Histological and molecular types of breast cancer: Is there a unifying taxonomy?

Nature Reviews Clinical Oncology

Volumn 6, Issue 12, 2009, Pages 718-730

  Weigelt, Britta ^a   Reis Filho, Jorge S ^b  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; CANCER CLASSIFICATION; CANCER GRADING; CANCER MODEL; CANCER MORPHOLOGY; CHROMOSOME ABERRATION; CORRELATIONAL STUDY; GENETIC ANALYSIS; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; HISTOPATHOLOGY; HUMAN; INVASIVE CARCINOMA; MICROARRAY ANALYSIS; MOLECULAR RECOGNITION; MOLECULARLY TARGETED THERAPY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TRANSCRIPTOMICS; BREAST TUMOR; CANCER STAGING; CLASSIFICATION; FEMALE; GENE EXPRESSION PROFILING; PATHOLOGY; PROGNOSIS;

BREAST NEOPLASMS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; NEOPLASM STAGING; PROGNOSIS;

EID: 75649149550     PISSN: 17594774     EISSN: 17594782     Source Type: Journal    
DOI: 10.1038/nrclinonc.2009.166     Document Type: Review

References (104)

1. Reis-Filho, J. S. & Lakhani, S. R. Breast cancer special types: why bother? J. Pathol. 216, 394-398 (2008).
2. Simpson, P. T., Reis-Filho, J. S., Gale, T. & Lakhani, S. R. Molecular evolution of breast cancer. J. Pathol. 205, 248-254 (2005).
3. Vargo-Gogola, T. & Rosen, J. M. Modelling breast cancer: one size does not fit all. Nat. Rev. Cancer 7, 659-672 (2007).
4. Perou, C. M. et al. Molecular portraits of human breast tumours. Nature 406, 747-752 (2000).
5. Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869-10874 (2001).
6. Sorlie, T. et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 100, 8418-8423 (2003).
7. Hu, Z. et al. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 7, 96 (2006).
8. Scarff, R. W. & Torloni, H. Histological Typing of Breast Tumours (WHO, Geneva, 1968).
9. Azzopardi, J. G., Ahmed, A. & Millis, R. R. Problems in Breast Pathology (W. B. Saunders Company Ltd, London, 1979).
10. Azzopardi, J. G. et al. The World Health Organization histological typing of breast tumors: second edition. The World Health Organization. Am. J. Clin. Pathol. 78, 806-816 (1982).
11. Huvos, A. G., Lucas, J. C. Jr & Foote, F. W. Jr. Metaplastic breast carcinoma: rare form of mammary cancer. NY State J. Med. 73, 1078-1082 (1973).
12. Tavassoli, F. A. Pathology of the Breast (Appleton & Lange, Stamford, 1999).
13. Rosen, P. P. Rosen's Breast Pathology (Lippincott Williams & Wilkins, Philadelphia, 2001).
14. Page, D. L. & Anderson, T. J. Diagnostic Histopathology of the Breast (Churchill Livingstone, edinburgh, 1987).
15. Elston, C. W. & ellis, I. O. 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 19, 403-410 (1991).
16. Ellis, I. O. et al. Pathological prognostic factors in breast cancer. II. Histological type: relationship with survival in a large study with long-term follow-up. Histopathology 20, 479-489 (1992).
17. Longacre, T. A. et al. Interobserver agreement and reproducibility in classification of invasive breast carcinoma: an NCI breast cancer family registry study. Mod. Pathol. 19, 195-207 (2006).
18. Rakha, e. A. et al. Prognostic significance of Nottingham histologic grade in invasive breast carcinoma. J. Clin. Oncol. 26, 3153-3158 (2008).
19. Habel, L. A. et al. A population-based study of tumor gene expression and risk of breast cancer death among lymph node-negative patients. Breast Cancer Res. 8, R25 (2006).
20. van de vijver, M. J. et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (2002).
21. Sotiriou, C. et al. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J. Natl Cancer Inst. 98, 262-272 (2006).
22. Ellis, P. et al. in WHO Classification of Tumours. Pathology and Genetics of Tumours of the Breast and Female Genital Organs (eds Tavassoli, F. A. & Devilee, P) 13-59 (Lyon Press, Lyon, 2003).
23. Rakha, e. A. et al. Histologic grading is an independent prognostic factor in invasive lobular carcinoma of the breast. Breast Cancer Res. Treat 111, 121-127 (2008).
24. Wang, Y. et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365, 671-679 (2005).
25. van 't veer, L. J. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536 (2002).
26. Wirapati, P. 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. 10, R65 (2008).
27. Geyer, F. C. & Reis-Filho, J. S. Microarray-based gene expression profiling as a clinical tool for breast cancer management: are we there yet? Int. J. Surg. Pathol. 17, 285-302 (2008).
28. Farmer, P. et al. Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 24, 4660-4671 (2005).
29. Abdullah-Sayani, A., Bueno-de-Mesquita, J. M. & van de vijver, M. J. Technology Insight: tuning into the genetic orchestra using microarrays: limitations of DNA microarrays in clinical practice. Nat. Clin. Pract. Oncol. 3, 501-516 (2006).
30. Rosen, P. P. & Oberman, H. A. Tumors of the Mammary Gland (Armed Forces Institute of Pathology, Washington, DC, 1993).
31. Tavassoli, F. A. Classification of metaplastic carcinomas of the breast. Pathol. Annu. 27 (Pt 2), 89-119 (1992).
32. Sakamoto, G. Histological classification of breast cancer [Japanese]. Gan No Rinsho (May Suppl.), 105-113 (1985).
33. Sakamoto, G. Histological classification of breast cancer: 2 [Japanese]. Gan No Rinsho (Jan Suppl.), 197-204 (1986).
34. Eusebi, V., Damiani, S., Ellis, I. O., Azzopardi, J. G. & Rosai J. Breast tumor resembling the tall cell variant of papillary thyroid carcinoma: report of 5 cases. Am. J. Surg. Pathol. 27, 1114-1118 (2003).
35. Asioli, S. et al. Polymorphous adenocarcinoma of the breast: report of three cases. Virchows Arch. 448, 29-34 (2006).
36. Collins, L. C. et al. Intracystic papillary carcinomas of the breast: a reevaluation using a panel of myoepithelial cell markers. Am. J. Surg. Pathol. 30, 1002-1007 (2006).
37. Mulligan, A. M. & O'Malley, F. P. Metastatic potential of encapsulated (intracystic) papillary carcinoma of the breast: a report of 2 cases with axillary lymph node micrometastases. Int. J. Surg. Pathol. 15, 143-147 (2007).
38. Leibl, S. & Moinfar, F. Mammary NOS-type sarcoma with CD10 expression: a rare entity with features of myoepithelial differentiation. Am. J. Surg. Pathol. 30, 450-456 (2006).
39. Wellings, S. R. & Jensen, H. M. On the origin and progression of ductal carcinoma in the human breast. J. Natl Cancer Inst. 50, 1111-1118 (1973).
40. Wellings, S. R., Jensen, H. M. & Marcum, R. G. An atlas of subgross pathology of the human breast with special reference to possible precancerous lesions. J. Natl Cancer Inst. 55, 231-273 (1975).
41. Potti, A. et al. Genomic signatures to guide the use of chemotherapeutics. Nat. Med. 12, 1294-1300 (2006).
42. Peppercorn, J., Perou, C. M. & Carey, L. A. Molecular subtypes in breast cancer evaluation and management: divide and conquer. Cancer Invest. 26, 1-10 (2008).
43. Gusterson, B. Do 'basal-like' breast cancers really exist? Nat. Rev. Cancer 9, 128-134 (2009).
44. Moinfar, F. Is 'basal-like' carcinoma of the breast a distinct clinicopathological entity? A critical review with cautionary notes. Pathobiology 75, 119-131 (2008).
45. Rakha, e. A. et al. Morphological and immunophenotypic analysis of breast carcinomas with basal and myoepithelial differentiation. J. Pathol. 208, 495-506 (2006).
46. Livasy, C. A. et al. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod. Pathol. 19, 264-271 (2006).
47. Rouzier, R. et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin. Cancer Res. 11, 5678-5685 (2005).
48. Parker, J. S. et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol. 27, 1160-1167 (2009).
49. Doane, A. S. et al. An estrogen receptor-negative breast cancer subset characterized by a hormonally regulated transcriptional program and response to androgen. Oncogene 25, 3994-4008 (2006).
50. Weigelt, B. et al. Refinement of breast cancer classification by molecular characterization of histological special types. J. Pathol. 216, 141-150 (2008).
51. Lien, H. C. et al. Molecular signatures of metaplastic carcinoma of the breast by largescale transcriptional profiling: identification of genes potentially related to epithelial-mesenchymal transition. Oncogene 26, 7859-7871 (2007).
52. Bertucci, F. et al. Lobular and ductal carcinomas of the breast have distinct genomic and expression profiles. Oncogene 27, 5359-5372 (2008).
53. Zhao, H. et al. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol. Biol. Cell 15, 2523-2536 (2004).
54. Korkola, J. e. et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 63, 7167-7175 (2003).
55. Weigelt, B., Kreike, B. & Reis-Filho, J. S. Metaplastic breast carcinomas are basal-like breast cancers: a genomic profiling analysis. Breast Cancer Res. Treat. 117, 273-280 (2008).
56. Bertucci, F. et al. Gene expression profiling shows medullary breast cancer is a subgroup of basal breast cancers. Cancer Res. 66, 4636-4644 (2006).
57. Jacquemier, J. et al. Typical medullary breast carcinomas have a basal/myoepithelial phenotype. J. Pathol. 207, 260-268 (2005).
58. Vincent-Salomon, A. et al. Identification of typical medullary breast carcinoma as a genomic sub-group of basal-like carcinomas, a heterogeneous new molecular entity. Breast Cancer Res. 9, R24 (2007).
59. Azoulay, S. et al. KIT is highly expressed in adenoid cystic carcinoma of the breast, a basal-like carcinoma associated with a favorable outcome. Mod. Pathol. 18, 1623-1631 (2005).
60. Reis-Filho, J. S. et al. Metaplastic breast carcinomas are basal-like tumours. Histopathology 49, 10-21 (2006).
61. Hayes, M. J., Thomas, D., emmons, A., Giordano, T. J. & Kleer, C. G. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin. Cancer Res. 14, 4038-4044 (2008).
62. Stingl, J. & Caldas, C. Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat. Rev. Cancer 7, 791-799 (2007).
63. Dontu, G., el-Ashry, D. & Wicha, M. S. Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol. Metab. 15, 193-197 (2004).
64. Behbod, F. & Rosen, J. M. Will cancer stem cells provide new therapeutic targets? Carcinogenesis 26, 703-711 (2005).
65. Hosey, A. M. et al. Molecular basis for estrogen receptor alpha deficiency in BRCA1-linked breast cancer. J. Natl Cancer Inst. 99, 1683-1694 (2007).
66. Liu, X. 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 104, 12111-12116 (2007).
67. McCarthy, A. et al. A mouse model of basal-like breast carcinoma with metaplastic elements. J. Pathol. 211, 389-398 (2007).
68. Polyak, K. Breast cancer: origins and evolution. J. Clin. Invest. 117, 3155-3163 (2007).
69. Tognon, C. et al. expression of the ETV6-NTRK3 gene fusion as a primary event in human secretory breast carcinoma. Cancer Cell 2, 367-376 (2002).
70. Marchio, C. et al. Genomic and immunophenotypical characterization of pure micropapillary carcinomas of the breast. J. Pathol. 215, 398-410 (2008).
71. Letessier, A. et al. ETV6 gene rearrangements in invasive breast carcinoma. Genes Chromosomes Cancer 44, 103-108 (2005).
72. Makretsov, N. et al. A fluorescence in situ hybridization study of ETV6-NTRK3 fusion gene in secretory breast carcinoma. Genes Chromosomes Cancer 40, 152-157 (2004).
73. Reis-Filho, J. S. et al. Is acinic cell carcinoma a variant of secretory carcinoma? A FISH study using eTv6 'split apart' probes. Histopathology 52, 840-846 (2008).
74. Nassar, H. Carcinomas with micropapillary morphology: clinical significance and current concepts. Adv. Anat. Pathol. 11, 297-303 (2004).
75. Thor, A. D. et al. Invasive micropapillary carcinoma of the breast is associated with chromosome 8 abnormalities detected by comparative genomic hybridization. Hum. Pathol. 33, 628-631 (2002).
76. Hanby, A. M. & Hughes, T. A. In situ and invasive lobular neoplasia of the breast. Histopathology 52, 58-66 (2008).
77. Mathieu, M. C. et al. The poor responsiveness of infiltrating lobular breast carcinomas to neoadjuvant chemotherapy can be explained by their biological profile. Eur. J. Cancer 40, 342-351 (2004).
78. Vos, C. B. et al. E-cadherin inactivation in lobular carcinoma in situ of the breast: an early event in tumorigenesis. Br. J. Cancer 76, 1131-1133 (1997).
79. Droufakou, S. et al. Multiple ways of silencing E-cadherin gene expression in lobular carcinoma of the breast. Int. J. Cancer 92, 404-408 (2001).
80. Sarrio, D. et al. epigenetic and genetic alterations of APC and CDH1 genes in lobular breast cancer: relationships with abnormal E-cadherin and catenin expression and microsatellite instability. Int. J. Cancer 106, 208-215 (2003).
81. Derksen, P. W. et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10, 437-449 (2006).
82. Reis-Filho, J. S. et al. EGFR amplification and lack of activating mutations in metaplastic breast carcinomas. J. Pathol. 209, 445-453 (2006).
83. Leibl, S., Gogg-Kammerer, M., Sommersacher, A., Denk, H. & Moinfar, F. Metaplastic breast carcinomas: are they of myoepithelial differentiation? Immunohistochemical profile of the sarcomatoid subtype using novel myoepithelial markers. Am. J. Surg. Pathol. 29, 347-353 (2005).
84. Leibl, S. & Moinfar, F. Metaplastic breast carcinomas are negative for Her-2 but frequently express eGFR (Her-1): potential relevance to adjuvant treatment with eGFR tyrosine kinase inhibitors? J. Clin. Pathol. 58, 700-704 (2005).
85. Turner, N. C. et al. BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene 26, 2126-2132 (2007).
86. Turner, N. C. & Reis-Filho, J. S. Basal-like breast cancer and the BRCA1 phenotype. Oncogene 25, 5846-5853 (2006).
87. Lien, H. C. et al. p53 overexpression and mutation in metaplastic carcinoma of the breast: genetic evidence for a monoclonal origin of both the carcinomatous and the heterogeneous sarcomatous components. J. Pathol. 204, 131-139 (2004).
88. Simpson, P. T. et al. Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am. J. Surg. Pathol. 29, 734-746 (2005).
89. Abdel-Fatah, T. M. et al. High frequency of coexistence of columnar cell lesions, lobular neoplasia, and low grade ductal carcinoma in situ with invasive tubular carcinoma and invasive lobular carcinoma. Am. J. Surg. Pathol. 31, 417-426 (2007).
90. Abdel-Fatah, T. M. et al. Morphologic and molecular evolutionary pathways of low nuclear grade invasive breast cancers and their putative precursor lesions: further evidence to support the concept of low nuclear grade breast neoplasia family. Am. J. Surg. Pathol. 32, 513-523 (2008).
91. Chin, K. et al. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 10, 529-541 (2006).
92. Natrajan, R. et al. Tiling path genomic profiling of grade 3 invasive ductal breast cancers. Clin. Cancer Res. 15, 2711-2722 (2009).
93. Marchio, C. et al. Mixed micropapillary-ductal carcinomas of the breast: a genomic and immunohistochemical analysis of morphologically distinct components. J. Pathol. 218, 301-315 (2009).
94. Slamon, D. J. et al. Human breast cancer: correlation of relapse and survival with amplification of the HeR-2/neu oncogene. Science 235, 177-182 (1987).
95. Bernard-Pierrot, I. et al. Characterization of the recurrent 8p11-12 amplicon identifies PPAPDC1B, a phosphatase protein, as a new therapeutic target in breast cancer. Cancer Res. 68, 7165-7175 (2008).
96. Reis-Filho, J. S. et al. FGFR1 emerges as a potential therapeutic target for lobular breast carcinomas. Clin. Cancer Res. 12, 6652-6662 (2006).
97. Cuny, M. et al. Relating genotype and phenotype in breast cancer: an analysis of the prognostic significance of amplification at eight different genes or loci and of p53 mutations. Cancer Res. 60, 1077-1083 (2000).
98. Elbauomy Elsheikh, S. et al. FGFR1 amplification in breast carcinomas: a chromogenic in situ hybridisation analysis. Breast Cancer Res. 9, R23 (2007).
99. Hennessy, B. T. et al. Biphasic metaplastic sarcomatoid carcinoma of the breast. Ann. Oncol. 17, 605-613 (2006).
100. Ashworth, A. A synthetic lethal therapeutic approach: poly(ADP) ribose polymerase inhibitors for the treatment of cancers deficient in DNA double-strand break repair. J. Clin. Oncol. 26, 3785-3790 (2008).
101. Flagiello, D. et al. Highly recurrent der(1;16) (q10;p10) and other 16q arm alterations in lobular breast cancer. Genes Chromosomes Cancer 23, 300-306 (1998).
102. Calza, S. et al. Intrinsic molecular signature of breast cancer in a population-based cohort of 412 patients. Breast Cancer Res. 8, R34 (2006).
103. Fan, C. et al. Concordance among gene-expression-based predictors for breast cancer. N. Engl. J. Med. 355, 560-569 (2006).
104. Rody, A. et al. The erbB2+ cluster of the intrinsic gene set predicts tumor response of breast cancer patients receiving neoadjuvant chemotherapy with docetaxel, doxorubicin and cyclophosphamide within the GePARTRIO trial. Breast 16, 235-240 (2007).