Prenatal zinc deficiency-dependent epigenetic alterations of mouse metallothionein-2 gene

Journal of Nutritional Biochemistry

Volumn 24, Issue 1, 2013, Pages 256-266

  Kurita, Hisaka ^a   Ohsako, Seiichiroh ^a   Hashimoto, Shin ichi ^a   Yoshinaga, Jun ^b   Tohyama, Chiharu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

DNA methylation; Epigenetics; Histone modification; Metallothionein; Zinc

Indexed keywords

CADMIUM; IMMUNOGLOBULIN M; METALLOTHIONEIN I; METALLOTHIONEIN II; METHYL CPG BINDING PROTEIN; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; HISTONE MODIFICATION; MALE; MOUSE; NEWBORN; NONHUMAN; PRENATAL DISORDER; PROMOTER REGION; PROTEIN BINDING; ZINC DEFICIENCY;

ANIMALS; CADMIUM; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; HISTONES; LIVER; MALE; METALLOTHIONEIN; MICE; MICE, INBRED C57BL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; ZINC;

MUS;

EID: 84870410742     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.05.013     Document Type: Article

References (50)

1. Painter R.C., Roseboom T.J., Bleker O.P. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 2005, 20:345-352.
2. Barker D.J., Winter P.D., Osmond C., Margetts B., Simmonds S.J. Weight in infancy and death from ischaemic heart disease. Lancet 1989, 2:577-580.
3. Barker D.J., Osmond C., Golding J., Kuh D., Wadsworth M.E. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989, 298:564-567.
4. Forsen T., Eriksson J.G., Tuomilehto J., Osmond C., Barker D.J. Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study. BMJ 1999, 319:1403-1407.
5. Gillman M.W., Barker D., Bier D., Cagampang F., Challis J., Fall C., et al. Meeting report on the 3rd International Congress on Developmental Origins of Health and Disease (DOHaD). Pediatr Res 2007, 61:625-629.
6. Torrens C., Poston L., Hanson M.A. Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation. Br J Nutr 2008, 100:760-766.
7. Burdge G.C., Slater-Jefferies J., Torrens C., Phillips E.S., Hanson M.A., Lillycrop K.A. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr 2007, 97:435-439.
8. Simmons R.A., Templeton L.J., Gertz S.J. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 2001, 50:2279-2286.
9. Park J.H., Stoffers D.A., Nicholls R.D., Simmons R.A. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest 2008, 118:2316-2324.
10. Bernal A.J., Jirtle R.L. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res A Clin Mol Teratol 2010, 88:938-944.
11. Newbold R.R., Padilla-Banks E., Jefferson W.N., Heindel J.J. Effects of endocrine disruptors on obesity. Int J Androl 2008, 31:201-208.
12. Waterland R.A., Travisano M., Tahiliani K.G. Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J 2007, 21:3380-3385.
13. Jones P.A., Baylin S.B. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002, 3:415-428.
14. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
15. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
16. Tomat A.L., Inserra F., Veiras L., Vallone M.C., Balaszczuk A.M., Costa M.A., et al. Moderate zinc restriction during fetal and postnatal growth of rats: effects on adult arterial blood pressure and kidney. Am J Physiol Regul Integr Comp Physiol 2008, 295:R543-R549.
17. Halas E.S., Eberhardt M.J., Diers M.A., Sandstead H.H. Learning and memory impairment in adult rats due to severe zinc deficiency during lactation. Physiol Behav 1983, 30:371-381.
18. Halas E.S., Hunt C.D., Eberhardt M.J. Learning and memory disabilities in young adult rats from mildly zinc deficient dams. Physiol Behav 1986, 37:451-458.
19. Beach R.S., Gershwin M.E., Hurley L.S. Gestational zinc deprivation in mice: persistence of immunodeficiency for three generations. Science 1982, 218:469-471.
20. Tuerk M.J., Fazel N. Zinc deficiency. Curr Opin Gastroenterol 2009, 25:136-143.
21. Vallee B.L., Falchuk K.H. The biochemical basis of zinc physiology. Physiol Rev 1993, 73:79-118.
22. Hunt J.R. Bioavailability of iron, zinc, and other trace minerals from vegetarian diets. Am J Clin Nutr 2003, 78:633S-639S.
23. Wastney M.E., Ahmed S., Henkin R.I. Changes in regulation of human zinc metabolism with age. Am J Physiol 1992, 263:R1162-R1168.
24. Menzano E., Carlen P.L. Zinc deficiency and corticosteroids in the pathogenesis of alcoholic brain dysfunction - a review. Alcohol Clin Exp Res 1994, 18:895-901.
25. Jeejeebhoy K. Zinc: an essential trace element for parenteral nutrition. Gastroenterology 2009, 137:S7-12.
26. Fischer Walker C.L., Ezzati M., Black R.E. Global and regional child mortality and burden of disease attributable to zinc deficiency. Eur J Clin Nutr 2009, 63:591-597.
27. Coyle P., Philcox J.C., Carey L.C., Rofe A.M. Metallothionein: the multipurpose protein. Cell Mol Life Sci 2002, 59:627-647.
28. Nies D.H. Microbial heavy-metal resistance. Appl Microbiol Biotechnol 1999, 51:730-750.
29. Solis W.A., Childs N.L., Weedon M.N., He L., Nebert D.W., Dalton T.P. Retrovirally expressed metal response element-binding transcription factor-1 normalizes metallothionein-1 gene expression and protects cells against zinc, but not cadmium, toxicity. Toxicol Appl Pharmacol 2002, 178:93-101.
30. Li Y., Kimura T., Huyck R.W., Laity J.H., Andrews G.K. Zinc-induced formation of a coactivator complex containing the zinc-sensing transcription factor MTF-1, p300/CBP, and Sp1. Mol Cell Biol 2008, 28:4275-4284.
31. Vruwink K.G., Hurley L.S., Gershwin M.E., Keen C.L. Gestational zinc deficiency amplifies the regulation of metallothionein induction in adult mice. Proc Soc Exp Biol Med 1988, 188:30-34.
32. Tomat A.L., Inserra F., Veiras L., Vallone M.C., Balaszczuk A.M., Costa M.A., et al. Moderate zinc restriction during fetal and postnatal growth of rats: effects on adult arterial blood pressure and kidney. Am J Physiol Regul Integr Comp Physiol 2008, 295:R543-R549.
33. Wang F.D., Bian W., Kong L.W., Zhao F.J., Guo J.S., Jing N.H. Maternal zinc deficiency impairs brain nestin expression in prenatal and postnatal mice. Cell Res 2001, 11:135-141.
34. Oteiza P.I., Hurley L.S., Lonnerdal B., Keen C.L. Marginal zinc deficiency affects maternal brain microtubule assembly in rats. J Nutr 1988, 118:735-738.
35. Shiizaki K., Ohsako S., Koyama T., Nagata R., Yonemoto J., Tohyama C. Lack of CYP1A1 expression is involved in unresponsiveness of the human hepatoma cell line SK-HEP-1 to dioxin. Toxicol Lett 2005, 160:22-33.
36. Clark S.J., Harrison J., Paul C.L., Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res 1994, 22:2990-2997.
37. Lee T.I., Johnstone S.E., Young R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 2006, 1:729-748.
38. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
39. Maekita T., Nakazawa K., Mihara M., Nakajima T., Yanaoka K., Iguchi M., et al. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res 2006, 12:989-995.
40. Nakajima T., Maekita T., Oda I., Gotoda T., Yamamoto S., Umemura S., et al. Higher methylation levels in gastric mucosae significantly correlate with higher risk of gastric cancers. Cancer Epidemiol Biomarkers Prev 2006, 15:2317-2321.
41. Fujiki K., Kano F., Shiota K., Murata M. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol 2009, 7:38.
42. Anier K., Malinovskaja K., Aonurm-Helm A., Zharkovsky A., Kalda A. DNA methylation regulates cocaine-induced behavioral sensitization in mice. Neuropsychopharmacology 2010, 35:2450-2461.
43. Bromer J.G., Zhou Y., Taylor M.B., Doherty L., Taylor H.S. Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J 2010, 24:2273-2280.
44. Asano H., Aonuma M., Sanosaka T., Kohyama J., Namihira M., Nakashima K. Astrocyte differentiation of neural precursor cells is enhanced by retinoic acid through a change in epigenetic modification. Stem Cells 2009, 27:2744-2752.
45. Okumura F., Li Y., Itoh N., Nakanishi T., Isobe M., Andrews G.K., et al. The zinc-sensing transcription factor MTF-1 mediates zinc-induced epigenetic changes in chromatin of the mouse metallothionein-I promoter. Biochim Biophys Acta 2011, 1809:56-62.
46. Andrews G.K., Geiser J. Expression of the mouse metallothionein-I and -II genes provides a reproductive advantage during maternal dietary zinc deficiency. J Nutr 1999, 129:1643-1648.
47. Dalton T., Fu K., Palmiter R.D., Andrews G.K. Transgenic mice that overexpress metallothionein-I resist dietary zinc deficiency. J Nutr 1996, 126:825-833.
48. Kelly E.J., Quaife C.J., Froelick G.J., Palmiter R.D. Metallothionein I and II protect against zinc deficiency and zinc toxicity in mice. J Nutr 1996, 126:1782-1790.
49. Wells J.C. The thrifty phenotype hypothesis: thrifty offspring or thrifty mother?. J Theor Biol 2003, 221:143-161.
50. Searle P.F., Davison B.L., Stuart G.W., Wilkie T.M., Norstedt G., Palmiter R.D. Regulation, linkage, and sequence of mouse metallothionein I and II genes. Mol Cell Biol 1984, 4:1221-1230.