Does DNA ploidy and synthesis phase dynamic accentuate the predictive power of oestrogen and progesterone receptors in breast cancer progression and prognosis?

Oestrogen and progesterone receptors (ER and PR) are closely associated with breast cancer progression. In this review we identify and discuss cellular markers that can accentuate or complement the deployment of ER and PR for predicting prognosis. The focus is on aneuploidy and DNA ploidy which appear to be significant independent predictors of overall survival in many forms of cancer. Their importance in cancer development and progression flows from their origin in the inherent genetic instability. Genetic instability of chromosomes is seen as aneuploidy, chromosomal deletions, translocations and sister-chromatid recombination, and at the DNA level as altered DNA repair, gene amplification and deletion and point mutations. Microsatellite loci of repetitive nucleotide sequences are inherently unstable. Microsatellite instability is characterised by the loss of DNA mismatch repair activity leading to a hypermutable phenotype. Chromosome abnormalities result from the deregulation of cell cycle and immune checkpoint regulators. Failure of the DNA mismatch repair pathway could be one of the reasons for their incidence, although the available evidence is not unequivocal. Some tumours such as the colorectal carcinomas do not show an indisputable relationship between aneuploidy and microsatellite instability or mismatch repair deficiency. Epithelial mesenchymal transition (EMT) plays a crucial role in cancer biology. EMT is associated with the emergence and maintenance of cancer stem cells (CSC). Polyploidy and aneuploidy appear as a staging post to the formation of CSCs together with parallel activation of EMT. Chromosomal alterations may occur concomitantly with EMT as well as with the reverse process of mesenchymal epithelial transformation. Genetic profiling has revealed significant information concerning the abnormal growth kinetics of cancer cells. The DNA ploidy pattern is reflected in the polyploid and aneuploid states, aberrant gene amplification and expression and enlarged S-phase fraction. Aneuploidy may be a consequence of cells entering the S-phase of the cell Oestrogen and progesterone receptors in breast cancer Atlas Genet Cytogenet Oncol Haematol. 2018; 22(9) 408 cycle prematurely. DNA ploidy is also associated with aberrant expression of growth factor and hormone receptors. The DNA indices and the synthesis phase fraction (SPF) have been studied extensively in relation to tumour progression. The question we pose here is whether they enhance or counteract the function of ER/PR. Could they serve as complementary factors to predict prognosis of breast cancer. The expression of these cellular markers is quantified here by image cytometry (ICM) and the accrued data have been analysed by using binomial regression algorithm and the fuzzy K-Nearest Neighbour (FK-NN) classifier to see whether these cellular markers aid the prediction of nodal status and survival of breast cancer patients. The FK-NN analyses have revealed high prediction rates for both nodal involvement and 5-year survival. The FK-NN appears much superior in performance than techniques of logistic regression and multilayer feed-forward backpropagation (MLFFBPNN) the artificial neural network tool. A wide spectrum of evidence is presented here which supports the view that DNA ploidy and SPF acting as complementary factors accentuate the predictive power of ER/PR of breast cancer progression and provides credibility that they could deliver a more reliable prognostic model to assist in patient management.

[1]  C. Osborne,et al.  Steroid hormone receptors in breast cancer management , 2004, Breast Cancer Research and Treatment.

[2]  J. Shine,et al.  Genetic instability and the development of steroid hormone insensitivity in cultured T 47D human breast cancer cells. , 1988, Cancer research.

[3]  Guo-Min Li,et al.  Mechanisms and functions of DNA mismatch repair , 2008, Cell Research.

[4]  A. Terzic,et al.  Increased expression of BubR1 protects against aneuploidy and cancer and extends healthy lifespan , 2012, Nature Cell Biology.

[5]  Muhammad G. Kibriya,et al.  A Genome-Wide Study of Cytogenetic Changes in Colorectal Cancer Using SNP Microarrays: Opportunities for Future Personalized Treatment , 2012, PloS one.

[6]  Huseyin Seker,et al.  Assessment of nodal involvement and survival analysis in breast cancer patients using image cytometric data: statistical, neural network and fuzzy approaches. , 2002, Anticancer research.

[7]  K. Kalland,et al.  Aneuploidy related transcriptional changes in endometrial cancer link low expression of chromosome 15q genes to poor survival , 2016, Oncotarget.

[8]  T. Pandita,et al.  Cell cycle checkpoint defects contribute to genomic instability in PTEN deficient cells independent of DNA DSB repair , 2009, Cell cycle.

[9]  斎藤 健一郎 Long interspersed nuclear element 1 hypomethylation is a marker of poor prognosis in stage IA non-small cell lung cancer , 2010 .

[10]  D P McDonnell,et al.  Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. , 1993, Molecular endocrinology.

[11]  J. Gustafsson,et al.  Progesterone receptor-estrogen receptor crosstalk: a novel insight , 2015, Trends in Endocrinology & Metabolism.

[12]  E. Tokunaga,et al.  Effect of EGFR and p-AKT Overexpression on Chromosomal Instability in Gastric Cancer , 2016, Annals of Surgical Oncology.

[13]  S. Elledge,et al.  Tumor aneuploidy correlates with markers of immune evasion and with reduced response to immunotherapy , 2017, Science.

[14]  R. Playford,et al.  The trefoil peptide TFF1 inhibits the growth of the human gastric adenocarcinoma cell line AGS , 1999, The Journal of pathology.

[15]  M. S. Lakshmi,et al.  Measurement of DNA content and nuclear pleomorphism in metastatic variants of the B16 murine melanoma and hamster lymphoma and its liver metastasis using image analysis techniques , 1990, Clinical & Experimental Metastasis.

[16]  D. Burke,et al.  Complexity in the spindle checkpoint. , 2000, Current opinion in genetics & development.

[17]  A. Nardulli,et al.  Sp1 binding sites and an estrogen response element half-site are involved in regulation of the human progesterone receptor A promoter. , 2000, Molecular endocrinology.

[18]  Michael Berger,et al.  Apoptosis - the p53 network , 2003, Journal of Cell Science.

[19]  P Giraud,et al.  Chapter 44 – Non–Small Cell Lung Cancer , 2016 .

[20]  S. Aebi,et al.  The role of DNA mismatch repair in drug resistance. , 1998, Clinical cancer research : an official journal of the American Association for Cancer Research.

[21]  G. Sherbet PGR (progesterone receptor) , 2018, Atlas of Genetics and Cytogenetics in Oncology and Haematology.

[22]  J. Pollard,et al.  Progesterone inhibits the estrogen-induced phosphoinositide 3-kinase-->AKT-->GSK-3beta-->cyclin D1-->pRB pathway to block uterine epithelial cell proliferation. , 2005, Molecular endocrinology.

[23]  A. Ghazalpour,et al.  Programmed Cell Death 1 (PD-1) and Its Ligand (PD-L1) in Common Cancers and Their Correlation with Molecular Cancer Type , 2014, Cancer Epidemiology, Biomarkers & Prevention.

[24]  Jeong-Won Lee,et al.  Ploidy and S-phase fraction are correlated with lymphovascular space invasion that is predictive of outcomes in endometrial cancer , 2012, International Journal of Clinical Oncology.

[25]  J. Thigpen Menopausal Hormone Therapy and Risk of Colorectal Cancer , 2009 .

[26]  R. Schiff,et al.  Endocrine responsiveness: understanding how progesterone receptor can be used to select endocrine therapy. , 2005, Breast.

[27]  S. Hanash,et al.  iTRAQ-Based Proteomic Analysis of Polyploid Giant Cancer Cells and Budding Progeny Cells Reveals Several Distinct Pathways for Ovarian Cancer Development , 2013, PloS one.

[28]  David Pellman,et al.  Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells , 2005, Nature.

[29]  R. Camplejohn,et al.  DNA index, S-phase fraction, histological grade and prognosis in breast cancer. , 1990, British Journal of Cancer.

[30]  R. Margolis,et al.  G1 tetraploidy checkpoint and the suppression of tumorigenesis , 2003, Journal of cellular biochemistry.

[31]  T. Sugai,et al.  Clinicopathological and molecular stability and methylation analyses of gastric papillary adenocarcinoma. , 2017, Pathology.

[32]  D. Cameron,et al.  Sensitivity to pertuzumab (2C4) in ovarian cancer models: cross-talk with estrogen receptor signaling , 2007, Molecular Cancer Therapeutics.

[33]  L. Diaz,et al.  Mismatch Repair Deficiency and Response to Immune Checkpoint Blockade. , 2016, The oncologist.

[34]  Raouf N. Gorgui-Naguib,et al.  DNA ploidy and cell cycle distribution of breast cancer aspirate cells measured by image cytometry and analyzed by artificial neural networks for their prognostic significance , 1999, IEEE Transactions on Information Technology in Biomedicine.

[35]  C. Perou,et al.  Prognostic significance of progesterone receptor-positive tumor cells within immunohistochemically defined luminal A breast cancer. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[36]  Nayoung Kim,et al.  ALU and LINE‐1 hypomethylations in multistep gastric carcinogenesis and their prognostic implications , 2012, International journal of cancer.

[37]  Wai Lok Woo,et al.  Cross Validation Evaluation for Breast Cancer Prediction Using Multilayer Perceptron Neural Networks , 2012 .

[38]  Francesca Rastelli,et al.  Factors Predictive of Response to Hormone Therapy in Breast Cancer , 2008 .

[39]  E. Scarpi,et al.  DNA ploidy and S-phase fraction analysis in peritoneal carcinomatosis from ovarian cancer: correlation with clinical pathological factors and response to chemotherapy , 2017, OncoTargets and therapy.

[40]  G. Taddei,et al.  Ten‐year results of a prospective study on the prognostic role of ploidy in endometrial carcinoma , 2007, Cancer.

[41]  Huseyin Seker,et al.  A soft measurement technique for searching significant subsets of prostate cancer prognostic markers , 2000 .

[42]  A. Gadducci,et al.  Immune Checkpoint Inhibitors in Gynecological Cancers: Update of Literature and Perspectives of Clinical Research. , 2017, Anticancer research.

[43]  D. Kell,et al.  Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses , 1996 .

[44]  Bert Vogelstein,et al.  Mutations of mitotic checkpoint genes in human cancers , 1998, Nature.

[45]  Steven M. Lipkin,et al.  Molecular models for the tissue specificity of DNA mismatch repair-deficient carcinogenesis , 2006, Nucleic acids research.

[46]  K. Hardwick,et al.  The spindle checkpoint , 2006, Journal of Cell Science.

[47]  Karl J. Dykema,et al.  Chromosome instability drives phenotypic switching to metastasis , 2016, Proceedings of the National Academy of Sciences.

[48]  A. Terzic,et al.  Early aging–associated phenotypes in Bub3/Rae1 haploinsufficient mice , 2006, The Journal of cell biology.

[49]  … and breast cancer , 1991 .

[50]  M. Frómeta,et al.  Flow Cytometric Measurement of Aneuploid DNA Content Correlates with High S-Phase Fraction and Poor Prognosis in Patients with Non-Small-Cell Lung Cancer , 2013 .

[51]  F. Craig,et al.  Flow cytometric immunophenotyping for hematologic neoplasms. , 2008, Blood.

[52]  L. Thim,et al.  The trefoil factor 1 participates in gastrointestinal cell differentiation by delaying G1-S phase transition and reducing apoptosis , 2002, The Journal of cell biology.

[53]  J. Xu,et al.  DNA aneuploidy and breast cancer: a meta-analysis of 141,163 cases , 2016, Oncotarget.

[54]  D. Felsher,et al.  MYC regulates the antitumor immune response through CD47 and PD-L1 , 2016, Science.

[55]  A. Giuliani,et al.  Somatic polyploidy is associated with the upregulation of c-MYC interacting genes and EMT-like signature , 2016, Oncotarget.

[56]  N. Cho,et al.  Alu and LINE-1 Hypomethylation Is Associated with HER2 Enriched Subtype of Breast Cancer , 2014, PloS one.

[57]  Robert LIN,et al.  NOTE ON FUZZY SETS , 2014 .

[58]  M. Wade,et al.  Adenocarcinoma of the endometrium. , 1967, American journal of obstetrics and gynecology.

[59]  S. Crispino,et al.  Factors predictive of response to hormone therapy in breast cancer. , 2008, Tumori.

[60]  James M. Keller,et al.  A fuzzy K-nearest neighbor algorithm , 1985, IEEE Transactions on Systems, Man, and Cybernetics.

[61]  Mark D. Aupperlee,et al.  Progesterone receptor isoform functions in normal breast development and breast cancer. , 2008, Critical reviews in eukaryotic gene expression.

[62]  Christopher D. McFarland,et al.  Oncogene-triggered suppression of DNA repair leads to DNA instability in cancer , 2014, Oncotarget.

[63]  N. Eberhardt,et al.  Opposing roles for p16Ink4a and p19Arf in senescence and ageing caused by BubR1 insufficiency , 2012, Nature Cell Biology.

[64]  C. Osborne,et al.  Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu , 1992, Breast Cancer Research and Treatment.

[65]  C. Sherr The ins and outs of RB: coupling gene expression to the cell cycle clock. , 1994, Trends in cell biology.

[66]  M. Kastan,et al.  Wild-type p 53 is a cell cycle checkpoint determinant following irradiation ( y irradiation / DNA damage / DNA replicatlon / carcinogenesis , 2022 .

[67]  Suet Yi Leung,et al.  Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1 , 2009, Nature Genetics.

[68]  D. Baker,et al.  Whole chromosome instability caused by Bub1 insufficiency drives tumorigenesis through tumor suppressor gene loss of heterozygosity. , 2009, Cancer cell.

[69]  P. Modrich,et al.  Mismatch repair in replication fidelity, genetic recombination, and cancer biology. , 1996, Annual review of biochemistry.

[70]  D. Kell,et al.  Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. , 1996, Microbiological reviews.

[71]  H. Brauch,et al.  Mechanisms of estrogen receptor antagonism toward p53 and its implications in breast cancer therapeutic response and stem cell regulation , 2010, Proceedings of the National Academy of Sciences.

[72]  R. Sarría,et al.  Cell proliferation, nuclear ploidy, and EGFr and HER2/neu tyrosine kinase oncoproteins in infiltrating ductal breast carcinoma. , 2002, Cancer genetics and cytogenetics.

[73]  M. Beato,et al.  Two Domains of the Progesterone Receptor Interact with the Estrogen Receptor and Are Required for Progesterone Activation of the c-Src/Erk Pathway in Mammalian Cells , 2003, Molecular and Cellular Biology.

[74]  T. Prolla,et al.  DNA mismatch repair and cancer. , 1998, Current opinion in cell biology.

[75]  Bin Wang,et al.  The T Box Transcription Factor TBX2 Promotes Epithelial-Mesenchymal Transition and Invasion of Normal and Malignant Breast Epithelial Cells , 2012, PloS one.

[76]  Satnam Dlay,et al.  Neural Analyses Validate and Emphasize the Role of Progesterone Receptor in Breast Cancer Progression and Prognosis. , 2016, Anticancer research.

[77]  B. Zhou,et al.  Stabilization of the transcription factors slug and twist by the deubiquitinase dub3 is a key requirement for tumor metastasis , 2017, Oncotarget.

[78]  V. Abeler,et al.  Prognostic importance of DNA ploidy and DNA index in stage I and II endometrioid adenocarcinoma of the endometrium , 2011, Annals of oncology : official journal of the European Society for Medical Oncology.

[79]  M. Park,et al.  The Role of Lymphovascular Invasion as a Prognostic Factor in Patients with Lymph Node-Positive Operable Invasive Breast Cancer , 2011, Journal of breast cancer.

[80]  S S Dlay,et al.  Oestrogen and progesterone receptor expression influences DNA ploidy and the proliferation potential of breast cancer cells. , 2003, Anticancer research.

[81]  S. André,et al.  DNA Ploidy is an Independent Predictor of Survival in Breast Invasive Ductal Carcinoma: A Long-term Multivariate Analysis of 393 Patients , 2013, Annals of Surgical Oncology.

[82]  H. Iwase,et al.  [Breast cancer]. , 2006, Nihon rinsho. Japanese journal of clinical medicine.

[83]  Wen-rong Gong,et al.  Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross‐talk with estrogen receptor , 1998, The EMBO journal.

[84]  Jeff S. Jasper,et al.  The metabolic regulator ERRα, a downstream target of HER2/IGF-1R, as a therapeutic target in breast cancer. , 2011, Cancer cell.

[85]  E. Cho,et al.  Relationship between p53‐associated proteins and estrogen receptor status in ovarian serous neoplasms , 2006, International journal of gynecological cancer : official journal of the International Gynecological Cancer Society.

[86]  Jianfeng Xu,et al.  Suppression of Tak1 promotes prostate tumorigenesis. , 2012, Cancer research.

[87]  Ji-yeon Lee,et al.  The mitotic checkpoint regulator RAE1 induces aggressive breast cancer cell phenotypes by mediating epithelial-mesenchymal transition , 2017, Scientific Reports.

[88]  J. Baselga,et al.  The role of hormonal therapy in the management of hormonal-receptor-positive breast cancer with co-expression of HER2 , 2008, Nature Clinical Practice Oncology.

[89]  G. Alexiou,et al.  DNA content is associated with malignancy of intracranial neoplasms , 2013, Clinical Neurology and Neurosurgery.

[90]  Predicting response to endocrine therapy in human breast cancer: a hypothesis. , 1976, Science.

[91]  A. Thompson,et al.  Multiparameter DNA content analysis identifies distinct groups in primary breast cancer , 2013, British Journal of Cancer.

[92]  A. Piastowska-Ciesielska,et al.  Oestrogens and oestrogen receptors in prostate cancer , 2016, SpringerPlus.

[93]  S. Prince,et al.  The T‐box transcription factor Tbx2: Its role in development and possible implication in cancer , 2009, IUBMB life.

[94]  T. Nishimura,et al.  The Role of DNA Methylation in Transposable Element Silencing and Genomic Imprinting , 2015 .

[95]  Caitlyn A. Miller,et al.  Extreme chromosome 17 copy number instability is a prognostic factor in patients with gastroesophageal adenocarcinoma: A retrospective cohort study , 2018, Genes, chromosomes & cancer.

[96]  K. Ohama,et al.  Are DNA Ploidy and Epidermal Growth Factor Receptor Prognostic Factors for Untreated Ovarian Cancer?: A Prospective Study , 2001, American journal of clinical oncology.

[97]  V. Brouste,et al.  D2-40 in breast cancer: should we detect more vascular emboli? , 2009, Modern Pathology.

[98]  R. Bast,et al.  Multivariable analysis of DNA ploidy, p53, and HER‐2/neu as prognostic factors in endometrial cancer , 1994, Cancer.

[99]  Z. Szentirmay,et al.  Deletions removing the last exon of TACSTD1 constitute a distinct class of mutations predisposing to Lynch syndrome , 2009, Human mutation.

[100]  S. Nass,et al.  The Loss of Estrogen and Progesterone Receptor Gene Expression in Human Breast Cancer , 2004, Journal of Mammary Gland Biology and Neoplasia.