Education and qualifications:
2009 – 2011
PGC, Academic Practice, University of Surrey, Guildford, Surrey, UK
1989 – 1994
PhD, Molecular Biology and Genetics, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
1991 – 1993
Doctoral research, Institute Curie, Paris, France
1984 – 1988
BSc, Biological Sciences, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
Lecturer in DNA Damage and Ageing/Toxicology (University of Surrey)
2008 – 2009
Research fellow (St. George’s University of London)
2001 – 2008
Research scientist (Massachusetts Institute of Technology, Cambridge, USA)
1999 – 2000
Instructor (UT Southwestern Medical Center, Dallas, USA)
1995 – 1998
Post-doctoral fellow (UT Southwestern Medical Center, Dallas, USA)
Summary and Research Vision
The overarching theme of my research has been the study of cellular responses to stress and their importance in the pathogenesis and therapeutics of cancer and other chronic diseases. In particular, my work has focused on alkylating agents, a ubiquitous family of reactive chemicals that are cytotoxic and mutagenic and pose significant threats to human health but are also commonly used systemically in the clinic as cancer chemotherapeutic agents.
My research has uncovered novel relationships between stress pathways and cellular metabolism that are important in the response to alkylating agents. The long-term goal of my research is to use knowledge from our studies to define new mechanisms of stress response and to develop therapies to treat human disease.
BMS1025 - Cell Biology
BMS3063 - Cancer: Pathogenesis and Therapeutics
BMS3099 - Mechanistic Toxicology and Pharmacokinetics
BMSM024 - Developing as a Scientist: Advanced Techniques in Biochemistry
Courses I teach on
Antioxidants neutralise free radicals including reactive oxygen specied (ROS), and have been widely reported to protect against disease. However, some studies have also reported that anti-oxidants may instead make disease progression worse. This thesis aims at evaluating the role of antioxidants in the cellular response to the alkylating agent, methylmethane sulfonate.
WT and Aag-deficient mouse embryonic fibroblasts (MEFs) were pre-treated with the antioxidant N-acetylcysteine (NAC) and exposed to MMS. NAC increased MMS-induced cell death in both Aag-deficient and wild-type (WT) MEFs. These were further confirmed with embryonic stem cells (ESc) being also sensitized to MMS-induced cell death by the anti-oxidant 2-mercaptoethanol (2-ME); and with 661W photoreceptor cells being sensitised to MMS-induced cell death by a commercial antioxidant mixture and NAC.
MEFs exhibited ROS generation when exposed to MMS, which was abrogated with NAC. The mitochondrial superoxide probe MitoSox proves that the MMS-induced ROS generation did not originate from the mitochondria. The NADPH oxidase inhibitor Diphenyleneiodonium (DPI) abrogated MMS-induced ROS generation and also sensitised cells to MMS in a similar fashion to NAC. Collectively, we conclude that cells generate ROS as a response to MMS treatment, and that this ROS generation is essential for cell survival.
We also show by using different glucose concentrations, ATP levels appear to be irrelevant to MMS-induced cell death, and that higher basal NAD levels correlates with higher amount of MMS-induced cell death.
This work reports the characterization of several glioblastoma cell lines in terms of their repair status and sensitivity to traditional therapy of X-ray irradiation and TMZ. We find that the expression of BER proteins differed between cell lines, with alkyladenine-DNA-glycosylase (AAG) showing the greatest variation in expression. Sensitivity to TMZ and X-rays was MGMT dependent. Moreover, our results suggest that cell lines expressing higher AAG levels display increased sensitivity to X-rays and TMZ combination treatment in an MGMT independent fashion.
Pharmacological inhibition of BER enzymes AP-endonuclease (APE) and polymerase b (PolB) was examined, intending to enhance sensitivity of the glioblastoma cell lines to TMZ and X-ray or proton treatment. Methoxyamine (MX), an inhibitor of AP-endonuclease (APE) activity, leads to a modest increase in TMZ sensitivity. The combination of X-rays, MX and TMZ sensitised MGMT-negative cell lines, this was not seen in proton radiation. PolB inhibition greatly increased TMZ toxicity in conjunction with radiation in glioblastoma cell lines.
Proton irradiation systems were analysed and developed within this work, leading to a high-throughput broadbeam irradiation system. These methodologies lead to differences being detected in response to proton irradiation depending on the method used. This might in future, lead to further understanding of low-dose hypersensitivity.
In conclusion, the modulation of BER can enhance glioblastoma sensitivity to current treatment modalities, however, this is in an MGMT dependent fashion. These studies could provide insight for current clinical trials.
model to examine differences between cell types on flux through the pathway. A novel assay format was developed and optimised to measure uracil DNA glycosylase, AP endonuclease, DNA polymerase ², DNA ligase, AP site repair and complete base repair. Data was generated for each enzyme activity in HepG2, Caco-2, and peripheral blood mononuclear cells (PBMCs), and the effects on the pathway were predicted using a mathematical model. In addition, the assay was used to examine variability in enzyme activity between the two cell lines, correlations between enzyme activities in primary human cells, and the effects of caloric restriction on BER in a human weight loss intervention trial. The model revealed marked differences in the response to aberrant uracil between the two immortalised cell lines and the PBMCs, with PBMC nuclear extract in general excising the base more slowly and causing a smaller and slower accumulation of harmful intermediates, such as abasic sites and single strand breaks, compared to the immortalised cell lines. The model underestimated complete repair when compared to the biological data for all cell types, potentially due to cooperativity between BER enzymes not captured when repair steps were measured individually under experimental conditions. There were also significant correlations found between enzyme activities in PBMC extracts from different individuals, and a significant predictive effect of weight loss method on polymerase ² activity in the caloric restriction trial. In conclusion, the research described here uncovered novel information regarding the effects of weight loss on DNA repair, and correlations between BER enzyme activities in healthy volunteers. This is also the first work to compare BER profiles of different cell types using biological data and mathematical modelling.
the DNA base excision repair pathway. The assays are highly sensitive: using HepG2 nuclear extract, enzyme activities were quantifiable at concentrationsof 0.0002 to 0.181 g per reaction, depending on the enzyme being measured. Assay coefficients of variation are comparable with other microplate-based assays. The assay format requires no specialist equipment and has the potential to be extended for analysis of a wide range of DNA repair enzyme activities. As such, these assays hold considerable promise for gaining new mechanistic insights into how DNA repair is related to individual genetics, disease status or progression and other environmental factors and investigating whether DNA repair activities can be used a biomarker of disease risk.
Most studies to-date have focussed on animal models and cells cultured directly from atherosclerotic plaque to ascertain if altered DDR and DNA repair exist and indeed contribute to the atherosclerotic process. By using peripheral whole blood as the base for down-stream analyses, an accessible method of determining if altered expression of genes involved in DDR and enzymes involved in DNA repair could be exploited.
DNA ligase is crucial in single (ssDNA) and double-stranded DNA break repair (DSBR) by facilitating the joining of DNA strands by catalysing phosphodiester bond formation. It was therefore chosen as a marker of DNA repair being a key enzyme involved in base excision repair (BER) and DSBR.
This study examined the differential expression of 22 genes pertinent in the DNA damage and response pathway (DDR), in addition to DNA ligase activity, between patients with stable, unstable coronary atherosclerosis (both undergoing percutaneous coronary intervention for obstructive coronary disease) and healthy controls. In addition, correlations were performed between atherosclerotic plaque features and both DNA ligase activity and the genes of interest. To accurately analyse plaque morphology, frequency domain optical coherence tomography (FD-OCT) was used which allowed high resolution delineation of fibrous tissue, lipid accumulation, calcific deposition and fibrous cap thickness, all key features in plaque vulnerability and therefore of clinical significance.
Peripheral blood mononuclear cells (PBMC) were isolated and DNA repair activity was measured from derived nuclear extracts, using a novel microplate assay examining mean
apparent DNA ligase activity. A custom microarray for the 22 genes of interest was used to perform quantitative reverse transcription polymerase chain reaction for differential gene expression between all 3 cohorts of patients recruited.
Data from this study demonstrated differences in DNA ligase activity and expression of genes involved in the DDR in patients with coronary atherosclerosis. DNA ligase activity correlated with the arc of lipid and cap thickness in both stable and unstable coronary patients. Differential DDR gene expression also correlated with fibrous cap thickness, predominantly in the unstable coronary group. This suggests that such alterations may contribute to the development and progression of the atherosclerotic lipid rich necrotic core as well as protective fibrous cap thickness.
Although significant correlations were found between DNA ligase, genes of interest and plaque features, this study demonstrates an association but does not provide a direct mechanism by which alterations in DDR contribute to atherogenesis.
Further studies are required to address differential expression across a broader spectrum of genes involved in DDR in coronary artery disease.
The aim of this study was to examine DNA ligase activity and expression of DNA damage response pathway (DDR) genes in patients with stable angina (SA) and non-ST elevation myocardial infarction (NSTEMI) and determine whether they correlate with plaque morphology.
Patients with coronary artery disease (CAD) have evidence of deoxyribonucleic acid (DNA) damage in peripheral blood mononuclear cells (PBMCs). It is unclear whether this represents excess damage or defective DNA repair activity.
DNA ligase activity and the expression of 22 DDR genes were measured in PBMCs of patients (both SA (n/=/47) and NSTEMI (n/=/42)) and in age and gender-matched controls (n/=/35). Target lesion anatomical assessment was undertaken with frequency domain optical coherent tomography.
DNA ligase activity was different across the three groups of patients (control/=/119/±/53, NSTEMI/=/115.6/±/85.1, SA/=/81/±/55.7/units/g of nuclear protein; ANOVA p/=/0.023). Pair wise comparison demonstrated that this significance is due to differences between the control and SA patients (p/=/0.046). Genes involved in double strand break repair and nucleotide excision repair pathways were differentially expressed in patients with SA and NSTEMI. In SA patients, fibrocalcific plaques were strongly associated with GTSE1, DDB1, MLH3 and ERCC1 expression. By contrast, in NSTEMI patients the strongest association was observed between fibrous plaques and ATM and XPA expression.
PBMCs from patients with CAD exhibit differences in DNA ligase activity and expression of DDR genes. Expression levels of certain DDR genes are strongly associated with plaque morphology and may play a role in plaque development and progression.
Healing, Eleanor, Charlier, Clara. F, Meira, Lisie and Elliott, Ruan (2019) A panel of colorimetric assays to measure enzymatic activity in the base excision DNA repair pathway Nucleic Acids Research, 47 (11), e61.
Leguisamo, NM, Gloria, HC, Kalil, AN, Martins, TV, Azambuja, DB, Meira, Lisiane and Saffi, J (2017) Base excision repair imbalance in colorectal cancer has prognostic value and modulates response to chemotherapy Oncotarget. pp. 1-16.
Totti, Styliani, Vernardis, SI, Meira, Lisiane, Pérez-Mancera, PA, Costello, E, Greenhalf, W, Palmer, D, Neoptolemos, J, Mantalaris, A and Velliou, Eirini (2017) Designing a bio-inspired bio-mimetic in vitro system for the optimisation of ex vivo studies of pancreatic cancer Drug Discovery Today, 22 (4). pp. 690-701.
Alasmael, N, Mohan, R, Meira, LB, Swales, KE and Plant, NJ (2015) Activation of the Farnesoid X-receptor in breast cancer cell lines results in cytotoxicity but not increased migration potential Cancer Letters.
Meira, LB, Calvo, JA, Shah, D, Klapacz, J, Moroski-Erkul, CA, Bronson, RT and Samson, LD (2014) Repair of endogenous DNA base lesions modulate lifespan in mice DNA REPAIR, 21. pp. 78-86.
Brignull, LM, Czimmerer, Z, Saidi, H, Daniel, B, Villela, I, Bartlett, NW, Johnston, SL, Meira, LB, Nagy, L and Nohturfft, A (2013) Reprogramming of lysosomal gene expression by interleukin-4 and Stat6 BMC GENOMICS, 14, ARTN 8.
Bordin, DL, Lima, M, Lenz, G, Saffi, J, Meira, LB, Mesange, P, Soares, DG, Larsen, AK, Escargueil, AE and Henriques, JAP (2013) DNA alkylation damage and autophagy induction MUTATION RESEARCH-REVIEWS IN MUTATION RESEARCH, 753 (2). pp. 91-99.
Polycarpou, E, Meira, LB, Carrington, S, Tyrrell, E, Modjtahedi, H and Carew, MA (2013) Resveratrol 3-O-D-glucuronide and resveratrol 4 '-O-D-glucuronide inhibit colon cancer cell growth: Evidence for a role of A3 adenosine receptors, cyclin D1 depletion, and G1 cell cycle arrest MOLECULAR NUTRITION & FOOD RESEARCH, 57 (10). pp. 1708-1717.
Calvo, JA, Moroski-Erkul, CA, Lake, A, Eichinger, LW, Shah, D, Jhun, I, Limsirichai, P, Bronson, RT, Christiani, DC, Meira, LB and Samson, LD (2013) Aag DNA Glycosylase Promotes Alkylation-Induced Tissue Damage Mediated by Parp1 PLOS GENETICS, 9 (4), ARTN e.
Barazzuol, L, Jena, R, Burnet, NG, Meira, LB, Jeynes, JC, Kirkby, KJ and Kirkby, NF (2013) Evaluation of poly (ADP-ribose) polymerase inhibitor ABT-888 combined with radiotherapy and temozolomide in glioblastoma. Radiat Oncol, 8.
Calvo, JA, Meira, LB, Lee, CY, Moroski-Erkul, CA, Abolhassani, N, Taghizadeh, K, Eichinger, LW, Muthupalani, S, Nordstrand, LM, Klungland, A and Samson, LD (2012) DNA repair is indispensable for survival after acute inflammation. The Journal of Clinical Investigation, 122 (7). pp. 2680-2689.
Villela, I, Heidenreich, B, Cheema, M, di Martino, T, Samson, LD and Meira, LB (2011) Dissecting the mechanism of DNA damage induced photoreceptor cell death TOXICOLOGY, 290 (2-3). p. 143.
Kisby, GE, Fry, RC, Lasarev, MR, Bammler, TK, Beyer, RP, Churchwell, M, Doerge, DR, Meira, LB, Palmer, VS, Ramos-Crawford, A-L, Ren, X, Sullivan, RC, Kavanagh, TJ, Samson, LD, Zarbl, H and Spencer, PS (2011) The Cycad Genotoxin MAM Modulates Brain Cellular Pathways Involved in Neurodegenerative Disease and Cancer in a DNA Damage-Linked Manner PLOS ONE, 6 (6), ARTN e.
Unnikrishnan, A, Raffoul, JJ, Patel, HV, Prychitko, TM, Anyangwe, N, Meira, LB, Friedberg, EC, Cabelof, DC and Heydari, AR (2009) Oxidative stress alters base excision repair pathway and increases apoptotic response in apurinic/apyrimidinic endonuclease 1/redox factor-1 haploinsufficient mice FREE RADICAL BIOLOGY AND MEDICINE, 46 (11). pp. 1488-1499.
Bugni, JM, Meira, LB and Samson, LD (2009) Alkylation-induced colon tumorigenesis in mice deficient in the Mgmt and Msh6 proteins ONCOGENE, 28 (5). pp. 734-741.
Meira, LB, Moroski-Erkul, CA, Green, SL, Calvo, JA, Bronson, RT, Shah, D and Samson, LD (2009) Aag-initiated base excision repair drives alkylation-induced retinal degeneration in mice. Proc Natl Acad Sci U S A, 106 (3). pp. 888-893.
Klapacz, J, Meira, LB, Luchetti, DG, Calvo, JA, Bronson, RT, Edelmann, W and Samson, LD (2009) O-6-methylguanine-induced cell death involves exonuclease 1 as well as DNA mismatch recognition in vivo PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 106 (2). pp. 576-581.
Maor-Shoshani, A, Meira, LB, Yang, X and Samson, LD (2008) 3-methyladenine DNA glycosylase ill important for cellular resistance to psoralen interstrand cross-links DNA REPAIR, 7 (8). pp. 1399-1406.
Meira, LB, Bugni, JM, Green, SL, Lee, C-W, Pang, B, Borenshtein, D, Rickman, BH, Rogers, AB, Moroski-Erkul, CA, McFaline, JL, Schauer, DB, Dedon, PC, Fox, JG and Samson, LD (2008) DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice JOURNAL OF CLINICAL INVESTIGATION, 118 (7). pp. 2516-2525.
Ringvoll, J, Moen, MN, Nordstrand, LM, Meira, LB, Pang, B, Bekkelund, A, Dedon, PC, Bjelland, S, Samson, LD, Falnes, PO and Klungland, A (2008) AlkB homologue 2-mediated repair of ethenoadenine lesions in mammalian DNA CANCER RESEARCH, 68 (11). pp. 4142-4149.
Lingaraju, GM, Kartalou, M, Meira, LB and Samson, LD (2008) Substrate specificity and sequence-dependent activity of the Saccharomyces cerevisiae 3-methyladenine DNA glycosylase (Mag) DNA REPAIR, 7 (6). pp. 970-982.
Dong, L, Meira, LB, Hazra, TK, Samson, LD and Cao, W (2008) Oxanine DNA glycosylase activities in mammalian systems DNA REPAIR, 7 (1). pp. 128-134.
Longerich, S, Meira, L, Shah, D, Samson, LD and Storb, U (2007) Alkyladenine DNA glycosylase (Aag) in somatic hypermutation and class switch recombination DNA REPAIR, 6 (12). pp. 1764-1773.
Beyer, RP, Fry, RC, Lasarev, MR, McConnachie, LA, Meira, LB, Palmer, VS, Powell, CL, Ross, PK, Bammler, TK, Bradford, BU, Cranson, AB, Cunningham, ML, Fannin, RD, Higgins, GM, Hurban, P, Kayton, RJ, Kerr, KF, Kosyk, O, Lobenhofer, EK, Sieber, SO, Vliet, PA, Weis, BK, Wolfinger, R, Woods, CG, Freedman, JH, Linney, E, Kaufmann, WK, Kavanagh, TJ, Paules, RS, Rusyn, I, Samson, LD, Spencer, PS, Suk, W, Tennant, RJ and Zarbl, H (2007) Multicenter study of acetaminophen hepatotoxicity reveals the importance of biological endpoints in genomic analyses TOXICOLOGICAL SCIENCES, 99 (1). pp. 326-337.
Lee, CW, Rickman, B, Meira, LB, Samson, L and Fox, JG (2007) Base excision repair genes alkyl adenine DNA glycosylase (Aag) and O6-methylguanine DNA methyltransferase (Mgmt) suppresses Helicobacter pylori-associated inflammation and progression to cancer GASTROENTEROLOGY, 132 (4). A319-A319.
Friedberg, EC and Meira, LB (2006) Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7 DNA REPAIR, 5 (2). pp. 189-209.
Meira, LB, Burgis, NE and Samson, LD (2005) Base excision repair pp. 125-173.
Friedberg, EC and Meira, LB (2004) Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage (Version 6) DNA REPAIR, 3 (12). pp. 1617-1638.
Hitchcock, TM, Dong, L, Connor, EE, Meira, LB, Samson, LD, Wyatt, MD and Cao, WG (2004) Oxanine DNA glycosylase activity from mammalian alkyladenine glycosylase JOURNAL OF BIOLOGICAL CHEMISTRY, 279 (37). pp. 38177-38183.
Raffoul, JJ, Cabelof, DC, Nakamura, J, Meira, LB, Friedberg, EC and Heydari, AR (2004) Apurinic/apyrimidinic endonuclease (APE/REF-1) haploinsufficient mice display tissue-specific differences in DNA polymerase beta-dependent base excision repair JOURNAL OF BIOLOGICAL CHEMISTRY, 279 (18). pp. 18425-18433.
Ham, AJL, Engelward, BP, Koc, H, Sangaiah, R, Meira, LB, Samson, LD and Swenberg, JA (2004) New immunoaffinity-LC-MS/MS methodology reveals that Aag null mice are deficient in their ability to clear 1,N-6-etheno-deoxyadenosine DNA lesions from lung and liver in vivo DNA REPAIR, 3 (3). pp. 257-265.
Friedberg, EC and Meira, LB (2003) Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 5 DNA REPAIR, 2 (5). pp. 501-530.
Meira, LB, Cheo, DL, Reis, AM, Chaij, N, Burns, DK, te Riele, H and Friedberg, EC (2002) Mice defective in the mismatch repair gene Msh2 show increased predisposition to UVB radiation-induced skin cancer (vol 1, pg 929, 2002) DNA REPAIR, 1 (12), PII S1568-. p. 1063.
Meira, LB, Cheo, DL, Reis, AM, Claij, N, Burns, DK, Riele, HT and Friedberg, EC (2002) Mice defective in the mismatch repair gene Msh2 show increased predisposition to UVB radiation-induced skin cancer DNA REPAIR, 1 (11), PII S1568-. pp. 929-934.
Meira, LB, Devaraj, S, Kisby, GE, Burns, DK, Daniel, RL, Hammer, RE, Grundy, S, Jialal, I and Friedberg, EC (2001) Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress CANCER RESEARCH, 61 (14). pp. 5552-5557.
Meira, LB, Reis, AMC, Cheo, DL, Nahari, D, Burns, DK and Friedberg, EC (2001) Cancer predisposition in mutant mice defective in multiple genetic pathways: uncovering important genetic interactions MUTATION RESEARCH-FUNDAMENTAL AND MOLECULAR MECHANISMS OF MUTAGENESIS, 477 (1-2). pp. 51-58.
Friedberg, EC and Meira, LB (2000) Database of mouse strains carrying targeted mutations in genes affecting cellular responses to DNA damage. Version 4 MUTATION RESEARCH-DNA REPAIR, 459 (4). pp. 243-274.
Meira, LB, Graham, JM, Greenberg, CR, Busch, DB, Doughty, ATB, Ziffer, DW, Coleman, DM, Savre-Train, I and Friedberg, EC (2000) Manitoba aboriginal kindred with original cerebro-oculo-facio-skeletal syndrome has a mutation in the Cockayne syndrome group B (CSB) gene AMERICAN JOURNAL OF HUMAN GENETICS, 66 (4). pp. 1221-1228.
Graham, JM, Meira, LB, Greenberg, CR, Busch, DB, Doughty, ATB, Ziffer, DW, Coleman, DM, Savre-Train, I and Friedberg, EC (2000) Original COFS syndrome Manitoba Aboriginal kindred has a mutation in the Cockayne syndrome group B (CSB) gene PEDIATRIC RESEARCH, 47 (4). 81A-81A.
Friedberg, EC, Bond, JP, Burns, DK, Cheo, DL, Greenblatt, MS, Meira, LB, Nahari, D and Reis, AM (2000) Defective nucleotide excision repair in Xpc mutant mice and its association with cancer predisposition MUTATION RESEARCH-DNA REPAIR, 459 (2). pp. 99-108.
Reis, AM, Cheo, DL, Meira, LB, Greenblatt, MS, Bond, JP, Nahari, D and Friedberg, EC (2000) Genotype-specific Trp53 mutational analysis in ultraviolet B radiation-induced skin cancers in Xpc and Xpc Trp53 mutant mice CANCER RESEARCH, 60 (6). pp. 1571-1579.
Cheo, DL, Meira, LB, Burns, DK, Reis, AM, Issac, T and Friedberg, EC (2000) Ultraviolet B radiation-induced skin cancer in mice defective in the Xpc, Trp53, and Apex (HAP1) genes: Genotype-specific effects on cancer predisposition and pathology of tumors CANCER RESEARCH, 60 (6). pp. 1580-1584.
Graham, JM, Meira, LB, Greenberg, CR, Busch, D and Friedberg, EC (2000) Original COFS syndrome kindred from Manitoba has a mutation in the cockayne syndrome group B (CSB) gene. JOURNAL OF INVESTIGATIVE MEDICINE, 48 (1). 48A-48A.
Graham, JM, Meira, LB, Greenberg, CR, Jaspers, NGJ, Busch, D, Coleman, DM, Ziffer, DW and Friedberg, EC (1999) Original COFS syndrome Manitoba Aboriginal kindred has a mutation in the Cockayne syndrome group B (CSB) gene. AMERICAN JOURNAL OF HUMAN GENETICS, 65 (4). A299-A299.
Friedberg, EC and Meira, LB (1999) Database of mouse strains carrying targeted mutations in genes affecting cellular responses to DNA damage: version 3 MUTATION RESEARCH-DNA REPAIR, 433 (2). pp. 69-87.
Cheo, DL, Burns, DK, Meira, LB, Houle, JF and Friedberg, EC (1999) Mutational inactivation of the xeroderma pigmentosum group C gene confers predisposition to 2-acetylaminofluorene-induced liver and lung cancer and to spontaneous testicular cancer in Trp53(-/-) mice CANCER RESEARCH, 59 (4). pp. 771-775.
Friedberg, EC, Meira, LB and Cheo, DL (1998) Database of mouse strains carrying targeted mutations in genes affecting cellular responses to DNA damage. Version 2 MUTATION RESEARCH-DNA REPAIR, 407 (3). pp. 217-226.
Meira, LB, Cheo, DL, Hammer, RE, Burns, DK, Reis, A and Friedberg, EC (1997) Genetic interaction between HAP1/REF-1 and p53 NATURE GENETICS, 17 (2). p. 145.
Friedberg, EC, Meira, LB and Cheo, DL (1997) Database of mouse strains carrying targeted mutations in genes affecting cellular responses to DNA damage MUTATION RESEARCH-DNA REPAIR, 383 (2). pp. 183-188.
Cheo, DL, Ruven, HJT, Meira, LB, Hammer, RE, Burns, DK, Tappe, NJ, vanZeeland, AA, Mullenders, LHF and Friedberg, EC (1997) Characterization of defective nucleotide excision repair in XPC mutant mice MUTATION RESEARCH-FUNDAMENTAL AND MOLECULAR MECHANISMS OF MUTAGENESIS, 374 (1). pp. 1-9.
Cheo, DL, Meira, LB, Hammer, RE, Burns, DK, Doughty, ATB and Friedberg, EC (1996) Synergistic interactions between XPC and p53 mutations in double-mutant mice: Neural tube abnormalities and accelerated UV radiation-induced skin cancer CURRENT BIOLOGY, 6 (12). pp. 1691-1694.