Trace metals alter DNA repair and histone modification pathways concurrently in mouse embryonic stem cells

Toxicology Letters

Volumn 212, Issue 2, 2012, Pages 169-179

  Gadhia, Sanket R ^a   Calabro, Anthony R ^a   Barile, Frank A ^a  

^a ST JOHN'S UNIVERSITY   (United States)

Author keywords

Cytotoxicity; Embryonic stem cells; Epigenetic; Histone modification; Metals; Paracellular permeability

Indexed keywords

ARSENIC TRIOXIDE; CADMIUM CHLORIDE; COPPER SULFATE; HISTONE H3; HISTONE H3 LYSINE 27; LEAD ACETATE; LITHIUM SULFATE; MERCURIC CHLORIDE; NICKEL CHLORIDE; PROTEIN; PROTEIN OGG 1; PROTEIN TOP 3A; RAD18 PROTEIN; TRACE METAL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA REPAIR; EMBRYONIC STEM CELL; EXPOSURE; GENE EXPRESSION; GENOTOXICITY; HISTONE METHYLATION; HISTONE MODIFICATION; IC 50; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; DNA REPAIR; EMBRYONIC STEM CELLS; GENE EXPRESSION; HISTONES; METALS; METHYLATION; MICE;

EID: 84861971325     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.05.013     Document Type: Article

References (72)

1. Akbarian S., Huang H. Epigenetic Regulation in Human BrainFocus on histone lysine methylation. Biological Psychiatry 2009, 65:198-203.
2. Bailly V., Prakash S., Prakash L. Domains required for dimerization of yeast Rad6 ubiquitin-conjugating enzyme and Rad18 DNA binding protein. Molecular Cell Biology 1997, 17:4536-4543.
3. Bain G., Kitchens D., Yao M., Huettner J.E., Gottlieb D.I. Embryonic stem cells express neuronal properties in vitro. Developmental Biology 1995, 168:342-357.
4. Barnes D.E., Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annual Review of Genetics 2004, 38:445-476.
5. Berger S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447:407-412.
6. Berger S.L., Kouzarides T., Shiekhattar R., Shilatifard A. An operational definition of epigenetics. Genes and Development 2009, 23:781-783.
7. Beyersmann D. Effects of carcinogenic metals on gene expression. Toxicology Letters 2002, 127:63-68.
8. Borenfreund E., Puerner J.A. Cytotoxicity of metals, metal-metal and metal-chelator combinations assayed in vitro. Toxicology 1986, 39:14.
9. Broberg K., Huynh E., Engström K.S., Björk J., Albin M., Ingvar C., Olsson H., Höglund M. Association between polymorphisms in RMI1, TOP3A, and BLM and risk of cancer, a case-control study. BMC Cancer 2009, 9.
10. Calabro A.R., Gazarian D.I., Barile F.A. Effect of metals on [beta]-actin and total protein synthesis in cultured human intestinal epithelial cells. Journal of Pharmacological and Toxicological Methods 2011, 63:47-58.
11. Calabro A.R., Konsoula Z.R., Barile F.A. Evaluation of in vitro cytotoxicity and paracellular permeability of intact monolayers with mouse embryonic stem cells. Toxiology In vitro 2008, 22:1273-1284.
12. Cheng K.C., Cahill D.S., Kasai H., Nishimura S., Loeb L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and A→C substitutions. Journal of Biological Chemistry 1992, 267:166-172.
13. Collman G.W. Developmental basis of disease: environmental impacts. Journal of Developmental Origins of Health and Disease 2011, 2:49-55.
14. Cousins R.J., Liuzzi J.P., Lichten L.A. Mammalian zinc transport, trafficking, and signals. Journal of Biological Chemistry 2006, 281:24085-24089.
15. Denkhaus E., Salnikow K. Nickel essentiality, toxicity and carcinogenicity. Critical Reviews in Oncology/Hematology 2002, 42:21.
16. Drab M., Haller H., Bychkov R., Erdmann B., Lindschau C., Haase H., Morano I., Luft F., Wobus A. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: a retinoic acid and db-cAMP in vitro differentiation model. The FASEB Journal 1997, 11:905-915.
17. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154.
18. Feinberg A.P., Ohlsson R., Henikoff S. The epigenetic progenitor origin of human cancer. Nature Reviews Genetics 2006, 7.
19. Ferm V.H. Teratogenic effects and placental permeability of heavy metals. Current Topics in Pathology 1976, 62:145.
20. Fishbein L. Overview of analysis of carcinogenic and/or mutagenic metals in biological and environmental samples. I. Arsenic, berylium, cadmium, chromium and selenium. International Journal of Environmental Analytical Chemistry 1984, 17:113.
21. Furue M., Okamoto T., Hayashi Y., Okochi H., Fujimoto G., Myoishi Y., Abe K., Ohnuma T., Sato G.H., Asashima M., Sato J.D. Leukemia inhibitory factor as an antiapoptotic mitogen for pluripotent mouse embryonic stem cells in a serum-free medium without feeder cells. In Vitro Cell Developmental Biology: Animal 2005, 42:19-28.
22. Gidekel S., Pizov G., Bergman Y., Pikarsky E. Oct-3/4 is a dose-dependent oncogenic fate determinant. Cancer Cell 2003, 4:361-370.
23. Ginis I., Luo Y., Miura T., Thies S., Brandenberger R., Gerecht-Nir S., Amit M., Hoke A., Carpenter M.K., Itskovitz-Eldor J. Differences between human and mouse embryonic stem cells. Developmental Biology 2004, 269:360-380.
24. Goering P.L., Waalkes M.P., Klaassen C.D. Toxicology of Cadmium. Handbook of Experimental Pharmacology: Toxicology of Metals, Biochemical Effects 1994, vol. 115:189-214. Springer-Verlag, New York.
25. Gonzalez-Mariscal I., Betanzos A., Nava P., Jaramillo B.E. Tight junction proteins. Progress in Biophysics and Molecular Biology 2003, 81:1-44.
26. Gopalakrishnan S., Vanemburgh B., Robertson K. DNA methylation in development and human disease. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 2008, 647:30-38.
27. Gritti A., Frölichsthal-Schoeller P., Galli R., Parati E.A., Cova L., Pagano S.F., Bjornson C.R., Vescovi A.L. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. Journal of Neuroscience 1999, 19:3287-3297.
28. GrØNbÆK K., Hother C., Jones P.A. Epigenetic changes in cancer. APMIS 2007, 115:1039-1059.
29. Gupta G.P., Massagué J. Cancer Metastasis: Building a Framework. Cell 2006, 127:679-695.
30. Heindel J.J. The fetal basis of adult disease: role of environmental exposures - introduction. Birth Defects Research A: Clinical and Molecular Teratology 2005, 73:2.
31. Hemberger M., Dean W., Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nature Reviews Molecular Cell Biology 2009, 10:526-537.
32. Hemberger M., Pedersen R. Epigenome Disruptors Science 2010, 330:598-599.
33. Jablonka E., Lamb M.J. The changing concept of epigenetics. Annals of the New York Academy of Sciences 2002, 981:15-21.
34. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics Supplement 2003, 33:10.
35. Jimi S., Uchiyama M., Takaki A.Y.A., Suzumiya J., Hara S. Mechanisms of Cell Death Induced by Cadmium and Arsenic. Annals of the New York Academy of Sciences 2004, 1011:325-331.
36. Kanwal R., Gupta S. Epigenetics and cancer. Journal of Applied Physiology 2010, 109:598-605.
37. Kasprzak K.S. Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radical Biology and Medicine 2002, 32:958-967.
38. Kebache S., Zuo D., Chevet E., Larose L. Modulation of protein translation by Nck-1. Proceedings of the National Academy of Sciences 2002, 99:5406-5411.
39. Keller G. Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes and Development 2005, 19:1129-1155.
40. Klug M.G., Soonpaa M.H., Koh G.Y., Field L.J. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. The Journal of Clinical Investigation 1996, 98:216-224.
41. Klungland A., Bjelland S. Oxidative damage to purines in DNA: role of mammalian Ogg1. DNA Repair 2007, 6:481-488.
42. Konsoula R., Barile F.A. Correlation of in vitro cytotoxicity with paracellular permeability in mortal rat intestinal cells. Journal of Pharmacological and Toxicological Methods 2007, 55:176-183.
43. Konsoula Z.R., Barile F.A. Correlation of in vitro cytotoxicity with paracellular permeability in Caco-2 cells. Toxicology in Vitro 2005, 19:675-684.
44. Krueger K.E., Srivastava S. Posttranslational protein modifications. Molecular and Cellular Proteomics 2006, 5:1799-1810.
45. Liu J., Goyer R.A., Waalkes M.P. Toxic effects of metals. Cassarett and Doull's Toxicology: Basic Science of Poisons 2008, McGraw-Hill. C.D. Klaassen (Ed.).
46. Martin G.R., Wiley L.M., Damjanov I. The development of cystic embryoid bodies in vitro from clonal teratocarcinoma stem cells. Developmental Biology 1977, 61:230-244.
47. McDonald J.W., Liu X.-Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I., Choi D.W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Medicine 1999, 5:1410-1412.
48. Monk M., Holding C. Human embryonic genes re-expressed in cancer cells. Oncogene 2001, 20:7-15.
49. Mosmann T. Rapis colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 1983, 65:55-63.
50. Newnham J.P., Ross M.G. Developmental origins of health and disease: the importance of environmental exposures. Early Life Origins of Human Health and Disease 2009, 42-51. Basel. J.P. Newnham, M.G. Ross (Eds.).
51. Niwa H., Miyazaki J., Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 2000, 24:372-376.
52. Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metabolism Review 2007, 39:13.
53. Pesce M., Schöler H.R. Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 2001, 19:271-278.
54. Pesce M., Wang X., Wolgemuth D.J., Schöler H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mechanisms of Development 1998, 71:89-98.
55. Potocnik A.J., Kohler H., Eichmann K. Hemato-lymphoid in vivo reconstitution potential of subpopulations derived from in vitro differentiated embryonic stem cells. Proceedings of the National Academy of Sciences 1997, 94:10295-10300.
56. Rajasekhar V.K., Begemann M. Concise review: roles of polycomb group proteins in development and disease: a stem cell perspective. Stem Cells 2007, 25:2498-2510.
57. Rana S. Metals and apoptosis: recent developments. Journal of Trace Elements in Medicine and Biology 2008, 22:262-284.
58. Rea S., Eisenhaber F., O'Carroll D., Strahl B.D., Sun Z.-W., Schmid M., Opravil S., Mechtler K., Ponting C.P., Allis C.D., Jenuwein T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000, 406:593-599.
59. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
60. Rohwedel J., Maltsev V., Bober E., Arnold H.H., Hescheler J., Wobus A.M. Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Developmental Biology 1994, 164:87-101.
61. Rossman T. Mechanism of arsenic carcinogenesis: an integrated approach. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 2003, 533:37-65.
62. Salnikow K., Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis. Chemical and Research Toxicology 2008, 21:28-44.
63. Schmidt C.M., Cheng C.N., Marino A., Konsoula R., Barile F.A. Hormesis effect of trace metals on cultured normal and immortal human mammary cells. Toxicology and Industrial Health 2004, 20:57-157.
64. Silbergeld E.K., Waalkes M., Rice J.M. Lead as a carcinogen: experimental evidence and mechanisms of action. American Journal of Industrial Medicine 2000, 38:316-323.
65. Simon J., Lange C. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 2008, 647:21-29.
66. Smith A.G. Embryo-derived stem cells: of mice and men. Annual Review of Cell and Developmental Biology 2001, 17.
67. Smith M.M. Histone structure and function. Current Opinion in Cell Biology 1991, 3:9.
68. Völkel P., Angrand P.-O. The control of histone lysine methylation in epigenetic regulation. Biochimie 2007, 89:1-20.
69. Watanabe K., Iwabuchi K., Sun J., Tsuji Y., Tani T., Tokunaga K., Date T., Hashimoto M., Yamaizumi M., Tateishi S. RAD18 promotes DNA double-strand break repair during G1 phase through chromatin retention of 53BP1. Nucleic Acids Research 2009, 37:2176-2193.
70. Waterland R.A., Michels K.B. Epigenetic epidemiology of the developmental origins hypothesis. Annual Reviews of Nutrition 2007, 27:363-388.
71. Wiles M.V., Keller G. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 1991, 111:259-267.
72. Yu H., Zhu S., Zhou B., Xue H., Han J.D.J. Inferring causal relationships among different histone modifications and gene expression. Genome Research 2008, 18:1314-1324.