Allan Balmain, PhD

Professor In Residence
HDF Comprehensive Cancer Ctr
+1 415 502-4180

Research in the Balmain laboratory has been focused on developing a deep understanding of how cancers emerge from normal tissues through a series of steps, from the first initiating event in single cells to early stage preneoplasia and then progression to metastasis. In particular, we have sought to investigate how environmental carcinogens, including those that cause mutations and others that act as non-mutagenic tumor promoters, cause the outgrowth of cell clones that ultimately develop into malignancies. In order to address these questions, we generated genetically heterogeneous mouse populations by crossing different strains and species of mice, and exposed them to different mutagens and tumor promoters, to investigate how genes and environmental factors conspire to induce cancer. Our data have led to the identification of the initiating mutation for skin cancers induced by carcinogens, and the stem cells in which these mutations occur. Using lineage tracing of stem cells during multistage carcinogenesis, we have demonstrated that initiation of benign tumor growth, and progression to malignancy are clonal events, i.e. they involve specific changes in single cells. The use of heterogeneous mouse populations that mimic the genetic diversity of humans has allowed us to explore how networks of genes, working together, induce these events. Gene expression network analysis has identified high plasticity cell states that evolve in early stage tumors in response to chronic inflammation induced by tumor promoters, eventually causing leading to progression. Some of these same cell states are induced by treatment of fully malignant tumors with chemotherapeutic agents, possibly providing new routes to development of resistance to therapy. These mouse models have shown that genomic mutations are critical for cancer development from single cells, but emphasize the importance of the process of tumor promotion and chronic tissue damage in causing outgrowth of otherwise latent mutated cells, leading to increased cancer incidence. Whole genome sequencing of tumors induced in mice by known or suspected human carcinogens has shown that perhaps 80% of carcinogens do not act through mutational mechanisms, but are more likely to promote tumor development from cells carrying pre-existing spontaneously arising mutations in normal tissues. Further studies are underway to address the mechanisms by which promoters cause these effects, to identify promoters in the environment, and identify new strategies for cancer prevention based on inhibition of the promotion stage.

Publications: 

Gene networks reveal stem-cell state convergence during preneoplasia and progression to malignancy in multistage skin carcinogenesis.

bioRxiv : the preprint server for biology

Taylor MA, Kandyba E, Halliwill K, Delrosario R, Koroshkin M, Goodarzi H, Quigley D, Li YR, Wu D, Bollam S, Mirzoeva O, Akhurst RJ, Balmain A

Genetic polymorphism in Methylenetetrahydrofolate Reductase chloride transport protein 6 (MTHFR CLCN6) gene is associated with keratinocyte skin cancer in a cohort of renal transplant recipients.

Skin health and disease

Griffin L, Ho L, Akhurst RJ, Arron ST, Boggs JME, Conlon P, O'Kelly P, Toland AE, Epstein EH, Balmain A, Bastian BC, Moloney FJ, Murphy GM, Laing ME

Circadian PERformance in breast cancer: a germline and somatic genetic study of PER3VNTR polymorphisms and gene co-expression.

NPJ breast cancer

Fores-Martos J, Cervera-Vidal R, Sierra-Roca J, Lozano-Asencio C, Fedele V, Cornelissen S, Edvarsen H, Tadeo-Cervera I, Eroles P, Lluch A, Tabares-Seisdedos R, Falcó A, Van't Veer LJ, Schmidt M, Quigley DA, Børresen-Dale AL, Kristensen VN, Balmain A, Climent J

Targeting KRAS4A splicing through the RBM39/DCAF15 pathway inhibits cancer stem cells.

Nature communications

Chen WC, To MD, Westcott PMK, Delrosario R, Kim IJ, Philips M, Tran Q, Bollam SR, Goodarzi H, Bayani N, Mirzoeva O, Balmain A

The mutational signature profile of known and suspected human carcinogens in mice.

Nature genetics

Riva L, Pandiri AR, Li YR, Droop A, Hewinson J, Quail MA, Iyer V, Shepherd R, Herbert RA, Campbell PJ, Sills RC, Alexandrov LB, Balmain A, Adams DJ

Integration of multiple biological contexts reveals principles of synthetic lethality that affect reproducibility.

Nature communications

Ku AA, Hu HM, Zhao X, Shah KN, Kongara S, Wu D, McCormick F, Balmain A, Bandyopadhyay S

Mutational signatures in tumours induced by high and low energy radiation in Trp53 deficient mice.

Nature communications

Rose Li Y, Halliwill KD, Adams CJ, Iyer V, Riva L, Mamunur R, Jen KY, Del Rosario R, Fredlund E, Hirst G, Alexandrov LB, Adams D, Balmain A

KRAS4A directly regulates hexokinase 1.

Nature

Amendola CR, Mahaffey JP, Parker SJ, Ahearn IM, Chen WC, Zhou M, Court H, Shi J, Mendoza SL, Morten MJ, Rothenberg E, Gottlieb E, Wadghiri YZ, Possemato R, Hubbard SR, Balmain A, Kimmelman AC, Philips MR

Niche-Specific Factors Dynamically Regulate Sebaceous Gland Stem Cells in the Skin.

Developmental cell

Veniaminova NA, Grachtchouk M, Doane OJ, Peterson JK, Quigley DA, Lull MV, Pyrozhenko DV, Nair RR, Patrick MT, Balmain A, Dlugosz AA, Tsoi LC, Wong SY

α-PD-1 therapy elevates Treg/Th balance and increases tumor cell pSmad3 that are both targeted by α-TGFβ antibody to promote durable rejection and immunity in squamous cell carcinomas.

Journal for immunotherapy of cancer

Dodagatta-Marri E, Meyer DS, Reeves MQ, Paniagua R, To MD, Binnewies M, Broz ML, Mori H, Wu D, Adoumie M, Del Rosario R, Li O, Buchmann T, Liang B, Malato J, Arce Vargus F, Sheppard D, Hann BC, Mirza A, Quezada SA, Rosenblum MD, Krummel MF, Balmain A, Akhurst RJ

A model for RAS mutation patterns in cancers: finding the sweet spot.

Nature reviews. Cancer

Li S, Balmain A, Counter CM

Multicolour lineage tracing reveals clonal dynamics of squamous carcinoma evolution from initiation to metastasis.

Nature cell biology

Reeves MQ, Kandyba E, Harris S, Del Rosario R, Balmain A

Lgr6 is a stem cell marker in mouse skin squamous cell carcinoma.

Nature genetics

Huang PY, Kandyba E, Jabouille A, Sjolund J, Kumar A, Halliwill K, McCreery M, DelRosario R, Kang HC, Wong CE, Seibler J, Beuger V, Pellegrino M, Sciambi A, Eastburn DJ, Balmain A

Age, estrogen, and immune response in breast adenocarcinoma and adjacent normal tissue.

Oncoimmunology

Quigley DA, Tahiri A, Lüders T, Riis MH, Balmain A, Børresen-Dale AL, Bukholm I, Kristensen V

Panx3 links body mass index and tumorigenesis in a genetically heterogeneous mouse model of carcinogen-induced cancer.

Genome medicine

Halliwill KD, Quigley DA, Kang HC, Del Rosario R, Ginzinger D, Balmain A

Gene Expression Architecture of Mouse Dorsal and Tail Skin Reveals Functional Differences in Inflammation and Cancer.

Cell reports

Quigley DA, Kandyba E, Huang P, Halliwill KD, Sjölund J, Pelorosso F, Wong CE, Hirst GL, Wu D, Delrosario R, Kumar A, Balmain A

K-Ras Promotes Tumorigenicity through Suppression of Non-canonical Wnt Signaling.

Cell

Wang MT, Holderfield M, Galeas J, Delrosario R, To MD, Balmain A, McCormick F

Evolution of metastasis revealed by mutational landscapes of chemically induced skin cancers.

Nature medicine

McCreery MQ, Halliwill KD, Chin D, Delrosario R, Hirst G, Vuong P, Jen KY, Hewinson J, Adams DJ, Balmain A

The Trp53 delta proline (Trp53ΔP) mouse exhibits increased genome instability and susceptibility to radiation-induced, but not spontaneous, tumor development.

Molecular carcinogenesis

Adams CJ, Yu JS, Mao JH, Jen KY, Costes SV, Wade M, Shoemake J, Aina OH, Del Rosario R, Menchavez PT, Cardiff RD, Wahl GM, Balmain A

Inhibition of KRAS codon 12 mutants using a novel DNA-alkylating pyrrole-imidazole polyamide conjugate.

Nature communications

Hiraoka K, Inoue T, Taylor RD, Watanabe T, Koshikawa N, Yoda H, Shinohara K, Takatori A, Sugimoto H, Maru Y, Denda T, Fujiwara K, Balmain A, Ozaki T, Bando T, Sugiyama H, Nagase H

Genetic variation in the functional ENG allele inherited from the non-affected parent associates with presence of pulmonary arteriovenous malformation in hereditary hemorrhagic telangiectasia 1 (HHT1) and may influence expression of PTPN14.

Frontiers in genetics

Letteboer TG, Benzinou M, Merrick CB, Quigley DA, Zhau K, Kim IJ, To MD, Jablons DM, van Amstel JK, Westermann CJ, Giraud S, Dupuis-Girod S, Lesca G, Berg JH, Balmain A, Akhurst RJ

The genetics of splicing in neuroblastoma.

Cancer discovery

Chen J, Hackett CS, Zhang S, Song YK, Bell RJ, Molinaro AM, Quigley DA, Balmain A, Song JS, Costello JF, Gustafson WC, Van Dyke T, Kwok PY, Khan J, Weiss WA

The mutational landscapes of genetic and chemical models of Kras-driven lung cancer.

Nature

Westcott PM, Halliwill KD, To MD, Rashid M, Rust AG, Keane TM, Delrosario R, Jen KY, Gurley KE, Kemp CJ, Fredlund E, Quigley DA, Adams DJ, Balmain A

Lymphocyte Invasion in IC10/Basal-Like Breast Tumors Is Associated with Wild-Type TP53.

Molecular cancer research : MCR

Quigley D, Silwal-Pandit L, Dannenfelser R, Langerød A, Vollan HK, Vaske C, Siegel JU, Troyanskaya O, Chin SF, Caldas C, Balmain A, Børresen-Dale AL, Kristensen V

Expression quantitative trait loci and receptor pharmacology implicate Arg1 and the GABA-A receptor as therapeutic targets in neuroblastoma.

Cell reports

Hackett CS, Quigley DA, Wong RA, Chen J, Cheng C, Song YK, Wei JS, Pawlikowska L, Bao Y, Goldenberg DD, Nguyen K, Gustafson WC, Rallapalli SK, Cho YJ, Cook JM, Kozlov S, Mao JH, Van Dyke T, Kwok PY, Khan J, Balmain A, Fan Q, Weiss WA

Milestones in skin carcinogenesis: the biology of multistage carcinogenesis.

The Journal of investigative dermatology

Balmain A, Yuspa SH

Modeling cutaneous squamous carcinoma development in the mouse.

Cold Spring Harbor perspectives in medicine

Huang PY, Balmain A

A multilevel model of postmenopausal breast cancer incidence.

Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology

Hiatt RA, Porco TC, Liu F, Balke K, Balmain A, Barlow J, Braithwaite D, Diez-Roux AV, Kushi LH, Moasser MM, Werb Z, Windham GC, Rehkopf DH

Identification of Hipk2 as an essential regulator of white fat development.

Proceedings of the National Academy of Sciences of the United States of America

Sjölund J, Pelorosso FG, Quigley DA, DelRosario R, Balmain A

Cellular reprogramming in skin cancer.

Seminars in cancer biology

Song IY, Balmain A

The 5p12 breast cancer susceptibility locus affects MRPS30 expression in estrogen-receptor positive tumors.

Molecular oncology

Quigley DA, Fiorito E, Nord S, Van Loo P, Alnæs GG, Fleischer T, Tost J, Moen Vollan HK, Tramm T, Overgaard J, Bukholm IR, Hurtado A, Balmain A, Børresen-Dale AL, Kristensen V

Keratin 16 regulates innate immunity in response to epidermal barrier breach.

Proceedings of the National Academy of Sciences of the United States of America

Lessard JC, Piña-Paz S, Rotty JD, Hickerson RP, Kaspar RL, Balmain A, Coulombe PA

Tmem79/Matt is the matted mouse gene and is a predisposing gene for atopic dermatitis in human subjects.

The Journal of allergy and clinical immunology

Saunders SP, Goh CS, Brown SJ, Palmer CN, Porter RM, Cole C, Campbell LE, Gierlinski M, Barton GJ, Schneider G, Balmain A, Prescott AR, Weidinger S, Baurecht H, Kabesch M, Gieger C, Lee YA, Tavendale R, Mukhopadhyay S, Turner SW, Madhok VB, Sullivan FM, Relton C, Burn J, Meggitt S, Smith CH, Allen MA, Barker JN, Reynolds NJ, Cordell HJ, Irvine AD, McLean WH, Sandilands A, Fallon PG

Inflammation and Hras signaling control epithelial-mesenchymal transition during skin tumor progression.

Genes & development

Wong CE, Yu JS, Quigley DA, To MD, Jen KY, Huang PY, Del Rosario R, Balmain A

Multiple self-healing squamous epithelioma (MSSE): rare variants in an adjacent region of chromosome 9q22.3 to known TGFBR1 mutations suggest a digenic or multilocus etiology.

The Journal of investigative dermatology

Kang HC, Quigley DA, Kim IJ, Wakabayashi Y, Ferguson-Smith MA, D'Alessandro M, Birgitte Lane E, Akhurst RJ, Goudie DR, Balmain A

Murine microenvironment metaprofiles associate with human cancer etiology and intrinsic subtypes.

Clinical cancer research : an official journal of the American Association for Cancer Research

Nguyen DH, Fredlund E, Zhao W, Perou CM, Balmain A, Mao JH, Barcellos-Hoff MH

Rewiring of human lung cell lineage and mitotic networks in lung adenocarcinomas.

Nature communications

Kim IJ, Quigley D, To MD, Pham P, Lin K, Jo B, Jen KY, Raz D, Kim J, Mao JH, Jablons D, Balmain A

Ptch1 overexpression drives skin carcinogenesis and developmental defects in K14Ptch(FVB) mice.

The Journal of investigative dermatology

Kang HC, Wakabayashi Y, Jen KY, Mao JH, Zoumpourlis V, Del Rosario R, Balmain A

Interactions between wild-type and mutant Ras genes in lung and skin carcinogenesis.

Oncogene

To MD, Rosario RD, Westcott PM, Banta KL, Balmain A

Pten regulates Aurora-A and cooperates with Fbxw7 in modulating radiation-induced tumor development.

Molecular cancer research : MCR

Kwon YW, Kim IJ, Wu D, Lu J, Stock WA, Liu Y, Huang Y, Kang HC, DelRosario R, Jen KY, Perez-Losada J, Wei G, Balmain A, Mao JH

Progressive genomic instability in the FVB/Kras(LA2) mouse model of lung cancer.

Molecular cancer research : MCR

To MD, Quigley DA, Mao JH, Del Rosario R, Hsu J, Hodgson G, Jacks T, Balmain A

Hipk2 cooperates with p53 to suppress γ-ray radiation-induced mouse thymic lymphoma.

Oncogene

Mao JH, Wu D, Kim IJ, Kang HC, Wei G, Climent J, Kumar A, Pelorosso FG, DelRosario R, Huang EJ, Balmain A

Fine-tuning p53 activity through C-terminal modification significantly contributes to HSC homeostasis and mouse radiosensitivity.

Genes & development

Wang YV, Leblanc M, Fox N, Mao JH, Tinkum KL, Krummel K, Engle D, Piwnica-Worms D, Piwnica-Worms H, Balmain A, Kaushansky K, Wahl GM

Network analysis of skin tumor progression identifies a rewired genetic architecture affecting inflammation and tumor susceptibility.

Genome biology

Quigley DA, To MD, Kim IJ, Lin KK, Albertson DG, Sjolund J, Pérez-Losada J, Balmain A

C/EBPδ: friend or foe? a novel role for C/EBPδ in metastasis.

The EMBO journal

Pelorosso FG, Balmain A

Polymorphic genetic control of tumor invasion in a mouse model of pancreatic neuroendocrine carcinogenesis.

Proceedings of the National Academy of Sciences of the United States of America

Chun MG, Mao JH, Chiu CW, Balmain A, Hanahan D

Deletion of the PER3 gene on chromosome 1p36 in recurrent ER-positive breast cancer.

Journal of clinical oncology : official journal of the American Society of Clinical Oncology

Climent J, Perez-Losada J, Quigley DA, Kim IJ, Delrosario R, Jen KY, Bosch A, Lluch A, Mao JH, Balmain A

Guidelines for the welfare and use of animals in cancer research.

British journal of cancer

Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, Double JA, Everitt J, Farningham DA, Glennie MJ, Kelland LR, Robinson V, Stratford IJ, Tozer GM, Watson S, Wedge SR, Eccles SA, Committee of the National Cancer Research Institute

Presenilin modulates EGFR signaling and cell transformation by regulating the ubiquitin ligase Fbw7.

Oncogene

Rocher-Ros V, Marco S, Mao JH, Gines S, Metzger D, Chambon P, Balmain A, Saura CA

An HDAC1-binding domain within FATS bridges p21 turnover to radiation-induced tumorigenesis.

Oncogene

Li Z, Zhang Q, Mao JH, Weise A, Mrasek K, Fan X, Zhang X, Liehr T, Lu KH, Balmain A, Cai WW

Proceedings from the 2009 genetic syndromes of the Ras/MAPK pathway: From bedside to bench and back.

American journal of medical genetics. Part A

Rauen KA, Schoyer L, McCormick F, Lin AE, Allanson JE, Stevenson DA, Gripp KW, Neri G, Carey JC, Legius E, Tartaglia M, Schubbert S, Roberts AE, Gelb BD, Shannon K, Gutmann DH, McMahon M, Guerra C, Fagin JA, Yu B, Aoki Y, Neel BG, Balmain A, Drake RR, Nolan GP, Zenker M, Bollag G, Sebolt-Leopold J, Gibbs JB, Silva AJ, Patton EE, Viskochil DH, Kieran MW, Korf BR, Hagerman RJ, Packer RJ, Melese T

A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis.

Cell

Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, Hann B, Solari A, Bobisse S, Rondina MB, Guzzardo V, Parenti AR, Rosato A, Bicciato S, Balmain A, Piccolo S

Genetic architecture of mouse skin inflammation and tumour susceptibility.

Nature

Quigley DA, To MD, Pérez-Losada J, Pelorosso FG, Mao JH, Nagase H, Ginzinger DG, Balmain A

Sequence divergence of Mus spretus and Mus musculus across a skin cancer susceptibility locus.

BMC genomics

Mahler KL, Fleming JL, Dworkin AM, Gladman N, Cho HY, Mao JH, Balmain A, Toland AE

FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression.

Science (New York, N.Y.)

Mao JH, Kim IJ, Wu D, Climent J, Kang HC, DelRosario R, Balmain A

Kras regulatory elements and exon 4A determine mutation specificity in lung cancer.

Nature genetics

To MD, Wong CE, Karnezis AN, Del Rosario R, Di Lauro R, Balmain A

Dissociation of epithelial and neuroendocrine carcinoma lineages in the transgenic adenocarcinoma of mouse prostate model of prostate cancer.

The American journal of pathology

Chiaverotti T, Couto SS, Donjacour A, Mao JH, Nagase H, Cardiff RD, Cunha GR, Balmain A

HIPK2 represses beta-catenin-mediated transcription, epidermal stem cell expansion, and skin tumorigenesis.

Proceedings of the National Academy of Sciences of the United States of America

Wei G, Ku S, Ma GK, Saito S, Tang AA, Zhang J, Mao JH, Appella E, Balmain A, Huang EJ

Crosstalk between Aurora-A and p53: frequent deletion or downregulation of Aurora-A in tumors from p53 null mice.

Cancer cell

Mao JH, Wu D, Perez-Losada J, Jiang T, Li Q, Neve RM, Gray JW, Cai WW, Balmain A

A functional switch from lung cancer resistance to susceptibility at the Pas1 locus in Kras2LA2 mice.

Nature genetics

To MD, Perez-Losada J, Mao JH, Hsu J, Jacks T, Balmain A

Genetic variants of Tgfb1 act as context-dependent modifiers of mouse skin tumor susceptibility.

Proceedings of the National Academy of Sciences of the United States of America

Mao JH, Saunier EF, de Koning JP, McKinnon MM, Higgins MN, Nicklas K, Yang HT, Balmain A, Akhurst RJ

Genomic instability in radiation-induced mouse lymphoma from p53 heterozygous mice.

Oncogene

Mao JH, Li J, Jiang T, Li Q, Wu D, Perez-Losada J, DelRosario R, Peterson L, Balmain A, Cai WW

Crosstalk between Pten and Ras signaling pathways in tumor development.

Cell cycle (Georgetown, Tex.)

To MD, Perez-Losada J, Mao JH, Balmain A

p63 and p73 do not contribute to p53-mediated lymphoma suppressor activity in vivo.

Oncogene

Perez-Losada J, Wu D, DelRosario R, Balmain A, Mao JH

Aurora-A/STK15 T+91A is a general low penetrance cancer susceptibility gene: a meta-analysis of multiple cancer types.

Carcinogenesis

Ewart-Toland A, Dai Q, Gao YT, Nagase H, Dunlop MG, Farrington SM, Barnetson RA, Anton-Culver H, Peel D, Ziogas A, Lin D, Miao X, Sun T, Ostrander EA, Stanford JL, Langlois M, Chan JM, Yuan J, Harris CC, Bowman ED, Clayman GL, Lippman SM, Lee JJ, Zheng W, Balmain A

Mapping segmental and sequence variations among laboratory mice using BAC array CGH.

Genome research

Snijders AM, Nowak NJ, Huey B, Fridlyand J, Law S, Conroy J, Tokuyasu T, Demir K, Chiu R, Mao JH, Jain AN, Jones SJ, Balmain A, Pinkel D, Albertson DG

Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene.

Nature

Mao JH, Perez-Losada J, Wu D, Delrosario R, Tsunematsu R, Nakayama KI, Brown K, Bryson S, Balmain A

Synergistic effects of STK15 gene polymorphisms and endogenous estrogen exposure in the risk of breast cancer.

Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology

Dai Q, Cai QY, Shu XO, Ewart-Toland A, Wen WQ, Balmain A, Gao YT, Zheng W

Forty years of cancer modelling in the mouse.

European journal of cancer (Oxford, England : 1990)

Hirst GL, Balmain A

Genomic segmental polymorphisms in inbred mouse strains.

Nature genetics

Li J, Jiang T, Mao JH, Balmain A, Peterson L, Harris C, Rao PH, Havlak P, Gibbs R, Cai WW

Mutually exclusive mutations of the Pten and ras pathways in skin tumor progression.

Genes & development

Mao JH, To MD, Perez-Losada J, Wu D, Del Rosario R, Balmain A

A gain of function TGFB1 polymorphism may be associated with late stage prostate cancer.

Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology

Ewart-Toland A, Chan JM, Yuan J, Balmain A, Ma J

Cancer: dangerous liaisons.

Nature

Balmain A, Akhurst RJ

Characterizing the protective component of the alphabeta T cell response to transplantable squamous cell carcinoma.

The Journal of investigative dermatology

Girardi M, Oppenheim D, Glusac EJ, Filler R, Balmain A, Tigelaar RE, Hayday AC

The genetics of cancer susceptibility: from mouse to man.

Toxicologic pathology

Ewart-Toland A, Balmain A

Genetic interactions between Pten and p53 in radiation-induced lymphoma development.

Oncogene

Mao JH, Wu D, Perez-Losada J, Nagase H, DelRosario R, Balmain A

Identification of Stk6/STK15 as a candidate low-penetrance tumor-susceptibility gene in mouse and human.

Nature genetics

Ewart-Toland A, Briassouli P, de Koning JP, Mao JH, Yuan J, Chan F, MacCarthy-Morrogh L, Ponder BA, Nagase H, Burn J, Ball S, Almeida M, Linardopoulos S, Balmain A

Stem-cell hierarchy in skin cancer.

Nature reviews. Cancer

Perez-Losada J, Balmain A

The genetics and genomics of cancer.

Nature genetics

Balmain A, Gray J, Ponder B

Developing novel oncolytic adenoviruses through bioselection.

Journal of virology

Yan W, Kitzes G, Dormishian F, Hawkins L, Sampson-Johannes A, Watanabe J, Holt J, Lee V, Dubensky T, Fattaey A, Hermiston T, Balmain A, Shen Y

Genomic approaches to identification of tumour-susceptibility genes using mouse models.

Current opinion in genetics & development

Mao JH, Balmain A

Novel approaches to identify low-penetrance cancer susceptibility genes using mouse models.

Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer

de Koning JP, Mao JH, Balmain A

Metastasis is driven by sequential elevation of H-ras and Smad2 levels.

Nature cell biology

Oft M, Akhurst RJ, Balmain A

High activity of serum response factor in the mesenchymal transition of epithelial tumor cells is regulated by RhoA signaling.

The Journal of biological chemistry

Psichari E, Balmain A, Plows D, Zoumpourlis V, Pintzas A

Genome-wide detection of chromosomal imbalances in tumors using BAC microarrays.

Nature biotechnology

Cai WW, Mao JH, Chow CW, Damani S, Balmain A, Bradley A

Absence of the CAAX endoprotease Rce1: effects on cell growth and transformation.

Molecular and cellular biology

Bergo MO, Ambroziak P, Gregory C, George A, Otto JC, Kim E, Nagase H, Casey PJ, Balmain A, Young SG

Building 'validated' mouse models of human cancer.

Current opinion in cell biology

Hann B, Balmain A

TGF-beta signaling in tumor suppression and cancer progression.

Nature genetics

Derynck R, Akhurst RJ, Balmain A

Role of matrix metalloproteinase-9 in progression of mouse skin carcinogenesis.

Molecular carcinogenesis

Papathoma AS, Zoumpourlis V, Balmain A, Pintzas A

TGF-beta inhibits p70 S6 kinase via protein phosphatase 2A to induce G(1) arrest.

Genes & development

Petritsch C, Beug H, Balmain A, Oft M

Productive replication of human adenoviruses in mouse epidermal cells.

Journal of virology

Ganly I, Mautner V, Balmain A

Integration of positive and negative growth signals during ras pathway activation in vivo.

Current opinion in genetics & development

Frame S, Balmain A

A subset of skin tumor modifier loci determines survival time of tumor-bearing mice.

Proceedings of the National Academy of Sciences of the United States of America

Nagase H, Mao JH, Balmain A

Target genes and target cells in carcinogenesis.

British journal of cancer

Frame S, Balmain A

Oncogenes and cell proliferation.

Current opinion in genetics & development

Dyson N, Balmain A

Epithelial carcinogenesis in the mouse: correlating the genetics and the biology.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences

Frame S, Crombie R, Liddell J, Stuart D, Linardopoulos S, Nagase H, Portella G, Brown K, Street A, Akhurst R, Balmain A

Transforming growth factor beta is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion.

Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research

Portella G, Cumming SA, Liddell J, Cui W, Ireland H, Akhurst RJ, Balmain A

Stochastic modelling of tumorigenesis in p53 deficient mice.

British journal of cancer

Mao JH, Lindsay KA, Balmain A, Wheldon TE

Chromosomal and genetic alterations of 7,12-dimethylbenz[a]anthracene-induced melanoma from TP-ras transgenic mice.

Molecular carcinogenesis

Gause PR, Lluria-Prevatt M, Keith WN, Balmain A, Linardopolous S, Warneke J, Powell MB

Changes in gap junctional intercellular communication in mouse skin carcinogenesis.

Carcinogenesis

Holden PR, McGuire B, Stoler A, Balmain A, Pitts JD

The p53 response to ionising radiation in adult and developing murine tissues.

Oncogene

MacCallum DE, Hupp TR, Midgley CA, Stuart D, Campbell SJ, Harper A, Walsh FS, Wright EG, Balmain A, Lane DP, Hall PA

Altered epidermal cell growth control in vivo by inducible expression of transforming growth factor beta 1 in the skin of transgenic mice.

Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research

Fowlis DJ, Cui W, Johnson SA, Balmain A, Akhurst RJ

Multigenic control of skin tumour development in mice.

Ciba Foundation symposium

Nagase H, Bryson S, Fee F, Balmain A

Deletion and altered regulation of p16INK4a and p15INK4b in undifferentiated mouse skin tumors.

Cancer research

Linardopoulos S, Street AJ, Quelle DE, Parry D, Peters G, Sherr CJ, Balmain A

Cancer. Exploring the bowels of DNA methylation.

Current biology : CB

Balmain A

Distinct genetic loci control development of benign and malignant skin tumours in mice.

Nature genetics

Nagase H, Bryson S, Cordell H, Kemp CJ, Fee F, Balmain A

Transgenic mice and squamous multistage skin carcinogenesis.

Cancer metastasis reviews

Brown K, Balmain A

Concerted action of TGF-beta 1 and its type II receptor in control of epidermal homeostasis in transgenic mice.

Genes & development

Cui W, Fowlis DJ, Cousins FM, Duffie E, Bryson S, Balmain A, Akhurst RJ

Regulatory elements in the first intron of the mouse Ha-ras gene.

Molecular carcinogenesis

Telliez JB, Plumb M, Balmain A, Bailleul B

Hyperpigmentation and melanocytic hyperplasia in transgenic mice expressing the human T24 Ha-ras gene regulated by a mouse tyrosinase promoter.

Molecular carcinogenesis

Powell MB, Hyman P, Bell OD, Balmain A, Brown K, Alberts D, Bowden GT

An allelotype of squamous carcinoma of the head and neck using microsatellite markers.

Cancer research

Ah-See KW, Cooke TG, Pickford IR, Soutar D, Balmain A

The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice.

Cancer research

Merritt AJ, Potten CS, Kemp CJ, Hickman JA, Balmain A, Lane DP, Hall PA

Importance of genetic alterations in tumour development.

Archives of toxicology. Supplement. = Archiv fur Toxikologie. Supplement

Brown K, Kemp C, Burns P, Balmain A

Molecular mechanisms of invasion and metastasis during mouse skin tumour progression.

Invasion & metastasis

Portella G, Liddell J, Crombie R, Haddow S, Clarke M, Stoler AB, Balmain A

Transgenic approaches to the analysis of ras and p53 function in multistage carcinogenesis.

Cold Spring Harbor symposia on quantitative biology

Kemp CJ, Burns PA, Brown K, Nagase H, Balmain A

Oncogenes and tumour suppressor genes in transgenic mouse models of neoplasia.

European journal of cancer (Oxford, England : 1990)

Fowlis DJ, Balmain A

Positive and negative growth control in multistage skin carcinogenesis.

Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer

Brown K, Kemp CJ, Burns PA, Stoler AB, Fowlis DJ, Akhurst RJ, Balmain A

Potential therapeutic targets in multistep oncogenesis.

Seminars in cancer biology

Burns PA, Balmain A

Discordant transforming growth factor beta 1 RNA and protein localization during chemical carcinogenesis of the skin.

Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research

Fowlis DJ, Flanders KC, Duffie E, Balmain A, Akhurst RJ

Expression of simple epithelial cytokeratins in mouse epidermal keratinocytes harboring Harvey ras gene alterations.

Cancer research

Diaz-Guerra M, Haddow S, Bauluz C, Jorcano JL, Cano A, Balmain A, Quintanilla M

Comparison of ras activation during epidermal carcinogenesis in vitro and in vivo.

Carcinogenesis

Quintanilla M, Haddow S, Jonas D, Jaffe D, Bowden GT, Balmain A

Genetic changes during mouse skin tumorigenesis.

Environmental health perspectives

Burns PA, Bremner R, Balmain A

Functional loss of tumour suppressor genes in multistage chemical carcinogenesis.

Princess Takamatsu symposia

Balmain A, Kemp CJ, Burns PA, Stoler AB, Fowlis DJ, Akhurst RJ

Molecular alterations in oncogenes or tumor suppressor genes during chemical carcinogenesis.

Progress in histochemistry and cytochemistry

Burns PA, Brown K, Bremner R, Clarke M, Balmain A

Structural analysis of the mouse c-Ha-ras gene promoter.

Molecular carcinogenesis

Plumb M, Telliez JB, Fee F, Daubersies P, Bailleul B, Balmain A

Skin hyperkeratosis and papilloma formation in transgenic mice expressing a ras oncogene from a suprabasal keratin promoter.

Cell

Bailleul B, Surani MA, White S, Barton SC, Brown K, Blessing M, Jorcano J, Balmain A

Carcinogen-induced mutations in the mouse c-Ha-ras gene provide evidence of multiple pathways for tumor progression.

Proceedings of the National Academy of Sciences of the United States of America

Brown K, Buchmann A, Balmain A

Analysis of the HMGI nuclear proteins in mouse neoplastic cells induced by different procedures.

Experimental cell research

Giancotti V, Buratti E, Perissin L, Zorzet S, Balmain A, Portella G, Fusco A, Goodwin GH

Chemical induction of oncogene mutations and growth factor activity in mouse skin carcinogenesis.

Environmental health perspectives

Bailleul B, Brown K, Ramsden M, Akhurst RJ, Fee F, Balmain A

Initiation of skin carcinogenesis can occur by induction of carcinogen-specific point mutations in the Harvey-ras gene.

Progress in clinical and biological research

Bailleul B, Brown K, Ramsden M, Fee F, Balmain A

The action of oncogenes and growth factors in tumour initiation and promotion.

Carcinogenesis; a comprehensive survey

Akhurst R, Bailleul B, Brown K, Ramsden M, Fee F, Balmain A

Molecular analysis of chemical carcinogenesis in the skin.

The British journal of cancer. Supplement

Balmain A, Brown K, Akhurst RJ, Fee FM

Isolation and characterization of the 5' flanking region of the mouse c-Harvey-ras gene.

Molecular carcinogenesis

Brown K, Bailleul B, Ramsden M, Fee F, Krumlauf R, Balmain A

Oncogene activation in chemical carcinogenesis.

Advances in cancer research

Balmain A, Brown K

An approach to the molecular mechanisms of cancer induction.

The Journal of pathology

Balmain A, Quintanilla M, Brown K, Ramsden M

Identification of a rapidly labelled 350K histidine-rich protein in neonatal mouse epidermis.

Differentiation; research in biological diversity

Ramsden M, Loehren D, Balmain A

Cloning and characterisation of the abundant cytoplasmic 7S RNA from mouse cells.

Nucleic acids research

Balmain A, Krumlauf R, Vass JK, Birnie GD

Nick translation of mammalian DNA.

Biochimica et biophysica acta

Balmain A, Birnie GD

Research Area: 
Adipocyte and Metabolism