 90: 8977-8981.
46. Kuraguchi M, Ohene-Baah NY, Sonkin D, Bronson RT, Kucherlapati R. Genetic mechanisms in Apc-mediated mammary tumorigenesis. PLoS Genet 2009; 5: e1000367.
47. Holland JD, Klaus A, Garratt AN, Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol 2013; 25: 254-264.
48. Livasy CA, Karaca G, Nanda R, Tretiakova MS, Olopade OI, Moore DT et al. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod Pathol 2006; 19: 264-271.
49. Foulkes WD. BRCA1 functions as a breast stem cell regulator. J Med Genet 2004; 41: 1-5.
50. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD et al. BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci USA 2008; 105: 1680-1685.
51. Foulkes WD, Stefansson IM, Chappuis PO, Bégin LR, Goffin JR, Wong N et al. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J Natl Cancer Inst 2003; 95: 1482-1485.
52. Liu X, Holstege H, Van Der Gulden H, Treur-Mulder M, Zevenhoven J, Velds A et al. 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.
53. Molyneux G, Geyer FC, Magnay F, McCarthy A, Kendrick H, Natrajan R et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010; 7: 403-417.
54. Proia TA, Keller PJ, Gupta PB, Klebba I, Jones AD, Sedic M et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011; 8: 149-163.
55. Phillips S, Prat A, Sedic M, Proia T, Wronski A, Mazumdar S et al. Cell-state transitions regulated by SLUG are critical for tissue regeneration and tumor initiation. Stem Cell Rep 2014; 2: 633-647.
56. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012; 148: 1015-1028.
57. Meyer DS, Brinkhaus H, Müller U, Müller M, Cardiff RD, Bentires-Alj M. Luminal expression of PIK3CA mutant H1047R in the mammary gland induces heterogeneous tumors. Cancer Res 2011; 71: 4344-4351.
58. Melchor L, Molyneux G, Mackay A, Magnay F, Atienza M, Kendrick H et al. Identification of cellular and genetic drivers of breast cancer heterogeneity in genetically engineered mouse tumour models. J Pathol 2014; 233: 124-137.
59. Keller PJ, Arendt LM, Skibinski A, Logvinenko T, Klebba I, Dong S et al. Defining the cellular precursors to human breast cancer. Proc Natl Acad Sci USA 2012; 109: 2772-2777.
60. 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. Gene Dev 2001; 15: 50-65.
61. Booth BW, Smith GH. Estrogen receptor-? and progesterone receptor are expressed in label-retaining mammary epithelial cells that divide asymmetrically and retain their template DNA strands. Breast Cancer Res 2006; 8: R49.
62. Shehata M, Teschendorff A, Sharp G, Novcic N, Russell IA, Avril S et al. Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland. Breast Cancer Res 2012; 14: R134.
63. Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006; 127: 1041-1055.
64. De Ruijter TC, Veeck J, De Hoon JPJ, Van Engeland M, Tjan-Heijnen VC. Characteristics of triple-negative breast cancer. J Cancer Res Clin Oncol 2011; 137: 183-192.
65. Ellis MJ, Perou CM. The genomic landscape of breast cancer as a therapeutic roadmap. Cancer Disc 2013; 3: 27-34.
66. Liu JC, Voisin V, Wang S, Wang DY, Jones RA, Datti A, Uehling D et al. Combined deletion of Pten and p53 in mammary epithelium accelerates triplenegative breast cancer with dependency on eEF2K. EMBO Mol Med 2014; 6: 1542-1560.
67. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K et al. Mutational processes molding the genomes of 21 breast cancers. Cell 2012; 149: 979-993.
68. Skibinski A, Breindel JL, Prat A, Galván P, Smith E, Rolfs A et al. The Hippo transducer TAZ interacts with the SWI/SNF complex to regulate breast epithelial lineage commitment. Cell Rep 2014; 6: 1059-1072.
69. Chen Q, Zhang N, Gray RS, Li H, Ewald AJ, Zahnow CA et al. A temporal requirement for Hippo signaling in mammary gland differentiation, growth, and tumorigenesis. Gene Dev 2014; 28: 432-437.
70. Gusterson BA, Ross DT, Heath VJ, Stein T. Basal cytokeratins and their relationship to the cellular origin and functional classification of breast cancer. Breast Cancer Res 2005; 7: 143-148.
71. Mani SA, Guo W, Liao M, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
72. Morel A-, Lièvre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008; 3: 8.
73. Tarin D. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 2005; 65: 5996-6000.
74. Chui MH. Insights into cancer metastasis from a clinicopathologic perspective: Epithelial-Mesenchymal Transition is not a necessary step. Int J Cancer 2013; 132: 1487-1495.
75. Sarrió 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: 989-997.
76. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO et al. Normal and neoplastic nonstem cells can spontaneously convert to a stemlike state. Proc Natl Acad Sci USA 2011; 108: 7950-7955.
77. 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.
78. Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Göktuna SI, Ziegler PK et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stemcell-like properties. Cell 2013; 152: 25-38.
79. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci USA 1992; 89: 10578-10582.
80. Wagner K, Boulanger CA, Henry MD, Sgagias M, Hennighausen L, Smith GH. An adjunct mammary epithelial cell population in parous females: Its role in functional adaptation and tissue renewal. Development 2002; 129: 1377-1386.
81. Boulanger CA, Wagner K, Smith GH. Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-?1 expression. Oncogene 2005; 24: 552-560.
82. Matulka LA, Triplett AA, Wagner K. Parity-induced mammary epithelial cells are multipotent and express cell surface markers associated with stem cells. Dev Biol 2007; 303: 29-44.
83. Chang TH, Kunasegaran K, Tarulli GA, De Silva D, Voorhoeve PM, Pietersen AM. New insights into lineage restriction of mammary gland epithelium using parityidentified mammary epithelial cells. Breast Cancer Res 2014; 16: 1.
84. Jeselsohn R, Brown NE, Arendt L, Klebba I, Hu MG, Kuperwasser C et al. Cyclin D1 kinase activity is required for the self-renewal of mammary stem and progenitor cells that are targets of MMTV-ErbB2 tumorigenesis. Cancer Cell 2010; 17: 65-76.
85. Henry MD, Triplett AA, Oh KB, Smith GH, Wagner K. Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice. Oncogene 2004; 23: 6980-6985.
86. Hollern DP, Andrechek ER. A genomic analysis of mouse models of breast cancer reveals molecular features of mouse models and relationships to human breast cancer. Breast Cancer Res 2014; 16: 3.
87. Pfefferle AD, Herschkowitz JI, Usary J, Harrell JC, Spike BT, Adams JR et al. Transcriptomic classification of genetically engineered mouse models of breast cancer identifies human subtype counterparts. Genome Biol 2013; 14: R125.