Home LiteratureArticle Details
PMID: 29276709 Published · epublish English Journal Article Review

Tumor Heterogeneity in Breast Cancer.

Frontiers in medicine ·Vol. 4 ·2017-00-00 ·Pages 227

Turashvili G, Brogi E

Abstract

Breast cancer is a heterogeneous disease and differs greatly among different patients (intertumor heterogeneity) and even within each individual tumor (intratumor heterogeneity). Clinical and morphologic intertumor heterogeneity is reflected by staging systems and histopathologic classification of breast cancer. Heterogeneity in the expression of established prognostic and predictive biomarkers, hormone receptors, and human epidermal growth factor receptor 2 oncoprotein is the basis for targeted treatment. Molecular classifications are indicators of genetic tumor heterogeneity, which is probed with multigene assays and can lead to improved stratification into low- and high-risk groups for personalized therapy. Intratumor heterogeneity occurs at the morphologic, genomic, transcriptomic, and proteomic levels, creating diagnostic and therapeutic challenges. Understanding the molecular and cellular mechanisms of tumor heterogeneity that are relevant to the development of treatment resistance is a major area of research. Despite the improved knowledge of the complex genetic and phenotypic features underpinning tumor heterogeneity, there has been only limited advancement in diagnostic, prognostic, or predictive strategies for breast cancer. The current guidelines for reporting of biomarkers aim to maximize patient eligibility for targeted therapy, but do not take into account intratumor heterogeneity. The molecular classification of breast cancer is not implemented in routine clinical practice. Additional studies and in-depth analysis are required to understand the clinical significance of rapidly accumulating data. This review highlights inter- and intratumor heterogeneity of breast carcinoma with special emphasis on pathologic findings, and provides insights into the clinical significance of molecular and cellular mechanisms of heterogeneity.

Keywords
biomarkers breast cancer genetic markers histopathology tumor heterogeneity
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Turashvili Gulisa
Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, United States.
Brogi Edi
Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, United States.
References (157)
157 references, click to expand
  1. Analytical validation of the PAM50-based Prosigna Breast Cancer Prognostic Gene Signature Assay and nCounter Analysis System using formalin-fixed paraffin-embedded breast tumor specimens.
    BMC Cancer. 2014 Mar 13;14:177 PMID: 24625003
  2. Marked intratumoral heterogeneity of c-myc and cyclinD1 but not of c-erbB2 amplification in breast cancer.
    Lab Invest. 2002 Oct;82(10):1419-26 PMID: 12379776
  3. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer.
    J Clin Oncol. 1999 May;17(5):1474-81 PMID: 10334533
  4. Therapeutic intervention based on circulating tumor cell phenotype in metastatic breast cancer: concept of the DETECT study program.
    Arch Gynecol Obstet. 2016 Feb;293(2):271-81 PMID: 26354331
  5. The perivascular niche regulates breast tumour dormancy.
    Nat Cell Biol. 2013 Jul;15(7):807-17 PMID: 23728425
  6. Microenvironmental regulation of tumor progression and metastasis.
    Nat Med. 2013 Nov;19(11):1423-37 PMID: 24202395
  7. Stochastic fluctuations and distributed control of gene expression impact cellular memory.
    PLoS One. 2014 Dec 22;9(12):e115574 PMID: 25531401
  8. Her2-positive breast cancer: herceptin and beyond.
    Eur J Cancer. 2008 Dec;44(18):2806-12 PMID: 19022660
  9. Efficacy of Lapatinib in Therapy-Resistant HER2-Positive Circulating Tumor Cells in Metastatic Breast Cancer.
    PLoS One. 2015 Jun 17;10(6):e0123683 PMID: 26083256
  10. Identification of cellular and genetic drivers of breast cancer heterogeneity in genetically engineered mouse tumour models.
    J Pathol. 2014 Jun;233(2):124-37 PMID: 24615332
  11. Intra-tumour heterogeneity: a looking glass for cancer?
    Nat Rev Cancer. 2012 Apr 19;12(5):323-34 PMID: 22513401
  12. Factors influencing prognosis in node-negative breast carcinoma: analysis of 767 T1N0M0/T2N0M0 patients with long-term follow-up.
    J Clin Oncol. 1993 Nov;11(11):2090-100 PMID: 8229123
  13. Genetic and phenotypic diversity in breast tumor metastases.
    Cancer Res. 2014 Mar 1;74(5):1338-48 PMID: 24448237
  14. Genetic heterogeneity in HER2 testing in breast cancer: panel summary and guidelines.
    Arch Pathol Lab Med. 2009 Apr;133(4):611-2 PMID: 19391661
  15. Intratumor variation in cell proliferation in breast carcinoma as determined by antiproliferating cell nuclear antigen monoclonal antibody and automated image analysis.
    Am J Clin Pathol. 1993 Mar;99(3):226-31 PMID: 8095363
  16. PIK3CA(H1047R) induces multipotency and multi-lineage mammary tumours.
    Nature. 2015 Sep 3;525(7567):114-8 PMID: 26266975
  17. Circulating tumour cells: the evolving concept and the inadequacy of their enrichment by EpCAM-based methodology for basic and clinical cancer research.
    Ann Oncol. 2014 Aug;25(8):1506-16 PMID: 24651410
  18. Interphase cytogenetics reveals a high incidence of aneuploidy and intra-tumour heterogeneity in breast cancer.
    Br J Cancer. 1995 Jul;72(1):51-5 PMID: 7599066
  19. Monitoring expression of HER-2 on circulating epithelial cells in patients with advanced breast cancer.
    Int J Oncol. 2002 Nov;21(5):1111-7 PMID: 12370762
  20. High-throughput protein expression analysis using tissue microarray technology of a large well-characterised series identifies biologically distinct classes of breast cancer confirming recent cDNA expression analyses.
    Int J Cancer. 2005 Sep 1;116(3):340-50 PMID: 15818618
  21. Supervised risk predictor of breast cancer based on intrinsic subtypes.
    J Clin Oncol. 2009 Mar 10;27(8):1160-7 PMID: 19204204
  22. Circulating tumor cells and response to chemotherapy in metastatic breast cancer: SWOG S0500.
    J Clin Oncol. 2014 Nov 1;32(31):3483-9 PMID: 24888818
  23. Heterogeneity of PIK3CA mutational status at the single cell level in circulating tumor cells from metastatic breast cancer patients.
    Mol Oncol. 2015 Apr;9(4):749-57 PMID: 25539732
  24. Transformation of different human breast epithelial cell types leads to distinct tumor phenotypes.
    Cancer Cell. 2007 Aug;12(2):160-70 PMID: 17692807
  25. Impact of intratumoural heterogeneity on the assessment of Ki67 expression in breast cancer.
    Breast Cancer Res Treat. 2016 Jul;158(2):287-95 PMID: 27380874
  26. Receptor heterogeneity of human breast cancer as measured by multiple intratumoral assays of estrogen and progesterone receptor.
    Eur J Cancer Clin Oncol. 1984 Mar;20(3):375-82 PMID: 6323188
  27. A Long-Lived Luminal Subpopulation Enriched with Alveolar Progenitors Serves as Cellular Origin of Heterogeneous Mammary Tumors.
    Stem Cell Reports. 2015 Jul 14;5(1):60-74 PMID: 26120057
  28. Gene expression pathway analysis to predict response to neoadjuvant docetaxel and capecitabine for breast cancer.
    Breast Cancer Res Treat. 2010 Feb;119(3):685-99 PMID: 20012355
  29. A molecular signature of the Nottingham prognostic index in breast cancer.
    Cancer Res. 2004 May 1;64(9):2962-8 PMID: 15126326
  30. Molecular evolution of breast cancer.
    J Pathol. 2005 Jan;205(2):248-54 PMID: 15641021
  31. Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials.
    Lancet. 2011 Aug 27;378(9793):771-84 PMID: 21802721
  32. Prognostic value of circulating tumor cells in metastatic breast cancer: a systemic review and meta-analysis.
    Clin Transl Oncol. 2016 Mar;18(3):322-30 PMID: 26260915
  33. Marked Intratumoral Heterogeneity of the Proto-Oncogene Her-2/neu Determined by Three Different Detection Systems.
    Breast J. 1999 Nov;5(6):369-374 PMID: 11348316
  34. Heterogeneity of breast cancer metastases: comparison of therapeutic target expression and promoter methylation between primary tumors and their multifocal metastases.
    Clin Cancer Res. 2008 Apr 1;14(7):1938-46 PMID: 18381931
  35. Identification of Biomarkers for Breast Cancer Using Databases.
    J Cancer Prev. 2016 Dec;21(4):235-242 PMID: 28053957
  36. The Warrens and other pioneering clinician pathologists of the Massachusetts General Hospital during its early years: an appreciation on the 200th anniversary of the hospital founding.
    Mod Pathol. 2011 Oct;24(10):1285-94 PMID: 21926958
  37. Breast cancer intratumor genetic heterogeneity: causes and implications.
    Expert Rev Anticancer Ther. 2012 Aug;12(8):1021-32 PMID: 23030222
  38. Defining the cellular precursors to human breast cancer.
    Proc Natl Acad Sci U S A. 2012 Feb 21;109 (8):2772-7 PMID: 21940501
  39. Intratumor Heterogeneity in Breast Cancer.
    Adv Exp Med Biol. 2016;882:169-89 PMID: 26987535
  40. Cytogenetic evidence that circulating epithelial cells in patients with carcinoma are malignant.
    Clin Cancer Res. 2002 Jul;8(7):2073-84 PMID: 12114406
  41. Genome remodelling in a basal-like breast cancer metastasis and xenograft.
    Nature. 2010 Apr 15;464(7291):999-1005 PMID: 20393555
  42. Can ki-67 play a role in prediction of breast cancer patients' response to neoadjuvant chemotherapy?
    Biomed Res Int. 2014;2014:628217 PMID: 24783217
  43. Mutational analysis of single circulating tumor cells by next generation sequencing in metastatic breast cancer.
    Oncotarget. 2016 May 3;7(18):26107-19 PMID: 27034166
  44. Direct evidence for concurrent morphological and genetic heterogeneity in an invasive ductal carcinoma of triple-negative phenotype.
    J Clin Pathol. 2011 Sep;64(9):822-8 PMID: 21676924
  45. Ki-67 as prognostic marker in early breast cancer: a meta-analysis of published studies involving 12,155 patients.
    Br J Cancer. 2007 May 21;96(10):1504-13 PMID: 17453008
  46. Distinct stem cells contribute to mammary gland development and maintenance.
    Nature. 2011 Oct 09;479(7372):189-93 PMID: 21983963
  47. Evolution of the cancer stem cell model.
    Cell Stem Cell. 2014 Mar 6;14(3):275-91 PMID: 24607403
  48. Intratumor heterogeneity of biomarker expression in breast carcinomas.
    Biotech Histochem. 2004 Feb;79(1):25-36 PMID: 15223751
  49. Ki67 in breast cancer: prognostic and predictive potential.
    Lancet Oncol. 2010 Feb;11(2):174-83 PMID: 20152769
  50. The life history of 21 breast cancers.
    Cell. 2012 May 25;149(5):994-1007 PMID: 22608083
  51. The AURORA initiative for metastatic breast cancer.
    Br J Cancer. 2014 Nov 11;111(10):1881-7 PMID: 25225904
  52. 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(4):R65 PMID: 18662380
  53. Intratumor genomic heterogeneity in breast cancer with clonal divergence between primary carcinomas and lymph node metastases.
    Breast Cancer Res Treat. 2007 Apr;102(2):143-55 PMID: 16906480
  54. Estrogen receptor and HER2/neu status affect epigenetic differences of tumor-related genes in primary breast tumors.
    Breast Cancer Res. 2008;10(3):R46 PMID: 18485221
  55. Progesterone receptor status significantly improves outcome prediction over estrogen receptor status alone for adjuvant endocrine therapy in two large breast cancer databases.
    J Clin Oncol. 2003 May 15;21(10):1973-9 PMID: 12743151
  56. Molecular classification of breast carcinomas by immunohistochemical analysis: are we ready?
    Diagn Mol Pathol. 2009 Sep;18(3):125-32 PMID: 19704256
  57. Repeated observation of breast tumor subtypes in independent gene expression data sets.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8418-23 PMID: 12829800
  58. Clinically used breast cancer markers such as estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 are unstable throughout tumor progression.
    J Clin Oncol. 2012 Jul 20;30(21):2601-8 PMID: 22711854
  59. Oestrogen receptors, lactate dehydrogenase and cellularity in human breast cancer.
    Clin Chim Acta. 1988 Jun 30;175(1):89-96 PMID: 3168286
  60. Circulating tumor cells: not all detected cells are bad and not all bad cells are detected.
    J Clin Oncol. 2011 Apr 20;29(12):1508-11 PMID: 21422428
  61. 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 Nov;19(5):403-10 PMID: 1757079
  62. A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer.
    Clin Cancer Res. 2010 Nov 1;16(21):5222-32 PMID: 20837693
  63. Quantification of CpG island methylation in progressive breast lesions from normal to invasive carcinoma.
    Cancer Lett. 2007 Nov 8;257(1):136-44 PMID: 17706863
  64. Whole-genome analysis informs breast cancer response to aromatase inhibition.
    Nature. 2012 Jun 10;486(7403):353-60 PMID: 22722193
  65. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis.
    Lancet. 2014 Jul 12;384(9938):164-72 PMID: 24529560
  66. Targeting the androgen receptor in triple-negative breast cancer.
    Curr Probl Cancer. 2016 Mar - Aug;40(2-4):141-150 PMID: 27816190
  67. Prognostic value of circulating tumor cells in primary and metastatic breast cancer.
    Expert Rev Anticancer Ther. 2012 Feb;12(2):203-14 PMID: 22316368
  68. Identification of molecular apocrine breast tumours by microarray analysis.
    Oncogene. 2005 Jul 7;24(29):4660-71 PMID: 15897907
  69. PIK3CA mutations rarely demonstrate genotypic intratumoral heterogeneity and are selected for in breast cancer progression.
    Breast Cancer Res Treat. 2011 Sep;129(2):635-43 PMID: 21617917
  70. Molecular analysis reveals a genetic basis for the phenotypic diversity of metaplastic breast carcinomas.
    J Pathol. 2010 Apr;220(5):562-73 PMID: 20099298
  71. Pooled Analysis of the Prognostic Relevance of Circulating Tumor Cells in Primary Breast Cancer.
    Clin Cancer Res. 2016 May 15;22(10):2583-93 PMID: 26733614
  72. Prospective study evaluating the impact of tissue confirmation of metastatic disease in patients with breast cancer.
    J Clin Oncol. 2012 Feb 20;30(6):587-92 PMID: 22124102
  73. The differences in the histological types of breast cancer and the response to neoadjuvant chemotherapy: the relationship between the outcome and the clinicopathological characteristics.
    Breast. 2012 Jun;21(3):289-95 PMID: 22277312
  74. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state.
    Proc Natl Acad Sci U S A. 2011 May 10;108(19):7950-5 PMID: 21498687
  75. Genome-driven integrated classification of breast cancer validated in over 7,500 samples.
    Genome Biol. 2014 Aug 28;15(8):431 PMID: 25164602
  76. Phase II trial of bicalutamide in patients with androgen receptor-positive, estrogen receptor-negative metastatic Breast Cancer.
    Clin Cancer Res. 2013 Oct 1;19(19):5505-12 PMID: 23965901
  77. Clinical application of circulating tumor cells in breast cancer: overview of the current interventional trials.
    Cancer Metastasis Rev. 2013 Jun;32(1-2):179-88 PMID: 23129208
  78. mRNA and microRNA expression profiles in circulating tumor cells and primary tumors of metastatic breast cancer patients.
    Clin Cancer Res. 2011 Jun 1;17(11):3600-18 PMID: 21505063
  79. Use of Biomarkers to Guide Decisions on Adjuvant Systemic Therapy for Women With Early-Stage Invasive Breast Cancer: American Society of Clinical Oncology Clinical Practice Guideline.
    J Clin Oncol. 2016 Apr 1;34(10 ):1134-50 PMID: 26858339
  80. Tumour heterogeneity in the clinic.
    Nature. 2013 Sep 19;501(7467):355-64 PMID: 24048068
  81. The prognostic value of circulating tumor cells lacking cytokeratins in metastatic breast cancer patients.
    J Cancer Res Ther. 2013 Jan-Mar;9(1):29-37 PMID: 23575071
  82. PIK3CA mutational status in circulating tumor cells can change during disease recurrence or progression in patients with breast cancer.
    Clin Cancer Res. 2014 Nov 15;20(22):5823-34 PMID: 25398847
  83. Breast cancer intra-tumor heterogeneity.
    Breast Cancer Res. 2014 May 20;16(3):210 PMID: 25928070
  84. Heterogeneity of estrogen receptor expression in circulating tumor cells from metastatic breast cancer patients.
    PLoS One. 2013 Sep 18;8(9):e75038 PMID: 24058649
  85. Tiling path genomic profiling of grade 3 invasive ductal breast cancers.
    Clin Cancer Res. 2009 Apr 15;15(8):2711-22 PMID: 19318498
  86. Prognostic value of HER2-positive circulating tumor cells in patients with metastatic breast cancer.
    Int J Clin Oncol. 2012 Apr;17(2):96-104 PMID: 21671160
  87. Intratumoral heterogeneity of Ki67 expression in early breast cancers exceeds variability between individual tumours.
    Histopathology. 2016 Nov;69(5):849-861 PMID: 27270560
  88. Distribution pattern of the Ki67 labelling index in breast cancer and its implications for choosing cut-off values.
    Breast. 2014 Jun;23(3):259-63 PMID: 24613255
  89. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution.
    Nature. 2009 Oct 8;461(7265):809-13 PMID: 19812674
  90. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression.
    Nat Med. 2011 Mar;17(3):320-9 PMID: 21383745
  91. Expression of the androgen receptor and its correlation with molecular subtypes in 980 chinese breast cancer patients.
    Breast Cancer (Auckl). 2012;6:1-8 PMID: 22259247
  92. The clonal and mutational evolution spectrum of primary triple-negative breast cancers.
    Nature. 2012 Apr 04;486(7403):395-9 PMID: 22495314
  93. Breast carcinoma--rare types: review of the literature.
    Ann Oncol. 2009 Nov;20(11):1763-70 PMID: 19602565
  94. Special types of invasive breast cancer, with clinical implications.
    Am J Surg Pathol. 2003 Jun;27(6):832-5 PMID: 12766589
  95. Reactivation of multipotency by oncogenic PIK3CA induces breast tumour heterogeneity.
    Nature. 2015 Sep 3;525(7567):119-23 PMID: 26266985
  96. The origin of breast tumor heterogeneity.
    Oncogene. 2015 Oct 16;34(42):5309-16 PMID: 25703331
  97. Trastuzumab decreases the incidence of clinical relapses in patients with early breast cancer presenting chemotherapy-resistant CK-19mRNA-positive circulating tumor cells: results of a randomized phase II study.
    Ann Oncol. 2012 Jul;23(7):1744-50 PMID: 22377561
  98. Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer.
    J Clin Oncol. 2006 Aug 10;24(23):3726-34 PMID: 16720680
  99. Prediction of late distant recurrence in patients with oestrogen-receptor-positive breast cancer: a prospective comparison of the breast-cancer index (BCI) assay, 21-gene recurrence score, and IHC4 in the TransATAC study population.
    Lancet Oncol. 2013 Oct;14(11):1067-76 PMID: 24035531
  100. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases.
    Clin Cancer Res. 2004 Oct 15;10(20):6897-904 PMID: 15501967
  101. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer.
    N Engl J Med. 2004 Dec 30;351(27):2817-26 PMID: 15591335
  102. High independent prognostic and predictive value of circulating tumor cells compared with serum tumor markers in a large prospective trial in first-line chemotherapy for metastatic breast cancer patients.
    Ann Oncol. 2012 Mar;23(3):618-24 PMID: 21642515
  103. Breast cancer prognostic classification in the molecular era: the role of histological grade.
    Breast Cancer Res. 2010;12(4):207 PMID: 20804570
  104. Changing levels of circulating tumor cells in monitoring chemotherapy response in patients with metastatic breast cancer.
    Anticancer Res. 2011 Mar;31(3):979-84 PMID: 21498725
  105. Molecular Heterogeneity in Primary Breast Carcinomas and Axillary Lymph Node Metastases Assessed by Genomic Fingerprinting Analysis.
    Cancer Growth Metastasis. 2015 Jul 20;8:15-24 PMID: 26279627
  106. Heterogeneity of miR-10b expression in circulating tumor cells.
    Sci Rep. 2015 Nov 02;5:15980 PMID: 26522916
  107. Use of Biomarkers to Guide Decisions on Systemic Therapy for Women With Metastatic Breast Cancer: American Society of Clinical Oncology Clinical Practice Guideline.
    J Clin Oncol. 2015 Aug 20;33(24):2695-704 PMID: 26195705
  108. Molecular heterogeneity in breast cancer: State of the science and implications for patient care.
    Semin Cell Dev Biol. 2017 Apr;64:65-72 PMID: 27569190
  109. Changes in multiple or sequential estrogen receptor determinations in breast cancer.
    Cancer. 1980 Feb 15;45(4):792-4 PMID: 7357496
  110. The implications of clonal genome evolution for cancer medicine.
    N Engl J Med. 2013 Feb 28;368(9):842-51 PMID: 23445095
  111. A Distributed Network for Intensive Longitudinal Monitoring in Metastatic Triple-Negative Breast Cancer.
    J Natl Compr Canc Netw. 2016 Jan;14 (1):8-17 PMID: 26733551
  112. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups.
    Nature. 2012 Apr 18;486(7403):346-52 PMID: 22522925
  113. Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer.
    Cancer Res. 1997 Apr 15;57(8):1597-604 PMID: 9108466
  114. The EndoPredict score provides prognostic information on late distant metastases in ER+/HER2- breast cancer patients.
    Br J Cancer. 2013 Dec 10;109(12):2959-64 PMID: 24157828
  115. Comprehensive molecular portraits of human breast tumours.
    Nature. 2012 Oct 4;490(7418):61-70 PMID: 23000897
  116. The landscape of cancer genes and mutational processes in breast cancer.
    Nature. 2012 May 16;486(7403):400-4 PMID: 22722201
  117. Circulating tumour cells: insights into tumour heterogeneity.
    J Intern Med. 2013 Aug;274(2):137-43 PMID: 23844916
  118. Androgen Receptor Biology in Triple Negative Breast Cancer: a Case for Classification as AR+ or Quadruple Negative Disease.
    Horm Cancer. 2015 Dec;6(5-6):206-13 PMID: 26201402
  119. Detection of circulating tumor cells during follow-up of patients with early breast cancer: Clinical utility for monitoring of therapy efficacy.
    Scand J Clin Lab Invest. 2014 Mar;74(2):132-42 PMID: 24350991
  120. Circulating tumor cells in breast cancer.
    Mol Oncol. 2016 Mar;10 (3):418-30 PMID: 26809472
  121. The genomic heritage of lymph node metastases: implications for clinical management of patients with breast cancer.
    Ann Surg Oncol. 2008 Apr;15(4):1056-63 PMID: 18246400
  122. In patients with metastatic breast cancer the identification of circulating tumor cells in epithelial-to-mesenchymal transition is associated with a poor prognosis.
    Breast Cancer Res. 2016 Mar 09;18(1):30 PMID: 26961140
  123. Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines.
    PLoS One. 2012;7(5):e33788 PMID: 22586443
  124. Clinical management of breast cancer heterogeneity.
    Nat Rev Clin Oncol. 2015 Jul;12(7):381-94 PMID: 25895611
  125. Breast Tumor Heterogeneity: Source of Fitness, Hurdle for Therapy.
    Mol Cell. 2015 Nov 19;60(4):537-46 PMID: 26590713
  126. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells.
    Cell. 2011 Aug 19;146(4):633-44 PMID: 21854987
  127. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer.
    Breast Cancer Res. 2010;12(5):R68 PMID: 20813035
  128. Cancer stem cell heterogeneity in hereditary breast cancer.
    Breast Cancer Res. 2008;10 (2):105 PMID: 18423071
  129. Sequence analysis of mutations and translocations across breast cancer subtypes.
    Nature. 2012 Jun 20;486(7403):405-9 PMID: 22722202
  130. Histological types of breast cancer: how special are they?
    Mol Oncol. 2010 Jun;4(3):192-208 PMID: 20452298
  131. Intratumoral heterogeneity of immunohistochemical marker expression in breast carcinoma: a tissue microarray-based study.
    Appl Immunohistochem Mol Morphol. 2010 Oct;18(5):433-41 PMID: 20485156
  132. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis.
    J Natl Cancer Inst. 2006 Feb 15;98(4):262-72 PMID: 16478745
  133. Tubular carcinoma of the breast: further evidence to support its excellent prognosis.
    J Clin Oncol. 2010 Jan 1;28(1):99-104 PMID: 19917872
  134. Epithelial-to-mesenchymal transition leads to loss of EpCAM and different physical properties in circulating tumor cells from metastatic breast cancer.
    Oncotarget. 2016 Apr 26;7(17 ):24677-87 PMID: 27013581
  135. Inferring tumor progression from genomic heterogeneity.
    Genome Res. 2010 Jan;20(1):68-80 PMID: 19903760
  136. Convergent loss of PTEN leads to clinical resistance to a PI(3)Kα inhibitor.
    Nature. 2015 Feb 12;518(7538):240-4 PMID: 25409150
  137. Characterization of metastatic heterogeneity among subpopulations of a single mouse mammary tumor: heterogeneity in phenotypic stability.
    Invasion Metastasis. 1983;3(1):22-31 PMID: 6677618
  138. Intratumoral heterogeneity of HER2 gene amplification in breast cancer: its clinicopathological significance.
    Mod Pathol. 2012 Jul;25(7):938-48 PMID: 22388760
  139. HER-2/neu (c-erbB-2) evaluation in primary breast carcinoma by fluorescent in situ hybridization and immunohistochemistry with special focus on intratumor heterogeneity and comparison of invasive and in situ components.
    Appl Immunohistochem Mol Morphol. 2004 Mar;12(1):14-20 PMID: 15163013
  140. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials.
    Lancet. 2005 May 14-20;365(9472):1687-717 PMID: 15894097
  141. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update.
    J Clin Oncol. 2013 Nov 1;31(31):3997-4013 PMID: 24101045
  142. Tumor suppressor p16INK4A regulates polycomb-mediated DNA hypermethylation in human mammary epithelial cells.
    J Biol Chem. 2006 Aug 25;281(34):24790-802 PMID: 16766534
  143. The clonal evolution of tumor cell populations.
    Science. 1976 Oct 1;194(4260):23-8 PMID: 959840
  144. Frequency of HER2 heterogeneity by fluorescence in situ hybridization according to CAP expert panel recommendations: time for a new look at how to report heterogeneity.
    Am J Clin Pathol. 2011 Dec;136(6):864-71 PMID: 22095371
  145. Adjuvant therapies for special types of breast cancer.
    Breast. 2011 Oct;20 Suppl 3:S153-7 PMID: 22015285
  146. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10869-74 PMID: 11553815
  147. Tumor heterogeneity and the biology of cancer invasion and metastasis.
    Cancer Res. 1978 Sep;38(9):2651-60 PMID: 354778
  148. Multiple estrogen receptor assays in human breast cancer.
    Cancer Res. 1983 Jan;43(1):413-6 PMID: 6847780
  149. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype.
    Clin Cancer Res. 2008 Mar 1;14(5):1368-76 PMID: 18316557
  150. Impact of the 21-gene recurrence score assay compared with standard clinicopathologic guidelines in adjuvant therapy selection for node-negative, estrogen receptor-positive breast cancer.
    Ann Surg Oncol. 2011 Nov;18(12):3399-406 PMID: 21537874
  151. American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer.
    J Clin Oncol. 2010 Jun 1;28(16):2784-95 PMID: 20404251
  152. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate.
    BMC Genomics. 2008 Dec 08;9:591 PMID: 19063729
  153. Metastasis results from preexisting variant cells within a malignant tumor.
    Science. 1977 Aug 26;197(4306):893-5 PMID: 887927
  154. Cellular heterogeneity and molecular evolution in cancer.
    Annu Rev Pathol. 2013 Jan 24;8:277-302 PMID: 23092187
  155. Prognostic Value of EMT-Circulating Tumor Cells in Metastatic Breast Cancer Patients Undergoing High-Dose Chemotherapy with Autologous Hematopoietic Stem Cell Transplantation.
    J Cancer. 2012;3:369-80 PMID: 23074378
  156. Androgen receptor expression is significantly associated with better outcomes in estrogen receptor-positive breast cancers.
    Ann Oncol. 2011 Aug;22(8):1755-62 PMID: 21310761
  157. Molecular profiling of the residual disease of triple-negative breast cancers after neoadjuvant chemotherapy identifies actionable therapeutic targets.
    Cancer Discov. 2014 Feb;4(2):232-45 PMID: 24356096
Article Info
Journal
Frontiers in medicine
Abbr.
Front Med (Lausanne)
ISSN
2296-858X
Published
2017-00-00
Epub
2017-00-08
Pages
227
Language
English
Region
Switzerland
NLM ID
101648047
PMCID
PMC5727049
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com