Imperial College London

DR JAMES M. FLANAGAN

Faculty of MedicineDepartment of Surgery & Cancer

Reader in Epigenetics
 
 
 
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Contact

 

+44 (0)20 7594 2127j.flanagan

 
 
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Location

 

Institute of Reproductive and Developmental BiologyHammersmith Campus

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Summary

 

Publications

Publication Type
Year
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129 results found

Oltra SS, Pena-Chilet M, Flower K, Teresa Martinez M, Alonso E, Burgues O, Lluch A, Flanagan JM, Ribas Get al., 2019, Acceleration in the DNA methylation age in breast cancer tumours from very young women, SCIENTIFIC REPORTS, Vol: 9, ISSN: 2045-2322

Journal article

Li A, Geyer FC, Blecua P, Lee JY, Selenica P, Brown DN, Pareja F, Lee SSK, Kumar R, Rivera B, Bi R, Piscuoglio S, Wen HY, Lozada JR, Gularte-Merida R, Cavallone L, Rezoug Z, Nguyen-Dumont T, Peterlongo P, Tondini C, Terkelsen T, Ronlund K, Boonen SE, Mannerma A, Winqvist R, Janatova M, Rajadurai P, Xia B, Norton L, Robson ME, Ng P-S, Looi L-M, Southey MC, Weigelt B, Soo-Hwang T, Tischkowitz M, Foulkes WD, Reis-Filho JS, Aghmesheh M, Amor D, Andrews L, Antill Y, Balleine R, Beesley J, Blackburn A, Bogwitz M, Brown M, Burgess M, Burke J, Butow P, Caldon L, Campbell I, Christian A, Clarke C, Cohen P, Crook A, Cui J, Cummings M, Dawson S-J, De Fazio A, Delatycki M, Dobrovic A, Dudding T, Duijf P, Edkins E, Edwards S, Farshid G, Fellows A, Field M, Flanagan J, Fong P, Forbes J, Forrest L, Fox S, French J, Friedlander M, Ortega DG, Gattas M, Giles G, Gill G, Gleeson M, Greening S, Haan E, Harris M, Hayward N, Hickie I, Hopper J, Hunt C, James P, Jenkins M, Kefford R, Kentwell M, Kirk J, Kollias J, Lakhani S, Lindeman G, Lipton L, Lobb L, Lok S, Macrea F, Mane G, Marsh D, Mclachlan S-A, Meiser B, Milne R, Nightingale S, O'Connell S, Pachter N, Patterson B, Phillips K, Saleh M, Salisbury E, Saunders C, Saunus J, Scott C, Scott R, Sexton A, Shelling A, Simpson P, Spigelman A, Spurdle M, Stone J, Taylor J, Thorne H, Trainer A, Trench G, Tucker K, Visvader J, Walker L, Wallis M, Williams R, Winship I, Wu K, Young MAet al., 2019, Homologous recombination DNA repair defects in PALB2-associated breast cancers, npj Breast Cancer, Vol: 5, Pages: 1-14, ISSN: 2374-4677

Mono-allelic germline pathogenic variants in the Partner And Localizer of BRCA2 (PALB2) gene predispose to a high-risk of breast cancer development, consistent with the role of PALB2 in homologous recombination (HR) DNA repair. Here, we sought to define the repertoire of somatic genetic alterations in PALB2-associated breast cancers (BCs), and whether PALB2-associated BCs display bi-allelic inactivation of PALB2 and/or genomic features of HR-deficiency (HRD). Twenty-four breast cancer patients with pathogenic PALB2 germline mutations were analyzed by whole-exome sequencing (WES, n = 16) or targeted capture massively parallel sequencing (410 cancer genes, n = 8). Somatic genetic alterations, loss of heterozygosity (LOH) of the PALB2 wild-type allele, large-scale state transitions (LSTs) and mutational signatures were defined. PALB2-associated BCs were found to be heterogeneous at the genetic level, with PIK3CA (29%), PALB2 (21%), TP53 (21%), and NOTCH3 (17%) being the genes most frequently affected by somatic mutations. Bi-allelic PALB2 inactivation was found in 16 of the 24 cases (67%), either through LOH (n = 11) or second somatic mutations (n = 5) of the wild-type allele. High LST scores were found in all 12 PALB2-associated BCs with bi-allelic PALB2 inactivation sequenced by WES, of which eight displayed the HRD-related mutational signature 3. In addition, bi-allelic inactivation of PALB2 was significantly associated with high LST scores. Our findings suggest that the identification of bi-allelic PALB2 inactivation in PALB2-associated BCs is required for the personalization of HR-directed therapies, such as platinum salts and/or PARP inhibitors, as the vast majority of PALB2-associated BCs without PALB2 bi-allelic inactivation lack genomic features of HRD.

Journal article

Beetch M, Lubecka K, Shen K, Flower K, Harandi-Zadeh S, Suderman M, Flanagan JM, Stefanska Bet al., 2019, Stilbenoid-Mediated Epigenetic Activation of Semaphorin 3A in Breast Cancer Cells Involves Changes in Dynamic Interactions of DNA with DNMT3A and NF1C Transcription Factor., Mol Nutr Food Res, Pages: e1801386-e1801386

SCOPE: Loci-specific increase in DNA methylation occurs in cancer and may underlie gene silencing. It is investigated whether dietary stilbenoids, resveratrol, and pterostilbene exert time-dependent effects on DNA methylation patterns and specifically methylation-silenced tumor suppressor genes in breast cancer cells. METHODS AND RESULTS: Following genome-wide DNA methylation analysis with Illumina-450K, changes characteristic of early and late response to stilbenoids are identified. Interestingly, often the same genes but at different CpG loci, the same gene families, or the same functional gene categories are affected. CpG loci that lose methylation in exposed cells correspond to genes functionally associated with cancer suppression. There is a group of genes, including SEMA3A, at which the magnitude of hypomethylation in response to stilbenoids rises with increasing invasive potential of cancer cells. Decreased DNA methylation at SEMA3A promoter and concomitant gene upregulation coincide with increased occupancy of active histone marks. Open chromatin upon exposure to stilbenoids may be linked to decreased DNMT3A binding followed by increased NF1C transcription factor occupancy. Sequestration of DNMT3A is possibly a result of stilbenoid-mediated increase in SALL3 expression, which was previously shown to bind and inhibit DNMT3A activity. CONCLUSIONS: The findings define mechanistic players in stilbenoid-mediated epigenetic reactivation of genes suppressing cancer.

Journal article

Bodelon C, Ambatipudi S, Dugué P-A, Johansson A, Sampson JN, Hicks B, Karlins E, Hutchinson A, Cuenin C, Chajès V, Southey MC, Romieu I, Giles GG, English D, Polidoro S, Assumma M, Baglietto L, Vineis P, Severi G, Herceg Z, Flanagan JM, Milne RL, Garcia-Closas Met al., 2019, Blood DNA methylation and breast cancer risk: a meta-analysis of four prospective cohort studies, Breast Cancer Research, Vol: 21, ISSN: 1465-5411

BACKGROUND: Environmental and genetic factors play an important role in the etiology of breast cancer. Several small blood-based DNA methylation studies have reported risk associations with methylation at individual CpGs and average methylation levels; however, these findings require validation in larger prospective cohort studies. To investigate the role of blood DNA methylation on breast cancer risk, we conducted a meta-analysis of four prospective cohort studies, including a total of 1663 incident cases and 1885 controls, the largest study of blood DNA methylation and breast cancer risk to date. METHODS: We assessed associations with methylation at 365,145 CpGs present in the HumanMethylation450 (HM450K) Beadchip, after excluding CpGs that did not pass quality controls in all studies. Each of the four cohorts estimated odds ratios (ORs) and 95% confidence intervals (CI) for the association between each individual CpG and breast cancer risk. In addition, each study assessed the association between average methylation measures and breast cancer risk, adjusted and unadjusted for cell-type composition. Study-specific ORs were combined using fixed-effect meta-analysis with inverse variance weights. Stratified analyses were conducted by age at diagnosis (< 50, ≥ 50), estrogen receptor (ER) status (+/-), and time since blood collection (< 5, 5-10, > 10 years). The false discovery rate (q value) was used to account for multiple testing. RESULTS: The average age at blood draw ranged from 52.2 to 62.2 years across the four cohorts. Median follow-up time ranged from 6.6 to 8.4 years. The methylation measured at individual CpGs was not associated with breast cancer risk (q value > 0.59). In addition, higher average methylation level was not associated with risk of breast cancer (OR = 0.94, 95% CI = 0.85, 1.05; P = 0.26; P for study heterogeneity = 0.86

Journal article

Johansson A, Palli D, Masala G, Grioni S, Agnoli C, Tumino R, Giurdanella MC, Fasanelli F, Sacerdote C, Panico S, Mattiello A, Polidoro S, Jones ME, Schoemaker MJ, Orr N, Tomczyk K, Johnson N, Fletcher O, Perduca V, Baglietto L, Dugué P-A, Southey MC, Giles GG, English DR, Milne RL, Severi G, Ambatipudi S, Cuenin C, Chajès V, Romieu I, Herceg Z, Swerdlow AJ, Vineis P, Flanagan JMet al., 2019, Epigenome-wide association study for lifetime estrogen exposure identifies an epigenetic signature associated with breast cancer risk, Clinical Epigenetics, Vol: 11, ISSN: 1868-7083

BackgroundIt is well established that estrogens and other hormonal factors influence breast cancer susceptibility. We hypothesized that a woman’s total lifetime estrogen exposure accumulates changes in DNA methylation, detectable in the blood, which could be used in risk assessment for breast cancer.MethodsAn estimated lifetime estrogen exposure (ELEE) model was defined using epidemiological data from EPIC-Italy (n = 31,864). An epigenome-wide association study (EWAS) of ELEE was performed using existing Illumina HumanMethylation450K Beadchip (HM450K) methylation data obtained from EPIC-Italy blood DNA samples (n = 216). A methylation index (MI) of ELEE based on 31 CpG sites was developed using HM450K data from EPIC-Italy and the Generations Study and evaluated for association with breast cancer risk in an independent dataset from the Generations Study (n = 440 incident breast cancer cases matched to 440 healthy controls) using targeted bisulfite sequencing. Lastly, a meta-analysis was conducted including three additional cohorts, consisting of 1187 case-control pairs.ResultsWe observed an estimated 5% increase in breast cancer risk per 1-year longer ELEE (OR = 1.05, 95% CI 1.04–1.07, P = 3 × 10−12) in EPIC-Italy. The EWAS identified 694 CpG sites associated with ELEE (FDR Q < 0.05). We report a DNA methylation index (MI) associated with breast cancer risk that is validated in the Generations Study targeted bisulfite sequencing data (ORQ4_vs_Q1 = 1.77, 95% CI 1.07–2.93, P = 0.027) and in the meta-analysis (ORQ4_vs_Q1 = 1.43, 95% CI 1.05–2.00, P = 0.024); however, the correlation between the MI and ELEE was not validated across study cohorts.ConclusionWe have identified a blood DNA methylation signature associated with breast cancer risk in this study. Further investigation is required to confirm the inte

Journal article

Flanagan JM, Skrobanski H, Shi X, Hirst Yet al., 2019, Self-care behaviors of ovarian cancer patients before their diagnosis: Proof-of-concept study, JMIR CANCER, Vol: 5, ISSN: 2369-1999

Background: Longer patient intervals can lead to more late-stage cancer diagnoses and higher mortality rates. Individuals may delay presenting to primary care with red flag symptoms and instead turn to the internet to seek information, purchase over-the-counter medication, and change their diet or exercise habits. With advancements in machine learning, there is the potential to explore this complex relationship between a patient’s symptom appraisal and their first consultation at primary care through linkage of existing datasets (eg, health, commercial, and online).Objective: Here, we aimed to explore feasibility and acceptability of symptom appraisal using commercial- and health-data linkages for cancer symptom surveillance.Methods: A proof-of-concept study was developed to assess the general public’s acceptability of commercial- and health-data linkages for cancer symptom surveillance using a qualitative focus group study. We also investigated self-care behaviors of ovarian cancer patients using high-street retailer data, pre- and postdiagnosis.Results: Using a high-street retailer’s data, 1118 purchases—from April 2013 to July 2017—by 11 ovarian cancer patients and one healthy individual were analyzed. There was a unique presence of purchases for pain and indigestion medication prior to cancer diagnosis, which could signal disease in a larger sample. Qualitative findings suggest that the public are willing to consent to commercial- and health-data linkages as long as their data are safeguarded and users of this data are transparent about their purposes.Conclusions: Cancer symptom surveillance using commercial data is feasible and was found to be acceptable. To test efficacy of cancer surveillance using commercial data, larger studies are needed with links to individual electronic health records.

Journal article

Mavaddat N, Michailidou K, Dennis J, Lush M, Fachal L, Lee A, Tyrer JP, Chen T-H, Wang Q, Bolla MK, Yang X, Adank MA, Ahearn T, Aittomäki K, Allen J, Andrulis IL, Anton-Culver H, Antonenkova NN, Arndt V, Aronson KJ, Auer PL, Auvinen P, Barrdahl M, Beane Freeman LE, Beckmann MW, Behrens S, Benitez J, Bermisheva M, Bernstein L, Blomqvist C, Bogdanova NV, Bojesen SE, Bonanni B, Børresen-Dale A-L, Brauch H, Bremer M, Brenner H, Brentnall A, Brock IW, Brooks-Wilson A, Brucker SY, Brüning T, Burwinkel B, Campa D, Carter BD, Castelao JE, Chanock SJ, Chlebowski R, Christiansen H, Clarke CL, Collée JM, Cordina-Duverger E, Cornelissen S, Couch FJ, Cox A, Cross SS, Czene K, Daly MB, Devilee P, Dörk T, Dos-Santos-Silva I, Dumont M, Durcan L, Dwek M, Eccles DM, Ekici AB, Eliassen AH, Ellberg C, Engel C, Eriksson M, Evans DG, Fasching PA, Figueroa J, Fletcher O, Flyger H, Försti A, Fritschi L, Gabrielson M, Gago-Dominguez M, Gapstur SM, García-Sáenz JA, Gaudet MM, Georgoulias V, Giles GG, Gilyazova IR, Glendon G, Goldberg MS, Goldgar DE, González-Neira A, Grenaker Alnæs GI, Grip M, Gronwald J, Grundy A, Guénel P, Haeberle L, Hahnen E, Haiman CA, Håkansson N, Hamann U, Hankinson SE, Harkness EF, Hart SN, He W, Hein A, Heyworth J, Hillemanns P, Hollestelle A, Hooning MJ, Hoover RN, Hopper JL, Howell A, Huang G, Humphreys K, Hunter DJ, Jakimovska M, Jakubowska A, Janni W, John EM, Johnson N, Jones ME, Jukkola-Vuorinen A, Jung A, Kaaks R, Kaczmarek K, Kataja V, Keeman R, Kerin MJ, Khusnutdinova E, Kiiski JI, Knight JA, Ko Y-D, Kosma V-M, Koutros S, Kristensen VN, Krüger U, Kühl T, Lambrechts D, Le Marchand L, Lee E, Lejbkowicz F, Lilyquist J, Lindblom A, Lindström S, Lissowska J, Lo W-Y, Loibl S, Long J, Lubiński J, Lux MP, MacInnis RJ, Maishman T, Makalic E, Maleva Kostovska I, Mannermaa A, Manoukian S, Margolin S, Martens JWM, Martinez ME, Mavroudis D, McLean C, Meindl A, Menon U, Middha P, Miller N, Moreno F, Mulligan AM, Mulot C, Muñoz-Garzon VM, Neuhausen SL, Nevanlinna H, Nevenet al., 2019, Polygenic Risk Scores for Prediction of Breast Cancer and Breast Cancer Subtypes., American journal of human genetics, Vol: 104, Pages: 21-34, ISSN: 0002-9297

Stratification of women according to their risk of breast cancer based on polygenic risk scores (PRSs) could improve screening and prevention strategies. Our aim was to develop PRSs, optimized for prediction of estrogen receptor (ER)-specific disease, from the largest available genome-wide association dataset and to empirically validate the PRSs in prospective studies. The development dataset comprised 94,075 case subjects and 75,017 control subjects of European ancestry from 69 studies, divided into training and validation sets. Samples were genotyped using genome-wide arrays, and single-nucleotide polymorphisms (SNPs) were selected by stepwise regression or lasso penalized regression. The best performing PRSs were validated in an independent test set comprising 11,428 case subjects and 18,323 control subjects from 10 prospective studies and 190,040 women from UK Biobank (3,215 incident breast cancers). For the best PRSs (313 SNPs), the odds ratio for overall disease per 1 standard deviation in ten prospective studies was 1.61 (95%CI: 1.57-1.65) with area under receiver-operator curve (AUC) = 0.630 (95%CI: 0.628-0.651). The lifetime risk of overall breast cancer in the top centile of the PRSs was 32.6%. Compared with women in the middle quintile, those in the highest 1% of risk had 4.37- and 2.78-fold risks, and those in the lowest 1% of risk had 0.16- and 0.27-fold risks, of developing ER-positive and ER-negative disease, respectively. Goodness-of-fit tests indicated that this PRS was well calibrated and predicts disease risk accurately in the tails of the distribution. This PRS is a powerful and reliable predictor of breast cancer risk that may improve breast cancer prevention programs.

Journal article

Oltra SS, Pena-Chilet M, Vidal-Tomas V, Flower K, Teresa Martinez M, Alonso E, Burgues O, Lluch A, Flanagan JM, Ribas Get al., 2018, Methylation deregulation of miRNA promoters identifies miR124-2 as a survival biomarker in Breast Cancer in very young women, Scientific Reports, Vol: 8, ISSN: 2045-2322

MiRNAs are part of the epigenetic machinery, and are also epigenetically modified by DNA methylation. MiRNAs regulate expression of different genes, so any alteration in their methylation status may affect their expression. We aimed to identify methylation differences in miRNA encoding genes in breast cancer affecting women under 35 years old (BCVY), in order to identify potential biomarkers in these patients. In Illumina Infinium MethylationEPIC BeadChip samples (metEPICVal), we analysed the methylation of 9,961 CpG site regulators of miRNA-encoding genes present in the array. We identified 193 differentially methylated CpG sites in BCVY (p-value < 0.05 and methylation differences ±0.1) that regulated 83 unique miRNA encoding genes. We validated 10 CpG sites using two independent datasets based on Infinium Human Methylation 450k array. We tested gene expression of miRNAs with differential methylation in BCVY in a meta-analysis using The Cancer Genome Atlas (TCGA), Clariom D and Affymetrix datasets. Five miRNAs (miR-9, miR-124-2, miR-184, miR-551b and miR-196a-1) were differently expressed (FDR p-value < 0.01). Finally, only miR-124-2 shows a significantly different gene expression by quantitative real-time PCR. MiR-124-hypomethylation presents significantly better survival rates for older patients as opposed to the worse prognosis observed in BCVY, identifying it as a potential specific survival biomarker in BCVY.

Journal article

Lubecka K, Flower K, Beetch M, Qiu J, Kurzava L, Buvala H, Ruhayel A, Gawrieh S, Liangpunsakul S, Gonzalez T, McCabe G, Chalasani N, Flanagan JM, Stefanska Bet al., 2018, Loci-specific differences in blood DNA methylation in HBV-negative populations at risk for hepatocellular carcinoma development, Epigenetics, Vol: 13, Pages: 605-626, ISSN: 1559-2294

Late onset of clinical symptoms in hepatocellular carcinoma (HCC) results in late diagnosis and poor disease outcome. Approximately 85% of individuals with HCC have underlying liver cirrhosis. However, not all cirrhotic patients develop cancer. Reliable tools that would distinguish cirrhotic patients who will develop cancer from those who will not are urgently needed. We used the Illumina HumanMethylation450 BeadChip microarray to test whether white blood cell DNA, an easily accessible source of DNA, exhibits site-specific changes in DNA methylation in blood of diagnosed HCC patients (post-diagnostic, 24 cases, 24 controls) and in prospectively collected blood specimens of HCC patients who were cancer-free at blood collection (pre-diagnostic, 21 cases, 21 controls). Out of 22 differentially methylated loci selected for validation by pyrosequencing, 19 loci with neighbouring CpG sites (probes) were confirmed in the pre-diagnostic study group and subjected to verification in a prospective cirrhotic cohort (13 cases, 23 controls). We established for the first time 9 probes that could distinguish HBV-negative cirrhotic patients who subsequently developed HCC from those who stayed cancer-free. These probes were identified within regulatory regions of BARD1, MAGEB3, BRUNOL5, FXYD6, TET1, TSPAN5, DPPA5, KIAA1210, and LSP1. Methylation levels within DPPA5, KIAA1210, and LSP1 were higher in prospective samples from HCC cases versus cirrhotic controls. The remaining probes were hypomethylated in cases compared with controls. Using blood as a minimally invasive material and pyrosequencing as a straightforward quantitative method, the established probes have potential to be developed into a routine clinical test after validation in larger cohorts.

Journal article

Gallon J, Loomis E, Martin N, Flanagan J, Brown Ret al., 2018, The chromatin context and consequence of cisplatin-adduct DNA damage, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Bodelon C, Ambatipudi S, Dugue P-A, Johansson A, Sampson JN, Southey MC, Giles GG, Polidoro S, Herceg Z, Flanagan JM, Milne RL, Garcia-Closas Met al., 2018, Genome-wide blood DNA methylation and breast cancer risk: A meta-analysis of four prospective studies, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Tyndall C, Lam C, Gunter M, Flanagan Jet al., 2018, Metformin's potential as a breast cancer preventative agent by altering epigenetic patterns, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Johansson A, Palli D, Masala G, Grioni S, Agnoli C, Tumino R, Giurdanella MC, Fasanelli F, Sacerdote C, Panico S, Mattiello A, Swerdlow A, Schoemaker M, Jones M, Orr N, Fletcher O, Johnson N, Tomczyk K, Vineis P, Flanagan JMet al., 2018, DNA methylation index of lifetime estrogen exposure in breast cancer, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Galea F, White PA, Arlt VM, Vineis P, Flanagan JMet al., 2018, The epigenetic effects of benzo[<i>a</i>]pyrene exposure, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

tutt A, tovey H, Cheang MCU, Kernaghan S, Kilburn L, Gazinska P, Owen J, Abraham J, Barrett S, Barrett-Lee P, Brown R, Chan S, Dowsett M, Flanagan JM, Fox L, Grigoriadis A, Gutin A, Harper-Wynne C, Hatton MQ, Hoadley KA, Parikh J, Parker P, Perou CM, Roylance R, Shah V, Shaw A, Smith IE, Timms KM, Wardley AM, Wilson G, Gillett C, Lanchbury JS, Ashworth A, Rahman N, Harries M, Ellis P, Pinder SE, Bliss JMet al., 2018, Carboplatin in BRCA1/2-mutated and triple-negative breast cancer BRCAness subgroups: the TNT Trial, Nature Medicine, Vol: 24, Pages: 628-637, ISSN: 1078-8956

Germline mutations in BRCA1/2 predispose individuals to breast cancer (termed germline-mutated BRCA1/2 breast cancer, gBRCA-BC) by impairing homologous recombination (HR) and causing genomic instability. HR also repairs DNA lesions caused by platinum agents and PARP inhibitors. Triple-negative breast cancers (TNBCs) harbor subpopulations with BRCA1/2 mutations, hypothesized to be especially platinum-sensitive. Cancers in putative ‘BRCAness’ subgroups—tumors with BRCA1 methylation; low levels of BRCA1 mRNA (BRCA1 mRNA-low); or mutational signatures for HR deficiency and those with basal phenotypes—may also be sensitive to platinum. We assessed the efficacy of carboplatin and another mechanistically distinct therapy, docetaxel, in a phase 3 trial in subjects with unselected advanced TNBC. A prespecified protocol enabled biomarker–treatment interaction analyses in gBRCA-BC and BRCAness subgroups. The primary endpoint was objective response rate (ORR). In the unselected population (376 subjects; 188 carboplatin, 188 docetaxel), carboplatin was not more active than docetaxel (ORR, 31.4% versus 34.0%, respectively; P = 0.66). In contrast, in subjects with gBRCA-BC, carboplatin had double the ORR of docetaxel (68% versus 33%, respectively; biomarker, treatment interaction P = 0.01). Such benefit was not observed for subjects with BRCA1 methylation, BRCA1 mRNA-low tumors or a high score in a Myriad HRD assay. Significant interaction between treatment and the basal-like subtype was driven by high docetaxel response in the nonbasal subgroup. We conclude that patients with advanced TNBC benefit from characterization of BRCA1/2 mutations, but not BRCA1 methylation or Myriad HRD analyses, to inform choices on platinum-based chemotherapy. Additionally, gene expression analysis of basal-like cancers may also influence treatment selection.

Journal article

Perry MM, Lavender P, Scott Kuo C-H, Galea F, Michaeloudes C, Flanagan JM, Fan Chung K, Adcock IMet al., 2018, DNA methylation modules in airway smooth muscle are associated with asthma severity, European Respiratory Journal, Vol: 51, ISSN: 0903-1936

Abnormal DNA methylation patterns distinguish airway smooth muscle cell function in asthma and asthma severity.

Journal article

Johansson A, Flanagan JM, 2017, Epigenome-wide association studies for breast cancer risk and risk factors, Trends in cancer research, Vol: 12, Pages: 19-28, ISSN: 0973-1040

There have been six epigenome-wide association studies (EWAS) for breast cancer risk using blood DNA from prospective cohorts published thus far, and the only consistent finding is a global loss of methylation observed in breast cancer cases compared with controls, with no individual CpG sites passing validation across studies. In contrast, a more successful approach has been the identification of EWAS signatures of cancer risk factors such as smoking, body mass index, age and alcohol use with numerous validated CpG sites. These signatures may be used as a molecular test to quantify cancer risk associated with these factors. It is clear from the larger EWAS of risk exposures that similar-sized large collaborative studies may be needed to robustly identify DNA methylation signatures of breast cancer risk.

Journal article

Sanchis S, Chilet MP, Martinez M, Flower K, Alonso E, Burgues O, Lluch A, Flanagan J, Ribas Get al., 2017, Epigenomic landscape of breast cancer in very young women, 42nd Annual Meeting of the European-Society-of-Medical-Oncology (ESMO), Publisher: OXFORD UNIV PRESS, ISSN: 0923-7534

Conference paper

Beetch M, Lubecka K, Kurzava L, Flower K, Flanagan JM, Stefanska Bet al., 2017, Polyphenol-mediated epigenetic reactivation of tumor suppressor gene <i>SEMA3A</i> in breast cancer cells, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Lubecka K, Beetch M, Qiu J, Kurzava L, Flower K, Gawrieh S, Liangpunsakul S, Chalasani N, Flanagan JM, Stefanska Bet al., 2017, Loci-specific differences in blood DNA methylation for early detection of hepatocellular carcinoma, Annual Meeting of the American-Association-for-Cancer-Research (AACR), Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Ek WE, Tobi EW, Ahsan M, Lampa E, Ponzi E, Kyrtopoulos SA, Georgiadis P, Lumey LH, Heijmans BT, Botsivali M, Bergdahl IA, Karlsson T, Rask-Andersen M, Palli D, Ingelsson E, Hedman Å, Nilsson LM, Vineis P, Lind L, Flanagan JM, Johansson Å, Epigenome-Wide Association study Consortiumet al., 2017, Tea and coffee consumption in relation to DNA methylation in four European cohorts., Human Molecular Genetics, Vol: 26, Pages: 3221-3231, ISSN: 0964-6906

Lifestyle factors, such as food choices and exposure to chemicals, can alter DNA methylation and lead to changes in gene activity. Two such exposures with pharmacologically active components are coffee and tea consumption. Both coffee and tea has been suggested to play an important role in modulating disease-risk in humans by suppressing tumour progression, decreasing inflammation and influencing estrogen metabolism. These mechanisms may be mediated by changes in DNA methylation.To investigate if DNA methylation in blood is associated with coffee and tea consumption we performed a genome-wide DNA methylation study for coffee and tea consumption in four European cohorts (N = 3,096). DNA methylation was measured from whole blood at 421,695 CpG sites distributed throughout the genome and analysed in men and women both separately and together in each cohort. Meta-analyses of the results and additional regional-level analyses were performed.After adjusting for multiple testing, the meta-analysis revealed that two individual CpG-sites, mapping to DNAJC16 and TTC17, were differentially methylated in relation to tea consumption in women. No individual sites were associated in men or in the sex-combined analysis for tea or coffee. The regional analysis revealed that 28 regions were differentially methylated in relation to tea consumption in women. These regions contained genes known to interact with estradiol metabolism and cancer. No significant regions were found in the sex-combined and male-only analysis for either tea or coffee consumption.

Journal article

Flanagan JM, Wilson A, Koo C, Masrour N, Gallon J, Loomis E, Flower K, Wilhelm-Benartzi C, Hergovich A, Cunnea P, Gabra H, Braicu EI, Sehouli J, Darb-Esfahani S, Vanderstichele A, Vergote I, Kreuzinger C, Cacsire Castillo-Tong D, Wisman GB, Berns EM, Siddiqui N, Paul J, Brown Ret al., 2017, Platinum-based chemotherapy induces methylation changes in blood DNA associated with overall survival in ovarian cancer patients, Clinical Cancer Research, Vol: 23, Pages: 2213-2222, ISSN: 1557-3265

PURPOSE: DNA damage repair can lead to epigenetic changes. DNA mismatch repair proteins bind to platinum DNA adducts and at sites of DNA damage can recruit the DNA methylating enzyme DNMT1, resulting in aberrant methylation. We hypothesised that DNA damage repair during platinum-based chemotherapy may cause aberrant DNA methylation in normal tissues of patients such as blood. EXPERIMENTAL DESIGN: We used Illumina 450k methylation arrays and bisulphite pyrosequencing to investigate methylation at presentation and relapse in blood DNA from ovarian cancer patients enrolled in the SCOTROC1 trial (n=247) and in a cohort of ovarian tumour DNA samples collected at first relapse (n=46). We used an ovarian cancer cell line model to investigate the role of the DNA mismatch repair gene MLH1 in platinum induced methylation changes. RESULTS: Specific CpG methylation changes in blood at relapse are observed following platinum-based chemotherapy and are associated with patient survival, independent of other clinical factors (HR=3.7; 95%CI 1.8-7.6, p=2.8x10-4). Similar changes occur in ovarian tumours at relapse, also associate with patient survival (HR=2.6; 95%CI 1.0-6.8, p=0.048). Using an ovarian cancer cell line model, we demonstrate that functional mismatch repair (MMR) increases the frequency of platinum-induced methylation. CONCLUSION: DNA methylation in blood at relapse following chemotherapy, and not at presentation, is informative about ovarian cancer patient survival. Functional DNA mismatch repair increases the frequency of DNA methylation changes induced by platinum. DNA methylation in blood following chemotherapy could provide a non-invasive means of monitoring patients' epigenetic responses to treatment without requiring a tumour biopsy.

Journal article

Stefanska B, Kurzava L, Lubecka K, Beetch M, Flower K, Flanagan JMet al., 2017, Epigenetic Regulation of WNT and Hedgehog Oncogenic Signaling in Breast Cancer Cells in Response to Dietary Polyphenols, Experimental Biology (EB) Annual Meeting, Publisher: WILEY, ISSN: 0892-6638

Conference paper

Phelan CM, Kuchenbaecker KB, Tyrer JP, Kar SP, Lawrenson K, Winham SJ, Dennis J, Pirie A, Riggan MJ, Chornokur G, Earp MA, Lyra PC, Lee JM, Coetzee S, Beesley J, McGuffog L, Soucy P, Dicks E, Lee A, Barrowdale D, Lecarpentier J, Leslie G, Aalfs CM, Aben KKH, Adams M, Adlard J, Andrulis IL, Anton-Culver H, Antonenkova N, Aravantinos G, Arnold N, Arun BK, Arver B, Azzollini J, Balmana J, Banerjee SN, Barjhoux L, Barkardottir RB, Bean Y, Beckmann MW, Beeghly-Fadiel A, Benitez J, Bermisheva M, Bernardini MQ, Birrer MJ, Bjorge L, Black A, Blankstein K, Blok MJ, Bodelon C, Bogdanova N, Bojesen A, Bonanni B, Borg A, Bradbury AR, Brenton JD, Brewer C, Brinton L, Broberg P, Brooks-Wilson A, Bruinsma F, Brunet J, Buecher B, Butzow R, Buys SS, Caldes T, Caligo MA, Campbell I, Cannioto R, Carney ME, Cescon T, Chan SB, Chang-Claude J, Chanock S, Chen XQ, Chiew Y-E, Chiquette J, Chung WK, Claes KBM, Conner T, Cook LS, Cook J, Cramer DW, Cunningham JM, D'Aloisio AA, Daly MB, Damiola F, Damirovna SD, Dansonka-Mieszkowska A, Dao F, Davidson R, DeFazio A, Delnatte C, Doheny KF, Diez O, Ding YC, Doherty JA, Domchek SM, Dorfling CM, Dork T, Dossus L, Duran M, Durst M, Dworniczak B, Eccles D, Edwards T, Eeles R, Eilber U, Ejlertsen B, Ekici AB, Ellis S, Elvira M, Eng KH, Engel C, Evans DG, Fasching PA, Ferguson S, Ferrer SF, Flanagan JM, Fogarty ZC, Fortner RT, Fostira F, Foulkes WD, Fountzilas G, Fridley BL, Friebel TM, Friedman E, Frost D, Ganz PA, Garber J, Garcia MJ, Garcia-Barberan V, Gehrig A, Gentry-Maharaj A, Gerdes A-M, Giles GG, Glasspool R, Glendon G, Godwin AK, Goldgar DE, Goranova T, Gore M, Greene MH, Gronwald J, Gruber S, Hahnen E, Haiman CA, Hakansson N, Hamann U, Hansen TVO, Harrington PA, Harris HR, Hauke J, Hein A, Henderson A, Hildebrandt MAT, Hillemanns P, Hodgson S, Hogdall CK, Hogdall E, Hogervorst FBL, Holland H, Hooning MJ, Hosking K, Huang R-Y, Hulick PJ, Hung J, Hunter DJ, Huntsman DG, Huzarski T, Imyanitov EN, Isaacs C, Iversen ES, Izatt L, Izquierdo A, Jakubet al., 2017, Identification of 12 new susceptibility loci for different histotypes of epithelial ovarian cancer, NATURE GENETICS, Vol: 49, Pages: 680-691, ISSN: 1061-4036

To identify common alleles associated with different histotypes of epithelial ovarian cancer (EOC), we pooled data from multiple genome-wide genotyping projects totaling 25,509 EOC cases and 40,941 controls. We identified nine new susceptibility loci for different EOC histotypes: six for serous EOC histotypes (3q28, 4q32.3, 8q21.11, 10q24.33, 18q11.2 and 22q12.1), two for mucinous EOC (3q22.3 and 9q31.1) and one for endometrioid EOC (5q12.3). We then performed meta-analysis on the results for high-grade serous ovarian cancer with the results from analysis of 31,448 BRCA1 and BRCA2 mutation carriers, including 3,887 mutation carriers with EOC. This identified three additional susceptibility loci at 2q13, 8q24.1 and 12q24.31. Integrated analyses of genes and regulatory biofeatures at each locus predicted candidate susceptibility genes, including OBFC1, a new candidate susceptibility gene for low-grade and borderline serous EOC.

Journal article

Vineis P, Chatziioannou A, Cunliffe VT, Flanagan JM, Hanson M, Kirsch-Volders M, Kyrtopoulos Set al., 2017, Epigenetic memory in response to environmental stressors, FASEB JOURNAL, Vol: 31, Pages: 2241-2251, ISSN: 0892-6638

Journal article

Flanagan JM, 2017, Epigenome-Wide Association Studies (EWAS) for breast cancer risk, Internal Medicine Review, ISSN: 2470-3524

Current breast cancer screening methods are effective, however, they could be improved by targeting those at highest risk and the idea of developing a risk stratified screening strategy is gaining support. Multiple lifestyle and environmental factors influence breast cancer aetiology, including age, hormonal and reproductive factors, body mass index, physical activity, alcohol intake, smoking, benign breast disease, high mammographic-density and family history. The addition of the combined “polygenic risk scores” integrating genetic risk markers is likely to make a modest improvement to breast cancer risk models, however, there is considerable room for improvement by identifying further independent risk factors. In this review we consider the evidence for epigenetic risk markers for breast cancer. There have been five EWAS for breast cancer risk using blood DNA from prospective cohorts published thus far, and the only consistent finding is a loss of methylation observed in breast cancer cases compared with controls, with no individual CpG sites validating across studies. In contrast, a more successful approach has been the identification of EWAS signatures of cancer risk factors such as smoking, body mass index, age and alcohol use with numerous validated CpG sites. These signatures may be used as a molecular test to quantify cancer risk associated with these factors. In summary, it is clear from the larger exposure related studies that similar sized large collaborative studies may be needed to robustly identify DNA methylation signatures of breast cancer risk.

Journal article

Flanagan JM, Curry E, Stirling L, Flower K, Orr N, Tomczyk K, Coulson P, Jones M, Ashworth A, Swerdlow A, Brown R, Garcia-Closas Met al., 2017, Epigenome-wide association study for breast cancer risk using whole genome and target captured bisulphite sequencing: A pooled case-control study nested in the breakthrough generations study, San Antonio Breast Cancer Symposium, Publisher: AMER ASSOC CANCER RESEARCH, ISSN: 0008-5472

Conference paper

Kar SP, Adler E, Tyrer J, Hazelett D, Anton-Culver H, Bandera EV, Beckmann MW, Berchuck A, Bogdanova N, Brinton L, Butzow R, Campbell I, Carty K, Chang-Claude J, Cook LS, Cramer DW, Cunningham JM, Dansonka-Mieszkowska A, Doherty JA, Doerk T, Duerst M, Eccles D, Fasching PA, Flanagan J, Gentry-Maharaj A, Glasspool R, Goode EL, Goodman MT, Gronwald J, Heitz F, Hildebrandt MAT, Hogdall E, Hogdall CK, Huntsman DG, Jensen A, Karlan BY, Kelemen LE, Kiemeney LA, Kjaer SK, Kupryjanczyk J, Lambrechts D, Levine DA, Li Q, Lissowska J, Lu KH, Lubinski J, Massuger LFAG, McGuire V, McNeish I, Menon U, Modugno F, Monteiro AN, Moysich KB, Ness RB, Nevanlinna H, Paul J, Pearce CL, Pejovic T, Permuth JB, Phelan C, Pike MC, Poole EM, Ramus SJ, Risch HA, Rossing MA, Salvesen HB, Schildkraut JM, Sellers TA, Sherman M, Siddiqui N, Sieh W, Song H, Southey M, Terry KL, Tworoger SS, Walsh C, Wentzensen N, Whittemore AS, Wu AH, Yang H, Zheng W, Ziogas A, Freedman ML, Gayther SA, Pharoah PDP, Lawrenson Ket al., 2017, Enrichment of putative PAX8 target genes at serous epithelial ovarian cancer susceptibility loci, BRITISH JOURNAL OF CANCER, Vol: 116, Pages: 524-535, ISSN: 0007-0920

Background: Genome-wide association studies (GWAS) have identified 18 loci associated with serous ovarian cancer (SOC) susceptibility but the biological mechanisms driving these findings remain poorly characterised. Germline cancer risk loci may be enriched for target genes of transcription factors (TFs) critical to somatic tumorigenesis.Methods: All 615 TF-target sets from the Molecular Signatures Database were evaluated using gene set enrichment analysis (GSEA) and three GWAS for SOC risk: discovery (2196 cases/4396 controls), replication (7035 cases/21 693 controls; independent from discovery), and combined (9627 cases/30 845 controls; including additional individuals).Results: The PAX8-target gene set was ranked 1/615 in the discovery (PGSEA<0.001; FDR=0.21), 7/615 in the replication (PGSEA=0.004; FDR=0.37), and 1/615 in the combined (PGSEA<0.001; FDR=0.21) studies. Adding other genes reported to interact with PAX8 in the literature to the PAX8-target set and applying an alternative to GSEA, interval enrichment, further confirmed this association (P=0.006). Fifteen of the 157 genes from this expanded PAX8 pathway were near eight loci associated with SOC risk at P<10−5 (including six with P<5 × 10−8). The pathway was also associated with differential gene expression after shRNA-mediated silencing of PAX8 in HeyA8 (PGSEA=0.025) and IGROV1 (PGSEA=0.004) SOC cells and several PAX8 targets near SOC risk loci demonstrated in vitro transcriptomic perturbation.Conclusions: Putative PAX8 target genes are enriched for common SOC risk variants. This finding from our agnostic evaluation is of particular interest given that PAX8 is well-established as a specific marker for the cell of origin of SOC.

Journal article

Johansson A, Vineis P, Flanagan JM, 2016, Evaluating the Estimated Lifetime Oestrogen Exposure (ELEE) model as a risk factor for breast cancer, UK Breast Cancer Research Symposium, Publisher: SPRINGER, Pages: 183-183, ISSN: 0167-6806

Conference paper

Tyndall C, Gunter M, Flanagan JM, 2016, Metformin: a new role in breast cancer prevention?, UK Breast Cancer Research Symposium, Publisher: SPRINGER, Pages: 182-182, ISSN: 0167-6806

Conference paper

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