The molecular pathology of breast cancer progression

Journal of Pathology

Volumn 223, Issue 2, 2011, Pages 308-318

  Bombonati, Alessandro ^a   Sgroi, Dennis C ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

atypical ductal hyperplasia; breast cancer progression; ductal carcinoma in situ; epigenetics; flat epithelial atypia; genetics; transcriptomics; tumour environment

Indexed keywords

BREAST CANCER; CANCER GROWTH; EPIGENETICS; EPITHELIUM CELL; EX VIVO STUDY; GENETIC TRANSCRIPTION; HUMAN; PRIORITY JOURNAL; REVIEW;

EID: 78650028237     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2808     Document Type: Review

References (120)

1. Jemal A, Siegel R, Xu J, et al., Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300.
2. Li CI, Anderson BO, Daling JR, et al., Trends in incidence rates of invasive lobular and ductal breast carcinoma. J Am Med Assoc 2003; 289: 1421-1424.
3. Li CI, Daling JR, Malone KE,. Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol 2003; 21: 28-34.
4. Jemal A, Siegel R, Ward E, et al., Cancer statistics, 2008. CA Cancer J Clin 2008; 58: 71-96.
5. Berry DA, Cronin KA, Plevritis SK, et al., Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med 2005; 353: 1784-1792.
6. Jatoi I, Chen BE, Anderson WF, et al., Breast cancer mortality trends in the United States according to estrogen receptor status and age at diagnosis. J Clin Oncol 2007; 25: 1683-1690.
7. Tavassoli F. A, DP,. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of the Breast and Female Genital Organs. WHO: Geneva, 2003; 9-19.
8. Rakha EA, Putti TC, Abd El-Rehim DM, et al., Morphological and immunophenotypic analysis of breast carcinomas with basal and myoepithelial differentiation. J Pathol 2006; 208: 495-506.
9. Wellings SR, Jensen HM,. On the origin and progression of ductal carcinoma in the human breast. J Natl Cancer Inst 1973; 50: 1111-1118.
10. Wellings SR, Jensen HM, Marcum RG,. An atlas of subgross pathology of the human breast with special reference to possible precancerous lesions. J Natl Cancer Inst 1975; 55: 231-273.
11. Oyama T, Maluf H, Koerner F,. Atypical cystic lobules: an early stage in the formation of low-grade ductal carcinoma in situ. Virchows Arch 1999; 435: 413-421.
12. Oyama T, Iijima K, Takei H, et al., Atypical cystic lobule of the breast: an early stage of low-grade ductal carcinoma in-situ. Breast Cancer 2000; 7: 326-331.
13. Lerwill MF,. Flat epithelial atypia of the breast. Arch Pathol Lab Med 2008; 132: 615-621.
14. Page DL, Dupont WD, Rogers LW, et al., Atypical hyperplastic lesions of the female breast. A long-term follow-up study. Cancer 1985; 55: 2698-2708.
15. Dupont WD, Page DL,. Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med 1985; 312: 146-151.
16. Kusama R, Fujimori M, Matsuyama I, et al., Clinicopathological characteristics of atypical cystic duct (ACD) of the breast: assessment of ACD as a precancerous lesion. Pathol Int 2000; 50: 793-800.
17. Otterbach F, Bankfalvi A, Bergner S, et al., Cytokeratin 5/6 immunohistochemistry assists the differential diagnosis of atypical proliferations of the breast. Histopathology 2000; 37: 232-240.
18. Boecker W, Moll R, Dervan P, et al., Usual ductal hyperplasia of the breast is a committed stem (progenitor) cell lesion distinct from atypical ductal hyperplasia and ductal carcinoma in situ. J Pathol 2002; 198: 458-467.
19. Bonnet D, Dick JE,. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
20. Nowell PC,. The clonal evolution of tumor cell populations. Science 1976; 194: 23-28.
21. Reya T, Morrison SJ, Clarke MF, et al., Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
22. Clarke MF, Dick JE, Dirks PB, et al., Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-9344.
23. Barabe F, Kennedy JA, Hope KJ, et al., Modeling the initiation and progression of human acute leukemia in mice. Science 2007; 316: 600-604.
24. Stingl J, Eaves CJ, Kuusk U, et al., Phenotypic and functional characterization in vitro of a multipotent epithelial cell present in the normal adult human breast. Differentiation 1998; 63: 201-213.
25. Kordon EC, Smith GH,. An entire functional mammary gland may comprise the progeny from a single cell. Development 1998; 125: 1921-1930.
26. Dontu G, Abdallah WM, Foley JM, et al., In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17: 1253-1270.
27. Baik I, Becker PS, DeVito WJ, et al., Stem cells and prenatal origin of breast cancer. Cancer Causes Control 2004; 15: 517-530.
28. Gudjonsson T, Villadsen R, Nielsen HL, et al., Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev 2002; 16: 693-706.
29. Stingl J, Raouf A, Emerman JT, et al., Epithelial progenitors in the normal human mammary gland. J Mammary Gland Biol Neoplasia 2005; 10: 49-59.
30. Villadsen R, Fridriksdottir AJ, Ronnov-Jessen L, et al., Evidence for a stem cell hierarchy in the adult human breast. J Cell Biol 2007; 177: 87-101.
31. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al., Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988. (Pubitemid 36418143)
32. Dontu G, El-Ashry D, Wicha MS,. Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol Metab 2004; 15: 193-197. (Pubitemid 38833988)
33. Ponti D, Zaffaroni N, Capelli C, et al., Breast cancer stem cells: an overview. Eur J Cancer 2006; 42: 1219-1224.
34. Ginestier C, Hur MH, Charafe-Jauffret E, 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.
35. Pece S, Tosoni D, Confalonieri S, et al., Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010; 140: 62-73.
36. Asselin-Labat ML, Vaillant F, Sheridan JM, et al., Control of mammary stem cell function by steroid hormone signalling. Nature 2010; 465: 798-802.
37. Joshi PA, Jackson HW, Beristain AG, et al., Progesterone induces adult mammary stem cell expansion. Nature 2010; 465: 803-807.
38. Tu SM, Lin SH, Logothetis CJ,. Stem-cell origin of metastasis and heterogeneity in solid tumours. Lancet Oncol 2002; 3: 508-513.
39. Dontu G, Al-Hajj M, Abdallah WM, et al., Stem cells in normal breast development and breast cancer. Cell Prolif 2003; 369 (suppl 1): 59-72. (Pubitemid 37521844)
40. Lim E, Vaillant F, Wu D, et al., Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009; 15: 907-913.
41. Molyneux G, Geyer FC, Magnay FA, 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.
42. Weigelt B, Geyer FC, Reis-Filho JS,. Histological types of breast cancer: how special are they? Mol Oncol 2010; 4: 192-208.
43. Elston CW, Ellis IO,. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991; 19: 403-410.
44. Elston CW, Ellis IO,. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. C. W. Elston & I. O. Ellis, Histopathology 1991; 19; 403-410. Histopathology 2002; 41: 151-152; discussion, 152-153.
45. Rakha EA, Reis-Filho JS, Baehner F, et al., Breast cancer prognostic classification in the molecular era: the role of histological grade. Breast Cancer Res 2010; 12: 207.
46. Tirkkonen M, Tanner M, Karhu R, et al., Molecular cytogenetics of primary breast cancer by CGH. Genes Chromosomes Cancer 1998; 21: 177-184.
47. Roylance R, Gorman P, Harris W, et al., Comparative genomic hybridization of breast tumors stratified by histological grade reveals new insights into the biological progression of breast cancer. Cancer Res 1999; 59: 1433-1436.
48. Buerger H, Otterbach F, Simon R, et al., Different genetic pathways in the evolution of invasive breast cancer are associated with distinct morphological subtypes. J Pathol 1999; 189: 521-526.
49. Buerger H, Mommers EC, Littmann R, et al., Ductal invasive G2 and G3 carcinomas of the breast are the end stages of at least two different lines of genetic evolution. J Pathol 2001; 194: 165-170.
50. Duffy SW, Tabar L, Fagerberg G, et al., Breast screening, prognostic factors and survival-results from the Swedish two county study. Br J Cancer 1991; 64: 1133-1138.
51. Rajakariar R, Walker RA,. Pathological and biological features of mammographically detected invasive breast carcinomas. Br J Cancer 1995; 71: 150-154.
52. Perou CM, Sorlie T, Eisen MB, et al., Molecular portraits of human breast tumours. Nature 2000; 406: 747-752.
53. Sorlie T, Perou CM, Tibshirani R, et al., Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001; 98: 10869-10874.
54. Sorlie T, Tibshirani R, Parker J, et al., Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 2003; 100: 8418-8423.
55. Sotiriou C, Neo SY, McShane LM, et al., Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci USA 2003; 100: 10393-10398.
56. Hu Z, Fan C, Oh DS, et al., The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 2006; 7: 96-103.
57. Loi S, Haibe-Kains B, Desmedt C, et al., Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol 2007; 25: 1239-1246.
58. Voduc KD, Cheang MC, Tyldesley S, et al., Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol 2010; 28: 1684-1691.
59. Carey LA, Perou CM, Livasy CA, et al., Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. J Am Med Assoc 2006; 295: 2492-2502.
60. Lusa L, McShane LM, Reid JF, et al., Challenges in projecting clustering results across gene expression-profiling datasets. J Natl Cancer Inst 2007; 99: 1715-1723.
61. Wirapati P, Sotiriou C, Kunkel S, et al., Meta-analysis of gene expression profiles in breast cancer: toward a unified understanding of breast cancer subtyping and prognosis signatures. Breast Cancer Res 2008; 10: R65.
62. Weigelt B, Mackay A, A'Hern R, et al., Breast cancer molecular profiling with single sample predictors: a retrospective analysis. Lancet Oncol 2010; 11: 339-349.
63. Farmer P, Bonnefoi H, Becette V, et al., Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 2005; 24: 4660-4671.
64. Weigelt B, Baehner FL, Reis-Filho JS,. The contribution of gene expression profiling to breast cancer classification, prognostication and prediction: a retrospective of the last decade. J Pathol 2010; 220: 263-280.
65. Sotiriou C, Pusztai L,. Gene-expression signatures in breast cancer. N Engl J Med 2009; 360: 790-800.
66. Paik S, Shak S, Tang G, et al., A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004; 351: 2817-2826.
67. van 't Veer LJ, Dai H, van de Vijver MJ, et al., Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002; 415: 530-536.
68. Ma XJ, Wang Z, Ryan PD, et al., A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 2004; 5: 607-616.
69. Wang Y, Klijn JG, Zhang Y, et al., Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005; 365: 671-679.
70. Fan C, Oh DS, Wessels L, et al., Concordance among gene-expression-based predictors for breast cancer. N Engl J Med 2006; 355: 560-569.
71. Haibe-Kains B, Desmedt C, Piette F, et al., Comparison of prognostic gene expression signatures for breast cancer. BMC Genomics 2008; 9: 394.
72. Sotiriou C, Wirapati P, Loi S, et al., Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst 2006; 98: 262-272.
73. Ma XJ, Salunga R, Dahiya S, et al., A five-gene molecular grade index and HOXB13:IL17BR are complementary prognostic factors in early stage breast cancer. Clin Cancer Res 2008; 14: 2601-2608.
74. Liedtke C, Hatzis C, Symmans WF, et al., Genomic grade index is associated with response to chemotherapy in patients with breast cancer. J Clin Oncol 2009; 27: 3185-3191.
75. Toussaint J, Sieuwerts AM, Haibe-Kains B, et al., Improvement of the clinical applicability of the Genomic Grade Index through a qRT-PCR test performed on frozen and formalin-fixed paraffin-embedded tissues. BMC Genomics 2009; 10: 424.
76. Nishizaki T, Chew K, Chu L, et al., Genetic alterations in lobular breast cancer by comparative genomic hybridization. Int J Cancer 1997; 74: 513-517.
77. Loveday RL, Greenman J, Simcox DL, et al., Genetic changes in breast cancer detected by comparative genomic hybridisation. Int J Cancer 2000; 86: 494-500.
78. Gunther K, Merkelbach-Bruse S, Amo-Takyi BK, et al., Differences in genetic alterations between primary lobular and ductal breast cancers detected by comparative genomic hybridization. J Pathol 2001; 193: 40-47.
79. Richard F, Pacyna-Gengelbach M, Schluns K, et al., Patterns of chromosomal imbalances in invasive breast cancer. Int J Cancer 2000; 89: 305-310.
80. Lakhani SR, Collins N, Sloane JP, et al., Loss of heterozygosity in lobular carcinoma in situ of the breast. Clin Mol Pathol 1995; 48: M74-78.
81. Simpson PT, Reis-Filho JS, Gale T, et al., Molecular evolution of breast cancer. J Pathol 2005; 205: 248-254.
82. Weigelt B, Geyer FC, Natrajan R, et al., The molecular underpinning of lobular histological growth pattern: a genome-wide transcriptomic analysis of invasive lobular carcinomas and grade- and molecular subtype-matched invasive ductal carcinomas of no special type. J Pathol 2010; 220: 45-57.
83. Middleton LP, Palacios DM, Bryant BR, et al., Pleomorphic lobular carcinoma: morphology, immunohistochemistry, and molecular analysis. Am J Surg Pathol 2000; 24: 1650-1656.
84. Simpson PT, Reis-Filho JS, Lambros MB, et al., Molecular profiling pleomorphic lobular carcinomas of the breast: evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol 2008; 215: 231-244.
85. Allred DC, Wu Y, Mao S, et al., Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin Cancer Res 2008; 14: 370-378.
86. Tavassoli FA, Norris HJ,. A comparison of the results of long-term follow-up for atypical intraductal hyperplasia and intraductal hyperplasia of the breast. Cancer 1990; 65: 518-529.
87. Page DL, Rogers LW,. Combined histologic and cytologic criteria for the diagnosis of mammary atypical ductal hyperplasia. Hum Pathol 1992; 23: 1095-1097.
88. Buerger H, Otterbach F, Simon R, et al., Comparative genomic hybridization of ductal carcinoma in situ of the breast-evidence of multiple genetic pathways. J Pathol 1999; 187: 396-402.
89. O'Connell P, Pekkel V, Fuqua SA, et al., Analysis of loss of heterozygosity in 399 premalignant breast lesions at 15 genetic loci. J Natl Cancer Inst 1998; 90: 697-703.
90. Moinfar F, Man YG, Bratthauer GL, et al., Genetic abnormalities in mammary ductal intraepithelial neoplasia-flat type ('clinging ductal carcinoma in situ'): a simulator of normal mammary epithelium. Cancer 2000; 88: 2072-2081.
91. Simpson PT, Gale T, Reis-Filho JS, et al., Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am J Surg Pathol 2005; 29: 734-746.
92. Kasami M, Vnencak-Jones CL, Manning S, et al., Loss of heterozygosity and microsatellite instability in breast hyperplasia. No obligate correlation of these genetic alterations with subsequent malignancy. Am J Pathol 1997; 150: 1925-1932.
93. Boecker W, Buerger H, Schmitz K, et al., Ductal epithelial proliferations of the breast: a biological continuum? Comparative genomic hybridization and high-molecular-weight cytokeratin expression patterns. J Pathol 2001; 195: 415-421.
94. Jones C, Merrett S, Thomas VA, et al., Comparative genomic hybridization analysis of bilateral hyperplasia of usual type of the breast. J Pathol 2003; 199: 152-156.
95. Geyer FC, Kushner YB, Lambros MB, et al., Microglandular adenosis or microglandular adenoma? A molecular genetic analysis of a case associated with atypia and invasive carcinoma. Histopathology 2009; 55: 732-743.
96. Shin SJ, Simpson PT, Da Silva L, et al., Molecular evidence for progression of microglandular adenosis (MGA) to invasive carcinoma. Am J Surg Pathol 2009; 33: 496-504.
97. Ma XJ, Salunga R, Tuggle JT, et al., Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA 2003; 100: 5974-5979.
98. Porter D, Lahti-Domenici J, Keshaviah A, et al., Molecular markers in ductal carcinoma in situ of the breast. Mol Cancer Res 2003; 1: 362-375.
99. Schuetz CS, Bonin M, Clare SE, et al., Progression-specific genes identified by expression profiling of matched ductal carcinomas in situ and invasive breast tumors, combining laser capture microdissection and oligonucleotide microarray analysis. Cancer Res 2006; 66: 5278-5286.
100. Ma XJ, Dahiya S, Richardson E, et al., Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res 2009; 11: R7.
101. Lu YJ, Osin P, Lakhani SR, et al., Comparative genomic hybridization analysis of lobular carcinoma in situ and atypical lobular hyperplasia and potential roles for gains and losses of genetic material in breast neoplasia. Cancer Res 1998; 58: 4721-4727.
102. Mastracci TL, Shadeo A, Colby SM, et al., Genomic alterations in lobular neoplasia: a microarray comparative genomic hybridization signature for early neoplastic proliferation in the breast. Genes Chromosomes Cancer 2006; 45: 1007-1017.
103. Morandi L, Marucci G, Foschini MP, et al., Genetic similarities and differences between lobular in situ neoplasia (LN) and invasive lobular carcinoma of the breast. Virchows Arch 2006; 449: 14-23.
104. Elenbaas B, Weinberg RA,. Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp Cell Res 2001; 264: 169-184.
105. Price JE, Polyzos A, Zhang RD, et al., Tumorigenicity and metastasis of human breast carcinoma cell lines in nude mice. Cancer Res 1990; 50: 717-721.
106. Mehta RR, Graves JM, Hart GD, et al., Growth and metastasis of human breast carcinomas with Matrigel in athymic mice. Breast Cancer Res Treat 1993; 25: 65-71.
107. Sternlicht MD, Kedeshian P, Shao ZM, et al., The human myoepithelial cell is a natural tumor suppressor. Clin Cancer Res 1997; 3: 1949-1958.
108. Allinen M, Beroukhim R, Cai L, et al., Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004; 6: 17-32. (Pubitemid 38903159)
109. Hu M, Yao J, Carroll DK, et al., Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 2008; 13: 394-406.
110. Hu M, Yao J, Cai L, et al., Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 2005; 37: 899-905.
111. Fiegl H, Millinger S, Goebel G, et al., Breast cancer DNA methylation profiles in cancer cells and tumor stroma: association with HER-2/neu status in primary breast cancer. Cancer Res 2006; 66: 29-33.
112. Sgroi DC,. Preinvasive breast cancer. Annu Rev Pathol; 5: 193-221.
113. Lopez-Garcia MA, Geyer FC, Lacroix-Triki M, et al., Breast cancer precursors revisited: molecular features and progression pathways. Histopathology 2010; 57: 171-192.
114. Natrajan R, Lambros MB, Geyer FC, et al., Loss of 16q in high grade breast cancer is associated with estrogen receptor status: evidence for progression in tumors with a luminal phenotype? Genes Chromosomes Cancer 2009; 48: 351-365.
115. Mullighan CG, Phillips LA, Su X, et al., Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 2008; 322: 1377-1380.
116. Godin-Heymann N, Ulkus L, Brannigan BW, et al., The T790M 'gatekeeper' mutation in EGFR mediates resistance to low concentrations of an irreversible EGFR inhibitor. Mol Cancer Ther 2008; 7: 874-879.
117. Heinrich MC, Maki RG, Corless CL, et al., Primary and secondary kinase genotypes correlate with the biological and clinical activity of sunitinib in imatinib-resistant gastrointestinal stromal tumor. J Clin Oncol 2008; 26: 5352-5359.
118. Geyer FC, Weigelt B, Natrajan R, et al., Molecular analysis reveals a genetic basis for the phenotypic diversity of metaplastic breast carcinomas. J Pathol 2010; 220: 562-573.
119. Shah SP, Morin RD, Khattra J, et al., Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009; 461: 809-813.
120. Ding L, Ellis MJ, Li S, et al., Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010; 464: 999-1005.