ZFIN ID: ZDB-LAB-050519-2
Charles Lee's Molecular Cytogenetic Research Lab
PI/Director: Lee, Charles
Contact Person: Hislop, Shona
Email: shislop@partners.org
URL: http://www.chromosome.bwh.harvard.edu
Address: Department of Pathology Brigham and Women's Hospital Harvard Medical School 20 Shattuck Street Thorn Building, Room 6-12A Boston, MA 02115 USA
Country: United States
Phone: 617.732.5790
Fax: 617.264.5169
Line Designation: None assigned



Casavant, Dave Post-Doc Cho, Eun Kyung Post-Doc Freeman, Jennifer Post-Doc
Kantarci, Sibel Post-Doc Ouahchi, Karim Post-Doc Tchinda, Joelle Post-Doc
Aggarwal, Abha Technical Staff Dallaire, Stephanie Technical Staff Hyland, Courtney Technical Staff
Listewnik, Marc Technical Staff Smith, Amanda Technical Staff Hislop, Shona Administrative Staff

Arjun, P., Freeman, J.L., Kannan, R.R. (2022) Neurospecific fabrication and toxicity assessment of a PNIPAM nanogel encapsulated with trans-tephrostachin for blood-brain-barrier permeability in zebrafish model. Heliyon. 8:e10237
Wang, S., Bryan, C., Xie, J., Zhao, H., Lin, L., Tai, J.A.C., Horzmann, K.A., Sanchez, O., Zhang, M., Freeman, J.L., Yuan, C. (2022) Atrazine exposure in zebrafish induces aberrant genome-wide methylation. Neurotoxicology and teratology. 92:107091
Ahkin Chin Tai, J.K., Horzmann, K.A., Franco, J., Jannasch, A.S., Cooper, B.R., Freeman, J.L. (2021) Developmental atrazine exposure in zebrafish produces the same major metabolites as mammals along with altered behavioral outcomes. Neurotoxicology and teratology. 85:106971
Wasel, O., Thompson, K.M., Gao, Y., Godfrey, A.E., Gao, J., Mahapatra, C.T., Lee, L.S., Sepúlveda, M.S., Freeman, J.L. (2020) Comparison of zebrafish in vitro and in vivo developmental toxicity assessments of perfluoroalkyl acids (PFAAs). Journal of toxicology and environmental health. Part A. 84(3):125-136
Wasel, O., Freeman, J.L. (2020) Chemical and Genetic Zebrafish Models to Define Mechanisms of and Treatments for Dopaminergic Neurodegeneration. International Journal of Molecular Sciences. 21(17)
Horzmann, K.A., Lin, L.F., Taslakjian, B., Yuan, C., Freeman, J.L. (2020) Embryonic atrazine exposure and later in life behavioral and brain transcriptomic, epigenetic, and pathological alterations in adult male zebrafish. Cell biology and toxicology. 37(3):421-439
Lee, J., Freeman, J.L. (2020) Exposure to the heavy metal lead induces DNA copy number alterations in zebrafish cells. Chemical Research in Toxicology. 33(8):2047-2053
Ahkin Chin Tai, J.K., Freeman, J.L. (2020) Zebrafish as an integrative vertebrate model to identify miRNA mechanisms regulating toxicity. Toxicology reports. 7:559-570
Zhang, R., Silic, M.R., Schaber, A., Wasel, O., Freeman, J.L., Sepúlveda, M.S. (2020) Exposure route affects the distribution and toxicity of polystyrene nanoplastics in zebrafish. The Science of the total environment. 724:138065
Horzmann, K.A., Portales, A.M., Batcho, K.G., Freeman, J.L. (2020) Developmental toxicity of trichloroethylene in zebrafish (Danio rerio). Environmental science. Processes & impacts. 22(3):728-739
Cassar, S., Adatto, I., Freeman, J.L., Gamse, J.T., Iturria, I., Lawrence, C., Muriana, A., Peterson, R., Van Cruchten, S., Zon, L. (2019) Use of Zebrafish in Drug Discovery Toxicology. Chemical Research in Toxicology. 33(1):95-118
Pitchai, A., Rajaretinam, R.K., Freeman, J.L. (2019) Zebrafish as an Emerging Model for Bioassay-Guided Natural Product Drug Discovery for Neurological Disorders. Medicines (Basel, Switzerland). 6(2)
Horzmann, K.A., Reidenbach, L.S., Thanki, D.H., Winchester, A.E., Qualizza, B.A., Ryan, G.A., Egan, K.E., Hedrick, V.E., Sobreira, T.J.P., Peterson, S.M., Weber, G.J., Wirbisky-Hershberger, S.E., Sepúlveda, M.S., Freeman, J.L. (2018) Embryonic atrazine exposure elicits proteomic, behavioral, and brain abnormalities with developmental time specific gene expression signatures. Journal of proteomics. 186:71-82
Caballero-Gallardo, K., Wirbisky-Hershberger, S.E., Olivero-Verbel, J., de la Rosa, J., Freeman, J.L. (2018) Embryonic exposure to an aqueous coal dust extract results in gene expression alterations associated with the development and function of connective tissue and the hematological system, immunological and inflammatory disease, and cancer in zebrafish. Metallomics : integrated biometal science. 10(3):463-473
Horzmann, K.A., Freeman, J.L. (2018) Making Waves: New Developments in Toxicology with the Zebrafish. Toxicological sciences : an official journal of the Society of Toxicology. 163(1):5-12
Zhou, W., Pal, A.S., Hsu, A.Y., Gurol, T., Zhu, X., Wirbisky-Hershberger, S.E., Freeman, J.L., Kasinski, A.L., Deng, Q. (2018) MicroRNA-223 Suppresses the Canonical NF-κB Pathway in Basal Keratinocytes to Dampen Neutrophilic Inflammation. Cell Reports. 22:1810-1823
Lee, J., Horzmann, K.A., Freeman, J.L. (2018) An embryonic 100μg/L lead exposure results in sex-specific expression changes in genes associated with the neurological system in female or cancer in male adult zebrafish brains. Neurotoxicology and teratology. 65:60-69
Horzmann, K.A., de Perre, C., Lee, L.S., Whelton, A.J., Freeman, J.L. (2017) Comparative analytical and toxicological assessment of methylcyclohexanemethanol (MCHM) mixtures associated with the Elk River chemical spill. Chemosphere. 188:599-607
Wirbisky-Hershberger, S.E., Sanchez, O.F., Horzmann, K.A., Thanki, D., Yuan, C., Freeman, J.L. (2017) Atrazine exposure decreases the activity of DNMTs, global DNA methylation levels, and dnmt expression. Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association. 109(Pt 1):727-734
Damayanti, N.P., Buno, K., Cui, Y., Voytik-Harbin, S.L., Pili, R., Freeman, J., Irudayaraj, J.M.K. (2017) Real-Time Multiplex Kinase Phosphorylation Sensors in Living Cells. ACS sensors. 2:1225-1230
Elsayed, M.S.A., Su, Y., Wang, P., Sethi, T., Agama, K., Ravji, A., Redon, C.E., Kiselev, E., Horzmann, K.A., Freeman, J.L., Pommier, Y., Cushman, M. (2017) Design and Synthesis of Chlorinated and Fluorinated 7-Azaindenoisoquinolines as Potent Cytotoxic Anticancer Agents That Inhibit Topoisomerase I. Journal of medicinal chemistry. 60:5364-5376
Lee, J., Peterson, S.M., Freeman, J.L. (2017) Sex-specific characterization and evaluation of the Alzheimer's disease genetic risk factor sorl1 in zebrafish during aging and in the adult brain following a 100 ppb embryonic lead exposure. Journal of applied toxicology : JAT. 37(4):400-407
Wirbisky, S.E., Freeman, J.L. (2017) Atrazine Exposure Elicits Copy Number Alterations in the Zebrafish Genome. Comparative biochemistry and physiology. Toxicology & pharmacology : CBP. 194:1-8
Sanchez, O.F., Lee, J., Yu King Hing, N., Kim, S.E., Freeman, J.L., Yuan, C. (2017) Lead (Pb) exposure reduces global DNA methylation level by non-competitive inhibition and alteration of dnmt expression. Metallomics : integrated biometal science. 9(2):149-160
Caballero-Gallardo, K., Olivero-Verbel, J., Freeman, J.L. (2016) Toxicogenomics to Evaluate Endocrine Disrupting Effects of Environmental Chemicals Using the Zebrafish Model. Current genomics. 17:515-527
Wirbisky, S.E., Weber, G.J., Schlotman, K.E., Sepúlveda, M.S., Freeman, J.L. (2016) Embryonic atrazine exposure alters zebrafish and human miRNAs associated with angiogenesis, cancer, and neurodevelopment. Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association. 98(Pt A):25-33
Horzmann, K.A., Freeman, J.L. (2016) Zebrafish Get Connected: Investigating Neurotransmission Targets and Alterations in Chemical Toxicity. Toxics. 4(3)
Wirbisky, S.E., Sepúlveda, M.S., Weber, G.J., Jannasch, A.S., Horzmann, K.A., Freeman, J.L. (2016) Embryonic atrazine exposure elicits alterations in genes associated with neuroendocrine function in adult male zebrafish. Toxicological sciences : an official journal of the Society of Toxicology. 153(1):149-64
Lee, J., Peterson, S.M., Freeman, J.L. (2016) Alzheimer's disease risk genes in wild-type adult zebrafish exhibit gender-specific expression changes during aging. Neurogenetics. 17(3):197-9
Lee, J., Freeman, J.L. (2016) Embryonic exposure to 10 μg L(-1) lead results in female-specific expression changes in genes associated with nervous system development and function and Alzheimer's disease in aged adult zebrafish brain. Metallomics : integrated biometal science. 8(6):589-96
Wirbisky, S.E., Weber, G.J., Sepúlveda, M.S., Lin, T.L., Jannasch, A.S., Freeman, J.L. (2016) An embryonic atrazine exposure results in reproductive dysfunction in adult zebrafish and morphological alterations in their offspring. Scientific Reports. 6:21337
Wirbisky, S.E., Damayanti, N.P., Mahapatra, C.T., Sepulveda, M.S., Irudayaraj, J., Freeman, J.L. (2016) Mitochondrial Dysfunction, Disruption of F-actin Polymerization, and Transcriptomic Alterations in Zebrafish Larvae Exposed to Trichloroethylene. Chemical Research in Toxicology. 29(2):169-79
Bault, Z.A., Peterson, S.M., Freeman, J.L. (2015) Directional and color preference in adult zebrafish: Implications in behavioral and learning assays in neurotoxicology studies. Journal of applied toxicology : JAT. 35(12):1502-10
Bishop, B., Ho, K.K., Tyler, K., Smith, A., Bonilla, S., Leung, Y.F., Ogas, J. (2015) The chromatin remodeler chd5 is necessary for proper head development during embryogenesis of Danio rerio. Biochimica et biophysica acta. Gene regulatory mechanisms. 1849(8):1040-50
Wirbisky, S.E., Weber, G.J., Sepúlveda, M.S., Xiao, C., Cannon, J.R., Freeman, J.L. (2015) Developmental origins of neurotransmitter and transcriptome alterations in adult female zebrafish exposed to atrazine during embryogenesis. Toxicology. 333:156-67
Wirbisky, S.E., Weber, G.J., Lee, J.W., Cannon, J.R., Freeman, J.L. (2014) Novel dose-dependent alterations in excitatory GABA during embryonic development associated with lead (Pb) neurotoxicity. Toxicology letters. 229(1):1-8
Freeman, J.L., Weber, G.J., Peterson, S.M., Nie, L.H. (2014) Embryonic ionizing radiation exposure results in expression alterations of genes associated with cardiovascular and neurological development, function, and disease and modified cardiovascular function in zebrafish. Frontiers in genetics. 5:268
Lee, J., Freeman, J.L. (2014) Zebrafish as a model for investigating developmental lead (Pb) neurotoxicity as a risk factor in adult neurodegenerative disease: A mini-review. Neurotoxicology. 43:57-64
Blackburn, J.S., Liu, S., Wilder, J.L., Dobrinski, K.P., Lobbardi, R., Moore, F.E., Martinez, S.A., Chen, E.Y., Lee, C., Langenau, D.M. (2014) Clonal evolution enhances leukemia-propagating cell frequency in T cell acute lymphoblastic leukemia through Akt/mTORC1 pathway activation. Cancer Cell. 25:366-78
Chen, E.Y., Dobrinski, K.P., Brown, K.H., Clagg, R., Edelman, E., Ignatius, M.S., Chen, J.Y., Brockmann, J., Nielsen, G.P., Ramaswamy, S., Keller, C., Lee, C., and Langenau, D.M. (2013) Cross-species array comparative genomic hybridization identifies novel oncogenic events in zebrafish and human embryonal rhabdomyosarcoma. PLoS Genetics. 9(8):e1003727
Peterson, S.M., Zhang, J., and Freeman, J.L. (2013) Developmental reelin expression and time point-specific alterations from lead exposure in zebrafish. Neurotoxicology and teratology. 38C:53-60
Howe, K., Clark, M.D., Torroja, C.F., Torrance, J., Berthelot, C., Muffato, M., Collins, J.E., Humphray, S., McLaren, K., Matthews, L., McLaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J.C., Koch, R., Rauch, G.J., White, S., Chow, W., Kilian, B., Quintais, L.T., Guerra-Assunção, J.A., Zhou, Y., Gu, Y., Yen, J., Vogel, J.H., Eyre, T., Redmond, S., Banerjee, R., Chi, J., Fu, B., Langley, E., Maguire, S.F., Laird, G.K., Lloyd, D., Kenyon, E., Donaldson, S., Sehra, H., Almeida-King, J., Loveland, J., Trevanion, S., Jones, M., Quail, M., Willey, D., Hunt, A., Burton, J., Sims, S., McLay, K., Plumb, B., Davis, J., Clee, C., Oliver, K., Clark, R., Riddle, C., Eliott, D., Threadgold, G., Harden, G., Ware, D., Mortimer, B., Kerry, G., Heath, P., Phillimore, B., Tracey, A., Corby, N., Dunn, M., Johnson, C., Wood, J., Clark, S., Pelan, S., Griffiths, G., Smith, M., Glithero, R., Howden, P., Barker, N., Stevens, C., Harley, J., Holt, K., Panagiotidis, G., Lovell, J., Beasley, H., Henderson, C., Gordon, D., Auger, K., Wright, D., Collins, J., Raisen, C., Dyer, L., Leung, K., Robertson, L., Ambridge, K., Leongamornlert, D., McGuire, S., Gilderthorp, R., Griffiths, C., Manthravadi, D., Nichol, S., Barker, G., Whitehead, S., Kay, M., Brown, J., Murnane, C., Gray, E., Humphries, M., Sycamore, N., Barker, D., Saunders, D., Wallis, J., Babbage, A., Hammond, S., Mashreghi-Mohammadi, M., Barr, L., Martin, S., Wray, P., Ellington, A., Matthews, N., Ellwood, M., Woodmansey, R., Clark, G., Cooper, J., Tromans, A., Grafham, D., Skuce, C., Pandian, R., Andrews, R., Harrison, E., Kimberley, A., Garnett, J., Fosker, N., Hall, R., Garner, P., Kelly, D., Bird, C., Palmer, S., Gehring, I., Berger, A., Dooley, C.M., Ersan-Ürün, Z., Eser, C., Geiger, H., Geisler, M., Karotki, L., Kirn, A., Konantz, J., Konantz, M., Oberländer, M., Rudolph-Geiger, S., Teucke, M., Osoegawa, K., Zhu, B., Rapp, A., Widaa, S., Langford, C., Yang, F., Carter, N.P., Harrow, J., Ning, Z., Herrero, J., Searle, S.M., Enright, A., Geisler, R., Plasterk, R.H., Lee, C., Westerfield, M., de Jong, P.J., Zon, L.I., Postlethwait, J.H., Nüsslein-Volhard, C., Hubbard, T.J., Crollius, H.R., Rogers, J., and Stemple, D.L. (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature. 496:498-503
Weber, G.J., Sepulveda, M.S., Peterson, S.M., Lewis, S.S., and Freeman, J.L. (2013) Transcriptome alterations following developmental atrazine exposure in zebrafish are associated with disruption of neuroendocrine and reproductive system function, cell cycle, and carcinogenesis. Toxicological sciences : an official journal of the Society of Toxicology. 132(2):458-466
Brown, K.H., Dobrinski, K.P., Lee, A.S., Gokcumen, O., Mills, R.E., Shi, X., Chong, W.W., Chen, J.Y., Yoo, P., David, S., Peterson, S.M., Raj, T., Choy, K.W., Stranger, B.E., Williamson, R.E., Zon, L.I., Freeman, J.L., and Lee, C. (2012) Extensive genetic diversity and substructuring among zebrafish strains revealed through copy number variant analysis. Proceedings of the National Academy of Sciences of the United States of America. 109(2):529-34
Frazer, J.K., Batchelor, L.A., Bradley, D.F., Brown, K.H., Dobrinski, K.P., Lee, C., and Trede, N.S. (2012) Genomic Amplification of an Endogenous Retrovirus in Zebrafish T-Cell Malignancies. Advances in hematology. 2012:627920
Zhang, J., Peterson, S.M., Weber, G.J., Zhu, X., Zheng, W., and Freeman, J.L. (2011) Decreased axonal density and altered expression profiles of axonal guidance genes underlying lead (Pb) neurodevelopmental toxicity at early embryonic stages in the zebrafish. Neurotoxicology and teratology. 33(6):715-20
Peterson, S.M., Zhang, J., Weber, G., and Freeman, J.L. (2011) Global Gene Expression Analysis Reveals Dynamic and Developmental Stage Dependent Enrichment of Lead (Pb)-Induced Neurological Gene Alterations. Environmental health perspectives. 119(5):615-622
Dobrinski, K.P., Brown, K.H., Freeman, J.L., and Lee, C. (2011) Molecular Cytogenetic Methodologies and a BAC Probe Panel Resource for Genomic Analyses in the Zebrafish. Methods in cell biology. 104:237-257
Peterson, S.M., and Freeman, J.L. (2009) Cancer Cytogenetics in the Zebrafish. Zebrafish. 6(4):355-360
Rhodes, J., Amsterdam, A., Sanda, T., Moreau, L.A., McKenna, K., Heinrichs, S., Ganem, N.J., Ho, K.W., Neuberg, D.S., Johnston, A., Ahn, Y., Kutok, J.L., Hromas, R., Wray, J., Lee, C., Murphy, C., Radke, I., Downing, J.R., Fleming, M.D., Macconaill, L.E., Amatruda, J.F., Gutierrez, A., Galinsky, I., Stone, R.M., Ross, E.A., Pellman, D.S., Kanki, J.P., and Look, A.T. (2009) Emi1 Maintains Genomic Integrity during Zebrafish Embryogenesis and Cooperates with p53 in Tumor Suppression. Molecular and cellular biology. 29(21):5911-5922
Peterson, S.M., and Freeman, J.L. (2009) Global gene expression analysis using a zebrafish oligonucleotide microarray platform. Journal of visualized experiments : JoVE. (30)
Peterson, S.M., and Freeman, J.L. (2009) RNA isolation from embryonic zebrafish and cDNA synthesis for gene expression analysis. Journal of visualized experiments : JoVE. (30)
Freeman, J.L., Ceol, C., Feng, H., Langenau, D.M., Belair, C., Stern, H.M., Song, A., Paw, B.H., Look, A.T., Zhou, Y., Zon, L.I., and Lee, C. (2009) Construction and application of a zebrafish array comparative genomic hybridization platform. Genes, chromosomes & cancer. 48(2):155-170
Langenau, D.M., Keefe, M.D., Storer, N.Y., Jette, C.A., Smith, A.C., Ceol, C.J., Bourque, C., Look, A.T., and Zon, L.I. (2008) Co-injection strategies to modify radiation sensitivity and tumor initiation in transgenic Zebrafish. Oncogene. 27(30):4242-4248
Yoder, J.A., Cannon, J.P., Litman, R.T., Murphy, C., Freeman, J.L., and Litman, G.W. (2008) Evidence for a transposition event in a second NITR gene cluster in zebrafish. Immunogenetics. 60(5):257-265
Freeman, J.L., Adeniyi, A., Banerjee, R., Dallaire, S., Maguire, S.F., Chi, J., Ng, B.L., Zepeda, C., Scott, C.E., Humphray, S., Rogers, J., Zhou, Y., Zon, L.I., Carter, N.P., Yang, F., and Lee, C. (2007) Definition of the zebrafish genome using flow cytometry and cytogenetic mapping. BMC Genomics. 8(1):195
Shepard, J.L., Amatruda, J.F., Finkelstein, D., Ziai, J., Finley, K.R., Stern, H.M., Chiang, K., Hersey, C., Barut, B., Freeman, J.L., Lee, C., Glickman, J.N., Kutok, J.L., Aster, J.C., and Zon, L.I. (2007) A mutation in separase causes genome instability and increased susceptibility to epithelial cancer. Genes & Development. 21(1):55-59
Shepard, J.L., Amatruda, J.F., Stern, H.M., Subramanian, A., Finkelstein, D., Ziai, J., Finley, K.R., Pfaff, K.L., Hersey, C., Zhou, Y., Barut, B., Freedman, M., Lee, C., Spitsbergen, J., Neuberg, D., Weber, G., Golub, T.R., Glickman, J.N., Kutok, J.L., Aster, J.C., and Zon, L.I. (2005) A zebrafish bmyb mutation causes genome instability and increased cancer susceptibility. Proceedings of the National Academy of Sciences of the United States of America. 102(37):13194-13199
Patton, E.E., Widlund, H.R., Kutok, J.L., Kopani, K.R., Amatruda, J.F., Murphey, R.D., Berghmans, S., Mayhall, E.A., Traver, D., Fletcher, C.D., Aster, J.C., Granter, S.R., Look, A.T., Lee, C., Fisher, D.E., and Zon, L.I. (2005) BRAF Mutations Are Sufficient to Promote Nevi Formation and Cooperate with p53 in the Genesis of Melanoma. Current biology : CB. 15(3):249-254
Poss, K.D., Nechiporuk, A., Stringer, K.F., Lee, C., and Keating, M.T. (2004) Germ cell aneuploidy in zebrafish with mutations in the mitotic checkpoint gene mps1. Genes & Development. 18(13):1527-1532
Paw, B.H., Davidson, A.J., Zhou, Y., Li, R., Pratt, S.J., Lee, C., Trede, N.S., Brownlie, A., Donovan, A., Liao, E.C., Ziai, J.M., Drejer, A.H., Guo, W., Kim, C.H., Gwynn, B., Peters, L.L., Chernova, M.N., Alper, S.L., Zapata, A., Wickramasinghe, S.N., Lee, M.J., Lux, S.E., Fritz, A., Postlethwait, J.H., and Zon, L.I. (2003) Cell-specific mitotic defect and dyserythropoiesis associated with erythroid band 3 deficiency. Nature Genetics. 34(1):59-64