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Institute of Applied Data Science

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Professor Trevor Graham

Trevor Graham

Professor of Cancer Evolution & Turing Fellow

Department Faculty of Medicine and Dentistry
 Barts Cancer Institute (BCI), Charterhouse Square, London, EC1M 6BQ
020 7882 6231

www.bci.qmul.ac.uk/en/staff/item/trevor-graham

Research

Characterising intra-tumour heterogeneity, Measuring the rate of evolution in premalignant lesions, Understanding how the clonal structure of tissue

Interests

Prof Conrad Bessant and Prof Trevor Graham are Principal Investigators on a project funded by the Alan Turing Institute: 'Automatic Learning In Cancer Research Using Artificial Intelligence'. The aim of the project is to create and apply an automatic research methodology to rationally design mechanistic mathematical models of cancer evolution, and then evaluate the models against primary ‘Big Data’ from public and our own repositories.  It is hoped that success in this project will have two major long-term impacts:

(1) to establish the value of artificial intelligence approaches in basic biology,

(2) to make further inroads into understanding the large and complex datasets available in cancer research.

Trevor has worked in Nick Wright's lab at the Cancer Research UK London Research Institute studying clonal expansions in human tissues (2008-2011), and Carlo Maley’s lab at UCSF looking at the pattern of clonal evolution in human cancers (2011-2013) and joined BCI in 2013. The central themes of his work include characterising intra-tumour heterogeneity and using it to predict prognosis; measuring the rate of evolution in premalignant lesions and using these measures to determine cancer risk; and understanding how the clonal structure of tissues (particularly in the GI tract) shape patterns of somatic evolution. The major tools employed in the lab are a combination of mathematical modelling, statistical inference and detailed genetic analysis.

Publications

Publications of specific relevance to Applied Data Science

2020

Werner B, Case J, Williams MJ, Chkhaidze K, Temko D, Fernández-Mateos J, Cresswell GD, Nichol D, Cross W, Spiteri I, Huang W, Tomlinson IPM, Barnes CP, Graham TA and Sottoriva A (2020). Measuring single cell divisions in human tissues from multi-region sequencing data. Nature Communications  vol. 11, (1) 10.1038/s41467-020-14844-6
Temko D, Tomlinson IPM, Severini S, Schuster-Böckler B and Graham TA (2020). Author Correction: The effects of mutational processes and selection on driver mutations across cancer types (Nature Communications, (2018), 9, 1, (1857), 10.1038/s41467-018-04208-6). Nature Communications  vol. 11, (1) 10.1038/s41467-020-15800-0
Lakatos E, Williams MJ, Schenck RO, Cross WCH, Househam J, Zapata L, Werner B, Gatenbee C, Robertson-Tessi M, Barnes CP, Anderson ARA, Sottoriva A and Graham TA (2020). Evolutionary dynamics of neoantigens in growing tumors. Nature Genetics  vol. 52, (10) 1057-1066. 10.1038/s41588-020-0687-1
Graham T, Caravagna G, Heide T, Williams M, Zapata L, Daniel N, Ketevan C, Cross W, Creswell G, Werner B, Acar A, Chesler L, Barnes C, Sanguinetti G and Sottoriva A (2020). Subclonal reconstruction of tumors using machine learning and population genetics. Nature Research  Nature Genetics  vol. 52, 898-907. 10.1038/s41588-020-0675-5
Lupo B, Sassi F, Pinnelli M, Galimi F, Zanella ER, Vurchio V, Migliardi G, Gagliardi PA, Puliafito A, Manganaro D, Luraghi P, Kragh M, Pedersen MW, Horak ID, Boccaccio C, Medico E, Primo L, Nichol D, Spiteri I, Heide T, Vatsiou A, Graham TA, Élez E, Argiles G, Nuciforo P, Sottoriva A, Dienstmann R, Pasini D, Grassi E and Isella C (2020). Colorectal cancer residual disease at maximal response to EGFR blockade displays a druggable Paneth cell–like phenotype. Science Translational Medicine  vol. 12, (555) 10.1126/SCITRANSLMED.AAX8313
Graham TA and Shibata D (2020). Navigating the path to distant metastasis. Nature Genetics  vol. 52, (7) 642-643. 10.1038/s41588-020-0660-z
Araf S, Korfi K, Bewicke-Copley F, Wang J, Cogliatti S, Kumar E, Forrer F, Barrington SF, Graham TA, Scott DW, Rimsza LM, Davies A, Johnson P, Okosun J, Fitzgibbon J and Fehr M (2020). Genetic heterogeneity highlighted by differential FDG-PET response in diffuse large B-cell lymphoma. Haematologica  vol. 105, (6) E318-E321. 10.3324/haematol.2019.242206
Demircioglu F, Wang J, Candido J, Costa ASH, Casado P, de Luxan Delgado B, Reynolds LE, Gomez-Escudero J, Newport E, Rajeeve V, Baker A-M, Roy-Luzarraga M, Graham TA, Foster J, Wang Y, Campbell JJ, Singh R, Zhang P, Schall TJ, Balkwill FR, Sosabowski J, Cutillas PR, Frezza C, Sancho P and Hodivala-Dilke K (2020). Cancer associated fibroblast FAK regulates malignant cell metabolism. Nature Research (Part of Springer Nature)  Nature Communications  vol. 11, (1) 1290-1290. 10.1038/s41467-020-15104-3
Williams MJ, Zapata L, Werner B, Barnes CP, Sottoriva A and Graham TA (2020). Measuring the distribution of fitness effects in somatic evolution by combining clonal dynamics with dN/dS ratios. Elife  vol. 9, 10.7554/eLife.48714
Turajlic S, Sottoriva A, Graham T and Swanton C (2020). Author Correction: Resolving genetic heterogeneity in cancer (Nature Reviews Genetics, (2019), 20, 7, (404-416), 10.1038/s41576-019-0114-6). Nature Reviews Genetics  vol. 21, (1) 10.1038/s41576-019-0188-1
Baker AM and Graham TA (2020). Concurrent in situ analysis of point mutations and immune infiltrate in FFPE cancers. Methods in Enzymology  10.1016/bs.mie.2019.05.009
Baker AM and Graham TA (2020). In Situ Point Mutation Detection in FFPE Colorectal Cancers Using the BaseScope Assay. 10.1007/978-1-0716-0623-0_22

2019

Saunderson EA, Baker A-M, Williams M, Curtius K, Jones JL, Graham TA and Ficz G (2019). A novel use of random priming-based single-strand library preparation for whole genome sequencing of formalin-fixed paraffin-embedded tissue samples. Oxford University Press  Nar Genomics and Bioinformatics  vol. 2, (1) lqz017-lqz017. 10.1093/nargab/lqz017
Chkhaidze K, Heide T, Werner B, Williams MJ, Huang W, Caravagna G, Graham TA and Sottoriva A (2019). Spatially constrained tumour growth affects the patterns of clonal selection and neutral drift in cancer genomic data. Plos Computational Biology  vol. 15, (7) 10.1371/journal.pcbi.1007243
Baker AM, Cross W, Curtius K, Al Bakir I, Choi CHR, Davis HL, Temko D, Biswas S, Martinez P, Williams MJ, Lindsay JO, Feakins R, Vega R, Hayes SJ, Tomlinson IPM, McDonald SAC, Moorghen M, Silver A, East JE, Wright NA, Wang LM, Rodriguez-Justo M, Jansen M, Hart AL, Leedham SJ and Graham TA (2019). Evolutionary history of human colitis-associated colorectal cancer. Gut  vol. 68, (6) 985-995. 10.1136/gutjnl-2018-316191
Araf S, Wang J, Korfi K, Pangault C, Kotsiou E, Rio-Machin A, Rahim T, Heward J, Clear A, Iqbal S, Davies JK, Johnson P, Calaminici M, Montoto S, Auer R, Chelala C, Gribben JG, Graham TA, Fest T, Fitzgibbon J and Okosun J (2019). Correction: Genomic profiling reveals spatial intra-tumor heterogeneity in follicular lymphoma (Leukemia, (2018), 32, 5, (1261-1265), 10.1038/s41375-018-0043-y). Leukemia  vol. 33, (6) 10.1038/s41375-019-0425-9
Schenck RO, Lakatos E, Gatenbee C, Graham TA and Anderson ARA (2019). NeoPredPipe: High-throughput neoantigen prediction and recognition potential pipeline. Bmc Bioinformatics  vol. 20, (1) 10.1186/s12859-019-2876-4
Baker A-M, Cereser B, Melton S, Fletcher AG, Rodriguez-Justo M, Tadrous PJ, Humphries A, Elia G, McDonald SAC, Wright NA, Simons BD, Jansen M and Graham TA (2019). Quantification of Crypt and Stem Cell Evolution in the Normal and Neoplastic Human Colon. Cell Rep  vol. 27, (8) 2524-2524. 10.1016/j.celrep.2019.05.035
Williams MJ, Sottoriva A and Graham TA (2019). Measuring Clonal Evolution in Cancer with Genomics. Annual Reviews  Annual Review of Genomics and Human Genetics  10.1146/annurev-genom-083117-021712
Araf S, Wang J, Ashton-Key M, Korfi K, Di Bella D, Rio-Machin A, Odabashian M, Foria V, Du M-Q, Cucco F, Barrans S, Johnson P, Laird SR, Fisher AM, Cullis JO, Graham TA, Okosun J, Fitzgibbon J and Chiecchio L (2019). Transmission of diffuse large B-cell lymphoma by an allogeneic stem-cell transplant. Haematologica  vol. 104, (4) e174-e177. 10.3324/haematol.2018.196907
Turajlic S, Sottoriva A, Graham T and Swanton C (2019). Resolving genetic heterogeneity in cancer. Nature Research (Part of Springer Nature)  Nature Reviews Genetics  vol. 20, (7) 404-416. 10.1038/s41576-019-0114-6
Heide T, Maurer A, Eipel M, Knoll K, Geelvink M, Veeck J, Knuechel R, van Essen J, Stoehr R, Hartmann A, Altmueller J, Graham TA and Gaisa NT (2019). Multiregion human bladder cancer sequencing reveals tumour evolution, bladder cancer phenotypes and implications for targeted therapy. Wiley  Journal of Pathology  vol. 248, (2) 230-242. 10.1002/path.5250
Choi CHR, Al Bakir I, Ding NSJ, Lee GH, Askari A, Warusavitarne J, Moorghen M, Humphries A, Ignjatovic-Wilson A, Thomas-Gibson S, Saunders BP, Rutter MD, Graham TA and Hart AL (2019). Cumulative burden of inflammation predicts colorectal neoplasia risk in ulcerative colitis: A large single-centre study. Gut  vol. 68, (3) 414-422. 10.1136/gutjnl-2017-314190
Baker AM, Gabbutt C, Williams MJ, Cereser B, Jawad N, Rodriguez-Justo M, Jansen M, Barnes CP, Simons BD, McDonald SAC, Graham TA and Wright NA (2019). Crypt fusion as a homeostatic mechanism in the human colon. Gut  vol. 68, (11) 1986-1993. 10.1136/gutjnl-2018-317540

2018

Martinez P, Mallo D, Paulson TG, Li X, Sanchez CA, Reid BJ, Graham TA, Kuhner MK and Maley CC (2018). Evolution of Barrett's esophagus through space and time at single-crypt and whole-biopsy levels. Nature Communications  vol. 9, (1) 10.1038/s41467-017-02621-x
Williams MJ, Werner B, Heide T, Barnes CP, Graham TA and Sottoriva A (2018). Reply to ‘Revisiting signatures of neutral tumor evolution in the light of complexity of cancer genomic data’. Nature Genetics  vol. 50, (12) 1628-1630. 10.1038/s41588-018-0210-0
Heide T, Zapata L, Williams MJ, Werner B, Caravagna G, Barnes CP, Graham TA and Sottoriva A (2018). Reply to ‘Neutral tumor evolution?’. Nature Genetics  vol. 50, (12) 1633-1637. 10.1038/s41588-018-0256-z
Werner B, Williams MJ, Barnes CP, Graham TA and Sottoriva A (2018). Reply to ‘Currently available bulk sequencing data do not necessarily support a model of neutral tumor evolution’. Nature Genetics  vol. 50, (12) 1624-1626. 10.1038/s41588-018-0235-4
Al Bakir I, Curtius K and Graham TA (2018). From Colitis to Cancer: An Evolutionary Trajectory That Merges Maths and Biology. Frontiers Media  Frontiers in Immunology  vol. 9, 2368-2368. 10.3389/fimmu.2018.02368
Williams MJ, Werner B, Heide T, Curtis C, Barnes CP, Sottoriva A and Graham TA (2018). Erratum to: Quantification of subclonal selection in cancer from bulk sequencing data (Nature Genetics, (2018), 50, 6, (895-903), 10.1038/s41588-018-0128-6). Nature Genetics  vol. 50, (9) 10.1038/s41588-018-0169-x
Caravagna G, Giarratano Y, Ramazzotti D, Tomlinson I, Graham TA, Sanguinetti G and Sottoriva A (2018). Detecting repeated cancer evolution from multi-region tumor sequencing data. Nature Methods  vol. 15, (9) 707-714. 10.1038/s41592-018-0108-x
Caravagna G, Giarratano Y, Ramazzotti D, Graham TA, Sanguinetti G and Sottoriva A (2018). Detecting repeated cancer evolution in human tumours from multi-region sequencing data. Nature Research  Nature Methods  vol. 15, 707-714. 10.1101/156729
Cross W, Kovac M, Mustonen V, Temko D, Davis H, Baker A-M, Biswas S, Arnold R, Chegwidden L, Gatenbee C, Anderson AR, Koelzer VH, Martinez P, Jiang X, Domingo E, Woodcock DJ, Feng Y, Kovacova M, Maughan T, S:CORT Consortium , Jansen M, Rodriguez-Justo M, Ashraf S, Guy R, Cunningham C, East JE, Wedge DC, Wang LM, Palles C and Heinimann K (2018). The evolutionary landscape of colorectal tumorigenesis. Nat Ecol Evol  vol. 2, (10) 1661-1672. 10.1038/s41559-018-0642-z
Foxler DE, Bridge KS, Foster JG, Grevitt P, Curry S, Shah KM, Davidson KM, Nagano A, Gadaleta E, Rhys HI, Kennedy PT, Hermida MA, Chang T-Y, Shaw PE, Reynolds LE, McKay TR, Wang H-W, Ribeiro PS, Plevin MJ, Lagos D, Lemoine NR, Rajan P, Graham TA, Chelala C, Hodivala-Dilke KM, Spendlove I and Sharp TV (2018). A HIF-LIMD1 negative feedback mechanism mitigates the pro-tumorigenic effects of hypoxia. Embo Mol Med  10.15252/emmm.201708304
Williams MJ, Werner B, Heide T, Curtis C, Barnes CP, Sottoriva A and Graham TA (2018). Quantification of subclonal selection in cancer from bulk sequencing data. Nature Genetics  vol. 50, (6) 895-903. 10.1038/s41588-018-0128-6
Temko D, Tomlinson IPM, Severini S, Schuster-Böckler B and Graham TA (2018). The effects of mutational processes and selection on driver mutations across cancer types. Nature Research  Nat Commun  vol. 9, (1) 1857-1857. 10.1038/s41467-018-04208-6
Araf S, Wang J, Korfi K, Pangault C, Kotsiou E, Rio-Machin A, Rahim T, Heward J, Clear A, Iqbal S, Davies JK, Johnson P, Calaminici M, Montoto S, Auer R, Chelala C, Gribben JG, Graham TA, Fest T, Fitzgibbon J and Okosun J (2018). Genomic profiling reveals spatial intra-tumor heterogeneity in follicular lymphoma. Leukemia  vol. 32, (5) 1258-1263. 10.1038/s41375-018-0043-y
Temko D, Van Gool IC, Rayner E, Glaire M, Makino S, Brown M, Chegwidden L, Palles C, Depreeuw J, Beggs A, Stathopoulou C, Mason J, Baker A-M, Williams M, Cerundolo V, Rei M, Taylor JC, Schuh A, Ahmed A, Amant F, Lambrechts D, Smit VT, Bosse T, Graham TA, Church DN and Tomlinson I (2018). Somatic POLE exonuclease domain mutations are early events in sporadic endometrial and colorectal carcinogenesis, determining driver mutational landscape, clonal neoantigen burden and immune response. John Wiley & Sons, Inc  J Pathol  vol. 245, (3) 283-296. 10.1002/path.5081
Quante M, Graham TA and Jansen M (2018). Insights Into the Pathophysiology of Esophageal Adenocarcinoma. Gastroenterology  vol. 154, (2) 406-420. 10.1053/j.gastro.2017.09.046
Curtius K, Wright NA and Graham TA (2018). An evolutionary perspective on field cancerization. Nat Rev Cancer  vol. 18, (1) 19-32. 10.1038/nrc.2017.102
Williams MJ, Werner B, Barnes CP, Graham TA and Sottoriva A (2018). Reply: Is the evolution of tumors Darwinian or non-Darwinian? National Science Review  vol. 5, (1) 17-19. 10.1093/nsr/nwx131

2017

Baker A-M, Huang W, Wang X-MM, Jansen M, Ma X-J, Kim J, Anderson CM, Wu X, Pan L, Su N, Luo Y, Domingo E, Heide T, Sottoriva A, Lewis A, Beggs AD, Wright NA, Rodriguez-Justo M, Park E, Tomlinson I and Graham TA (2017). Robust RNA-based in situ mutation detection delineates colorectal cancer subclonal evolution. Macmillan Publishers Limited, Part of Springer Nature  Nat Commun  vol. 8, (1) 1998-1998. 10.1038/s41467-017-02295-5
Curtius K, Wright NA and Graham TA (2017). Evolution of premalignant disease. Cold Spring Harbor Perspectives in Medicine  vol. 7, (12) 10.1101/cshperspect.a026542
Maley CC, Aktipis A, Graham TA, Sottoriva A, Boddy AM, Janiszewska M, Silva AS, Gerlinger M, Yuan Y, Pienta KJ, Anderson KS, Gatenby R, Swanton C, Posada D, Wu C-I, Schiffman JD, Hwang ES, Polyak K, Anderson ARA, Brown JS, Greaves M and Shibata D (2017). Classifying the evolutionary and ecological features of neoplasms. M a C Mill a N P U Bl I S H E R S Li Mit E D, P a Rt O F S P Ri N G E R N a T U R E  Nat Rev Cancer  vol. 17, (10) 605-619. 10.1038/nrc.2017.69
Williams MJ, Werner B, Barnes CP, Graham TA and Sottoriva A (2017). Reply: Uncertainties in tumor allele frequencies limit power to infer evolutionary pressures. Nature Genetics  vol. 49, (9) 1289-1291. 10.1038/ng.3877
Sun R, Hu Z, Sottoriva A, Graham TA, Harpak A, Ma Z, Fischer JM, Shibata D and Curtis C (2017). Between-region genetic divergence reflects the mode and tempo of tumor evolution. Nature Genetics  vol. 49, (7) 1015-1024. 10.1038/ng.3891
Martinez P, Kimberley C, BirkBak NJ, Marquard A, Szallasi Z and Graham TA (2017). Quantification of within-sample genetic heterogeneity from SNP-array data. Macmillan Publishers Limited, Part of Springer Nature.  Sci Rep  vol. 7, (1) 3248-3248. 10.1038/s41598-017-03496-0
Choi CHR, Bakir IA, Hart AL and Graham TA (2017). Clonal evolution of colorectal cancer in IBD. Nature Reviews Gastroenterology and Hepatology  vol. 14, (4) 218-229. 10.1038/nrgastro.2017.1
Shah V, Nowinski S, Levi D, Shinomiya I, Kebaier Ep Chaabouni N, Gillett C, Grigoriadis A, Graham TA, Roylance R, Simpson MA, Pinder SE and Sawyer EJ (2017). PIK3CA mutations are common in lobular carcinoma in situ, but are not a biomarker of progression. Breast Cancer Research  vol. 19, (1) 10.1186/s13058-016-0789-y
Sottoriva A, Barnes CP and Graham TA (2017). Catch my drift? Making sense of genomic intra-tumour heterogeneity. Elsevier  Biochim Biophys Acta  vol. 1867, (2) 95-100. 10.1016/j.bbcan.2016.12.003

2016

GRAHAM TA and Sottoriva A (2016). Measuring cancer evolution from the genome. Wiley  Journal of Pathology  10.1002/path.4821
Cross W, Graham TA and Wright NA (2016). New paradigms in clonal evolution: punctuated equilibrium in cancer. Wiley  Journal of Pathology  10.1002/path.4757
Martinez P, Timmer MR, Lau CT, Calpe S, Sancho-Serra MDC, Straub D, Baker A-M, Meijer SL, Kate FJWT, Mallant-Hent RC, Naber AHJ, van Oijen AHAM, Baak LC, Scholten P, Böhmer CJM, Fockens P, Bergman JJGHM, Maley CC, Graham TA and Krishnadath KK (2016). Dynamic clonal equilibrium and predetermined cancer risk in Barrett’s oesophagus. Nature Publishing Group: Nature Communications  Nature Communications  vol. 7, 12158-12158. 10.1038/ncomms12158
Lavery DL, Martinez P, Gay LJ, Cereser B, Novelli MR, Rodriguez-Justo M, Meijer SL, Graham TA, McDonald SAC, Wright NA and Jansen M (2016). Evolution of oesophageal adenocarcinoma from metaplastic columnar epithelium without goblet cells in Barrett's oesophagus. Gut  vol. 65, (6) 907-913. 10.1136/gutjnl-2015-310748
Williams MJ, Werner B, Graham TA and Sottoriva A (2016). Functional versus non-functional intratumor heterogeneity in cancer. Taylor & Francis Group  Molecular & Cellular Oncology  vol. 3, (4) e1162897-e1162897. 10.1080/23723556.2016.1162897
Findlay JM, Castro-Giner F, Makino S, Rayner E, Kartsonaki C, Cross W, Kovac M, Ulahannan D, Palles C, Gillies RS, MacGregor TP, Church D, Maynard ND, Buffa F, Cazier J-B, Graham TA, Wang L-M, Sharma RA, Middleton M and Tomlinson I (2016). Differential clonal evolution in oesophageal cancers in response to neo-adjuvant chemotherapy. Nature Communications  vol. 7, 11111-11111. 10.1038/ncomms11111
Dhawan A, Graham TA and Fletcher AG (2016). A computational modeling approach for deriving biomarkers to predict cancer risk in premalignant disease. Cancer Prevention Research  vol. 9, (4) 283-295. 10.1158/1940-6207.CAPR-15-0248
Baker AM and Graham TA (2016). Quantifying human intestinal stem cell and crypt dynamics: The implications for cancer screening and prevention. Expert Review of Gastroenterology and Hepatology  vol. 10, (3) 277-279. 10.1586/17474124.2016.1134314
Williams MJ, Werner B, Barnes CP, Graham TA and Sottoriva A (2016). Identification of neutral tumor evolution across cancer types. Nature Genetics  vol. 48, (3) 238-244. 10.1038/ng.3489
Andor N, Graham TA, Jansen M, Xia LC, Aktipis CA, Petritsch C, Ji HP and Maley CC (2016). Pan-cancer analysis of the extent and consequences of intratumor heterogeneity. Nature Medicine  vol. 22, (1) 105-113. 10.1038/nm.3984
Gay L, Baker AM and Graham TA (2016). Tumour Cell Heterogeneity. F1000research  vol. 5, 10.12688/f1000research.7210.1

2015

Choi CHR, Ignjatovic-Wilson A, Askari A, Lee GH, Warusavitarne J, Moorghen M, Thomas-Gibson S, Saunders BP, Rutter MD, Graham TA and Hart AL (2015). Low-grade dysplasia in ulcerative colitis: Risk factors for developing high-grade dysplasia or colorectal cancer. American Journal of Gastroenterology  vol. 110, (10) 1461-1471. 10.1038/ajg.2015.248
Caulin AF, Graham TA, Wang LS and Maley CC (2015). Solutions to peto’s paradox revealed by mathematical modelling and cross-species cancer gene analysis. Philosophical Transactions of The Royal Society B: Biological Sciences  vol. 370, (1673) 10.1098/rstb.2014.0222
Timmer MR, Martinez P, Lau CT, Westra WM, Calpe S, Rygiel AM, Rosmolen WD, Meijer SL, Ten Kate FJW, Dijkgraaf MGW, Mallant-Hent RC, Naber AHJ, Van Oijen AHAM, Baak LC, Scholten P, Böhmer CJM, Fockens P, Maley CC, Graham TA, Bergman JJGHM and Krishnadath KK (2015). Derivation of genetic biomarkers for cancer risk stratification in Barrett's oesophagus: A prospective cohort study. Gut  vol. 65, (10) 1602-1610. 10.1136/gutjnl-2015-309642
Asfaha S, Hayakawa Y, Muley A, Stokes S, Graham TA, Ericksen RE, Westphalen CB, Von Burstin J, Mastracci TL, Worthley DL, Guha C, Quante M, Rustgi AK and Wang TC (2015). Krt19+/Lgr5- Cells Are Radioresistant Cancer-Initiating Stem Cells in the Colon and Intestine. Cell Stem Cell  vol. 16, (6) 627-638. 10.1016/j.stem.2015.04.013
Sottoriva A, Kang H, Ma Z, Graham TA, Salomon MP, Zhao J, Marjoram P, Siegmund K, Press MF, Shibata D and Curtis C (2015). A big bang model of human colorectal tumor growth. Nature Genetics  vol. 47, (3) 209-216. 10.1038/ng.3214
Worthley DL, Churchill M, Compton JT, Tailor Y, Rao M, Si Y, Levin D, Schwartz MG, Uygur A, Hayakawa Y, Gross S, Renz BW, Setlik W, Martinez AN, Chen X, Nizami S, Lee HG, Kang HP, Caldwell JM, Asfaha S, Westphalen CB, Graham T, Jin G, Nagar K, Wang H, Kheirbek MA, Kolhe A, Carpenter J, Glaire M and Nair A (2015). Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell  vol. 160, (1-2) 269-284. 10.1016/j.cell.2014.11.042
Baker AM, Graham TA, Elia G, Wright NA and Rodriguez-Justo M (2015). Characterization of LGR5 stem cells in colorectal adenomas and carcinomas. Scientific Reports  vol. 5, 10.1038/srep08654
McDonald SAC, Graham TA, Lavery DL, Wright NA and Jansen M (2015). The Barrett's Gland in Phenotype Space. Cellular and Molecular Gastroenterology and Hepatology  vol. 1, (1) 41-54. 10.1016/j.jcmgh.2014.10.001
Choi CHR, Rutter MD, Askari A, Lee GH, Warusavitarne J, Moorghen M, Thomas-Gibson S, Saunders BP, Graham TA and Hart AL (2015). Forty-year analysis of colonoscopic surveillance program for neoplasia in ulcerative colitis: An updated overview. American Journal of Gastroenterology  vol. 110, (7) 1022-1034. 10.1038/ajg.2015.65

2014

Baker AM and Graham TA (2014). Revealing human intestinal stem cell and crypt dynamics. Molecular and Cellular Oncology  vol. 1, (3) 10.4161/23723548.2014.970069
Walther V and Graham TA (2014). Location, location, location! The reality of life for an intestinal stem cell in the crypt. J Pathol  vol. 234, (1) 1-4. 10.1002/path.4370
Baker A-M, Cereser B, Melton S, Fletcher AG, Rodriguez-Justo M, Tadrous PJ, Humphries A, Elia G, McDonald SAC, Wright NA, Simons BD, Jansen M and Graham TA (2014). Quantification of crypt and stem cell evolution in the normal and neoplastic human colon. Cell Rep  vol. 8, (4) 940-947. 10.1016/j.celrep.2014.07.019
Pipinikas CP, Kiropoulos TS, Teixeira VH, Brown JM, Varanou A, Falzon M, Capitanio A, Bottoms SE, Carroll B, Navani N, McCaughan F, George JP, Giangreco A, Wright NA, McDonald SAC, Graham TA and Janes SM (2014). Cell migration leads to spatially distinct but clonally related airway cancer precursors. Thorax  vol. 69, (6) 548-557. 10.1136/thoraxjnl-2013-204198
Jawad N, Graham TA, McDonald SAC and Wright NA (2014). Re: Mitochondria and tumor progression in ulcerative colitis. J Natl Cancer Inst  vol. 106, (2) 10.1093/jnci/djt436
Pipinikas CP, Kiropoulos TS, Teixeira VH, Brown JM, Varanou A, Falzon M, Capitanio A, Bottoms SE, Carrol B, Navani N, McCaughan F, George JP, Giangreco A, Wright NA, McDonald SAC, Graham TA and Janes SM (2014). Cell migration leads to spatially distinct but clonally related airway cancer precursors. Thorax  vol. 69, (6) 548-557. 10.1136/thoraxjnl-2013-204198

2013

Shaw JA, Graham TA and Stebbing J (2013). Genomic instability in pre-neoplastic colonic lesions. Oncogene  vol. 32, (46) 5331-5332. 10.1038/onc.2013.21
Teixeira VH, Nadarajan P, Graham TA, Pipinikas CP, Brown JM, Falzon M, Nye E, Poulsom R, Lawrence D, Wright NA, McDonald S, Giangreco A, Simons BD and Janes SM (2013). Stochastic homeostasis in human airway epithelium is achieved by neutral competition of basal cell progenitors. Elife  vol. 2, 10.7554/eLife.00966
Zeki SS, Haidry R, Graham TA, Rodriguez-Justo M, Novelli M, Hoare J, Dunn J, Wright NA, Lovat LB and McDonald SAC (2013). Clonal selection and persistence in dysplastic Barrett's esophagus and intramucosal cancers after failed radiofrequency ablation. Am J Gastroenterol  vol. 108, (10) 1584-1592. 10.1038/ajg.2013.238
Zeki SS, Haidry R, Graham TA, Rodriguez-Justo M, Novelli M, Hoare J, Dunn J, Wright NA, Lovat LB and McDonald SAC (2013). Clonal selection and persistence in dysplastic Barrett's esophagus and intramucosal cancers after failed radiofrequency ablation. American Journal of Gastroenterology  vol. 108, (10) 1584-1592. 10.1038/ajg.2013.238
Khan S, McDonald SAC, Wright NA, Graham TA, Odze RD, Rodriguez-Justo M and Zeki S (2013). Crypt dysplasia in Barrett's oesophagus shows clonal identity between crypt and surface cells. Journal of Pathology  vol. 231, (1) 98-104. 10.1002/path.4211
Humphries A, Cereser B, Gay LJ, Miller DSJ, Das B, Gutteridge A, Elia G, Nye E, Jeffery R, Poulsom R, Novelli MR, Rodriguez-Justo M, McDonald SAC, Wright NA and Graham TA (2013). Lineage tracing reveals multipotent stem cells maintain human adenomas and the pattern of clonal expansion in tumor evolution. Proc Natl Acad Sci U S A  vol. 110, (27) E2490-E2499. 10.1073/pnas.1220353110
Willis L, Graham TA, Alarcon T, Alison MR, Tomlinson IPM and Page KM (2013). What Can Be Learnt about Disease Progression in Breast Cancer Dormancy from Relapse Data? Plos One  vol. 8, (5) 10.1371/journal.pone.0062320
Baker A-M, Graham TA and Wright NA (2013). Pre-tumour clones, periodic selection and clonal interference in the origin and progression of gastrointestinal cancer: potential for biomarker development. J Pathol  vol. 229, (4) 502-514. 10.1002/path.4157
Lu L, Teixeira VH, Yuan Z, Graham TA, Endesfelder D, Kolluri K, Al-Juffali N, Hamilton N, Nicholson AG, Falzon M, Kschischo M, Swanton C, Wright NA, Carroll B, Watt FM, George JP, Jensen KB, Giangreco A and Janes SM (2013). LRIG1 regulates cadherin-dependent contact inhibition directing epithelial homeostasis and pre-invasive squamous cell carcinoma development. Journal of Pathology  vol. 229, (4) 608-620. 10.1002/path.4148
S Datta R, Gutteridge A, Swanton C, Maley CC and Graham TA (2013). Modelling the evolution of genetic instability during tumour progression. Evol Appl  vol. 6, (1) 20-33. 10.1111/eva.12024
Leedham SJ, Rodenas-Cuadrado P, Howarth K, Lewis A, Mallappa S, Segditsas S, Davis H, Jeffery R, Rodriguez-Justo M, Keshav S, Travis SPL, Graham TA, East J, Clark S and Tomlinson IPM (2013). A basal gradient of Wnt and stem-cell number influences regional tumour distribution in human and mouse intestinal tracts. Gut  vol. 62, (1) 83-93. 10.1136/gutjnl-2011-301601

2012

Nicholson AM, Graham TA, Simpson A, Humphries A, Burch N, Rodriguez-Justo M, Novelli M, Harrison R, Wright NA, McDonald SAC and Jankowski JA (2012). Barrett's metaplasia glands are clonal, contain multiple stem cells and share a common squamous progenitor. Gut  vol. 61, (10) 1380-1389. 10.1136/gutjnl-2011-301174
Gilbertson RJ and Graham TA (2012). Cancer: Resolving the stem-cell debate. Nature  vol. 488, (7412) 462-463. 10.1038/nature11480
Gilbertson RJ and Graham TA (2012). Cancer: Resolving the stem-cell debate. Nature  10.1038/nature11480
Humphries A, Graham TA, Cereser B, McDonald SA and Wright NA (2012). HUMAN COLORECTAL ADENOMA GROWTH IS CHARACTERISED BY PERIODS OF QUIESCENCE AND RAPID CLONAL EXPANSION. Gut  vol. 61, A7-A8. 10.1136/gutjnl-2012-302514a.16
Galandiuk S, Rodriguez-Justo M, Jeffery R, Nicholson AM, Cheng Y, Oukrif D, Elia G, Leedham SJ, McDonald SAC, Wright NA and Graham TA (2012). Field cancerization in the intestinal epithelium of patients with Crohn's ileocolitis. Gastroenterology  vol. 142, (4) 855-864.e8. 10.1053/j.gastro.2011.12.004
Zeki S, Graham TA and McDonald SAC (2012). Utilizing DNA mutations to trace epithelial cell lineages in human tissues. Methods Mol Biol  vol. 916, 289-301. 10.1007/978-1-61779-980-8_22

2011

Zeki SS, McDonald SA and Graham TA (2011). Field cancerization in Barrett's esophagus. Discov Med  vol. 12, (66) 371-379.
Gaisa NT, Graham TA, McDonald SAC, Cañadillas-Lopez S, Poulsom R, Heidenreich A, Jakse G, Tadrous PJ, Knuechel R and Wright NA (2011). The human urothelium consists of multiple clonal units, each maintained by a stem cell. J Pathol  vol. 225, (2) 163-171. 10.1002/path.2945
Gaisa NT, Graham TA, McDonald SA, Poulsom R, Heidenreich A, Jakse G, Knuechel R and Wright NA (2011). Clonal architecture of human prostatic epithelium in benign and malignant conditions. J Pathol  vol. 225, (2) 172-180. 10.1002/path.2959
Graham TA, McDonald SA and Wright NA (2011). Field cancerization in the GI tract. Future Oncol  vol. 7, (8) 981-993. 10.2217/fon.11.70
Endesfelder D, McGranahan N, Birkbak NJ, Szallasi Z, Kschischo M, Graham TA and Swanton C (2011). A breast cancer meta-analysis of two expression measures of chromosomal instability reveals a relationship with younger age at diagnosis and high risk histopathological variables. Oncotarget  vol. 2, (7) 529-537. 10.18632/oncotarget.298
Graham TA, Humphries A, Sanders T, Rodriguez-Justo M, Tadrous PJ, Preston SL, Novelli MR, Leedham SJ, McDonald SAC and Wright NA (2011). Use of methylation patterns to determine expansion of stem cell clones in human colon tissue. Gastroenterology  vol. 140, (4) 10.1053/j.gastro.2010.12.036
Gutierrez-Gonzalez L, Graham TA, Rodriguez-Justo M, Leedham SJ, Novelli MR, Gay LJ, Ventayol-Garcia T, Green A, Mitchell I, Stoker DL, Preston SL, Bamba S, Yamada E, Kishi Y, Harrison R, Jankowski JA, Wright NA and McDonald SAC (2011). The clonal origins of dysplasia from intestinal metaplasia in the human stomach. Gastroenterology  vol. 140, (4) 10.1053/j.gastro.2010.12.051
Zeki SS, Graham TA and Wright NA (2011). Stem cells and their implications for colorectal cancer. Nat Rev Gastroenterol Hepatol  vol. 8, (2) 90-100. 10.1038/nrgastro.2010.211
Humphries A, Graham TA and McDonald SAC (2011). Stem cells and inflammation in the intestine. Recent Results Cancer Res  vol. 185, 51-63. 10.1007/978-3-642-03503-6_3
Nicholson AM, Graham TA, Simpson A, Humphries A, Burch N, Rodriguez-Justo M, Novelli M, Harrison R, Wright NA, McDonald SAC and Jankowski JA (2011). Barrett's metaplasia glands are clonal, contain multiple stem cells and share a common squamous progenitor. Gut  10.1136/gutjnl-2011-301174

2010

Graham TA and Leedham SJ (2010). Field defects in DNA repair: is loss of MGMT an initial event in colorectal carcinogenesis? Gut  vol. 59, (11) 1452-1453. 10.1136/gut.2010.222398
Jankowski J, Graham T and Harrison R (2010). Authors' response. Gut  vol. 59, (8) 10.1136/gut.2010.218776
Graham TA, Jawad N and Wright NA (2010). Spindles losing their bearings: Does disruption of orientation in stem cells predict the onset of cancer? Bioessays  vol. 32, (6) 468-472. 10.1002/bies.201000032
Willis L, Alarcón T, Elia G, Jones JL, Wright NA, Tomlinson IPM, Graham TA and Page KM (2010). Breast cancer dormancy can be maintained by small numbers of micrometastases. Cancer Res  vol. 70, (11) 4310-4317. 10.1158/0008-5472.CAN-09-3144
Thirlwell C, Will OCC, Domingo E, Graham TA, McDonald SAC, Oukrif D, Jeffrey R, Gorman M, Rodriguez-Justo M, Chin-Aleong J, Clark SK, Novelli MR, Jankowski JA, Wright NA, Tomlinson IPM and Leedham SJ (2010). Clonality assessment and clonal ordering of individual neoplastic crypts shows polyclonality of colorectal adenomas. Gastroenterology  vol. 138, (4) 1441-1454.e7. 10.1053/j.gastro.2010.01.033
Graham TA and McDonald SAC (2010). Genetic diversity during the development of Barrett's oesophagus-associated adenocarcinoma: how, when and why? Biochem Soc Trans  vol. 38, (2) 374-379. 10.1042/BST0380374
Lin WR, Lim SN, McDonald SAC, Graham T, Wright VL, Peplow CL, Humphries A, Kocher HM, Wright NA, Dhillon AP and Alison MR (2010). The histogenesis of regenerative nodules in human liver cirrhosis. Hepatology  vol. 51, (3) 1017-1026. 10.1002/hep.23483
Obszynska JA, Atherfold PA, Nanji M, Glancy D, Santander S, Graham TA, Otto WR, West K, Harrison RF and Jankowski JAZ (2010). Long-term proton pump induced hypergastrinaemia does induce lineage-specific restitution but not clonal expansion in benign Barrett's oesophagus in vivo. Gut  vol. 59, (2) 156-163. 10.1136/gut.2009.186775

2009

McDonald SAC, Graham TA, Schier S, Wright NA and Alison MR (2009). Stem cells and solid cancers. Virchows Arch  vol. 455, (1) 1-13. 10.1007/s00428-009-0783-1
Lanza R, Hogan B, Gaerhart J, Melton D and Pedersen R (2009). Stem Cells in the Gastrointestinal Tract. Essentials of Stem Cell Biology  Academic Pr  10.1016/B978-0-12-374729-7.00036-6
Leedham SJ, Graham TA, Oukrif D, McDonald SAC, Rodriguez-Justo M, Harrison RF, Shepherd NA, Novelli MR, Jankowski JAZ and Wright NA (2009). Clonality, Founder Mutations, and Field Cancerization in Human Ulcerative Colitis-Associated Neoplasia. Gastroenterology  vol. 136, (2) 542-550. 10.1053/j.gastro.2008.10.086

2008

Graham TA and Wright NA (2008). Investigating the fixation and spread of mutations in the gastrointestinal epithelium. Future Oncol  vol. 4, (6) 825-839. 10.2217/14796694.4.6.825
Graham T, Halford S, Page KM and Tomlinson IPM (2008). Most low-level microsatellite instability in colorectal cancers can be explained without an elevated slippage rate. Journal of Pathology  vol. 215, (2) 204-210. 10.1002/path.2351
Jones AM, Mitter R, Springall R, Graham T, Winter E, Gillett C, Hanby AM, Tomlinson IPM, Sawyer EJ, Walker R, Pinder S, Jones L, Ellis I, Puay HT, Macartney J, Green D, Hales S, Harding-Mackean C, Colclough A, MacNeil F, Rowlands D, Smith C, Fentiman I, Cane P, Desai A, Goderya R, Nerurkar A, Kissin M and Jackson P (2008). A comprehensive genetic profile of phyllodes tumours of the breast detects important mutations, intra-tumoral genetic heterogeneity and new genetic changes on recurrence. Journal of Pathology  vol. 214, (5) 533-544. 10.1002/path.2320

2007

Jones AM, Thirlwell C, Howarth KM, Graham T, Chambers W, Segditsas S, Page KM, Phillips RKS, Thomas HJW, Sieber OM, Sawyer EJ and Tomlinson IPM (2007). Analysis of copy number changes suggests chromosomal instability in a minority of large colorectal adenomas. Journal of Pathology  vol. 213, (3) 249-256. 10.1002/path.2234

2006

McDonald SAC, Graham T, Potten CS, Wright NA, Tomlinson IPM and Renehan AG (2006). Intestinal stem cells and the development of colorectal neoplasia. Tissue Stem Cells  10.3109/9781420016833-12