Cerebral gene expression and neurobehavioural responses in mice pups exposed to methylmercury and docosahexaenoic acid through the maternal diet

Environmental Toxicology and Pharmacology

Volumn 33, Issue 1, 2012, Pages 26-38

  Jayashankar, S ^a,b   Glover, C N ^c   Folven, K I ^a   Brattelid, T ^a,b   Hogstrand, C ^a,d   Lundebye, A K ^a,b  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c UNIVERSITY OF CANTERBURY   (New Zealand)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Docosahexaenoic acid; Grasping reflex; Methylmercury; Mice; Microarray; Polyunsaturated fatty acids

Indexed keywords

DOCOSAHEXAENOIC ACID; METHYLMERCURY;

ANALYTIC METHOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN TISSUE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIET SUPPLEMENTATION; DRUG EXPOSURE; FATTY ACID ANALYSIS; FEMALE; GENE EXPRESSION; MALE; MATERNAL NUTRITION; MICROARRAY ANALYSIS; MOUSE; NEUROTOXICITY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGENY;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; DIET; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; MALE; METHYLMERCURY COMPOUNDS; MICE; MICE, INBRED BALB C; MICROARRAY ANALYSIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION;

MAMMALIA; MUS;

EID: 80155141230     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2011.10.001     Document Type: Article

References (59)

1. Akbar M., Kim H.Y. Protective effects of docosahexaenoic acid in Staurosporine induced apoptosis: involvement of phosphatidylinositol-3 kinase pathway. J. Neurochem. 2002, 82:655-665.
2. Alves da Costa C. Recent advances on alpha-synuclein cell biology: functions and dysfunctions. Curr. Mol. Med. 2003, 3:17-24.
3. Aschner M., Syversen T. Methylmercury-recent advances in the understanding of its neurotoxicity. Ther. Drug Monit. 2005, 27:278-283.
4. Aschner M., Yao C.P., Allen J.W., Tan K.H. Methylmercury alters glutamate transport in astrocytes. Neurochem. Int. 2000, 37:199-206.
5. Atchison W.D. Is chemical neurotransmission altered specifically during methylmercury-induced cerebellar dysfunction?. Trends Pharmacol. Sci. 2005, 26:549-557.
6. Beblo S., Reinhardt H., Demmelmair H., Muntau A.C., Koletzko B. Effect of fish oil supplementation on fatty acid status, coordination, and fine motor skills in children with phenylketonuria. J. Pediatr. 2006, 150:479-484.
7. Bellum B., Thuett K.A., Taylor R.J., Abbott L.C. Assessment of mercury concentrations in mouse brain using different routes of administration and different tissue preparations. Toxicol. Mech. Methods. 2007, 17:165-173.
8. Berntssen M.H.G., Hylland K., Lundebye A.K., Julshamn K. Higher faecal excretion and lower tissue accumulation of mercury in Wistar rats from contaminated fish than from methylmercury chloride added to fish. Food Chem. Toxicol. 2004, 42:1359-1366.
9. Bronstein J.M., Tiwari-Woodruff S., Buznikov A.G., Stevens D.B. Involvement of OSP/claudin-11 in oligodendrocyte membrane interactions: role in biology and disease. J. Neurosci. Res. 2000, 59:706-711.
10. Chapman L., Chan H.M. The influence of nutrition on methyl mercury intoxication. Environ. Health Perspect. 2000, 108:29-56.
11. Choi B.H., Cho K.H., Lapham L.W. Effects of methylmercury on DNA synthesis of human fetal astrocytes: a radioautographic study. Brain Res. 1980, 202:238-242.
12. Clarkson T.W. The toxicology of mercury. Crit. Rev. Clin. Lab. Sci. 1997, 34:369-403.
13. Clarkson T.W., Strain J.J. Nutritional factors may modify the toxic action of methyl mercury in fish-eating populations. J. Nutr. 2003, 133:1539-1543.
14. Coluccia A., Borracci P., Renna G., Giustino A., Latronico T., Riccio P., Carratu M.R. Developmental omega-3 supplementation improves motor skills in juvenile-adult rats. Int. J. Dev. Neurosci. 2009, 27:599-605.
15. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003, 4:3.
16. Domingo J.L., Bocio A., Falcó J., Llobet J.M. Benefits and risks of fish consumption. I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology 2007, 230:219-226.
17. Falnoga I., Tusek-Znidaric M., Horvat M., Stegnar P. Mercury, selenium, and cadmium in human autopsy samples from Idrija residents and mercury mine workers. Environ. Res. 2000, 84:211-218.
18. Folven K.I., Glover C.N., Malde M.K., Lundebye A.K. Does selenium modify neurobehavioural impacts of developmental methylmercury exposure in mice?. Environ. Toxicol. Pharmacol. 2009, 28:111-119.
19. Genuis S.J. To sea or not to sea: Benefits and risks of gestational fish consumption. Reprod. Toxicol. 2008, 26:81-85.
20. Geisbrecht B.V., Zhang D., Schulz H., Gould S.J. Characterization of PECI, a novel monofunctional Delta(3), Delta(2)-enoyl-CoA isomerase of mammalian peroxisomes. J. Biol. Chem. 1999, 274:21797-21803.
21. Glover C.N., Zheng D., Jayashankar S., Sales G.D., Hogstrand C., Lundebye A.K. Methylmercury speciation influences brain gene expression and behaviour in gestationally-exposed mice pups. Toxicol. Sci. 2009, 110:389-400.
22. Goulet S., Dore F.Y., Mirault M.E. Neurobehavioral changes in mice chronically exposed to methylmercury during fetal and early postnatal development. Neurotoxicol. Teratol. 2003, 25:335-347.
23. Grandjean P., Weihe P., White R.F., Debes F., Araki S., Yokoyama K., Murata K., Sorensen N., Dahl R., Jorgensen P.J. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 1997, 19:417-428.
24. Han J., Lee J.D., Jiang Y., Li Z., Feng L., Ulevitch R.J. Characterization of. the structure and function of a novel MAP kinase kinase (MKK6). J. Biol. Chem. 1996, 271:2886-2891.
25. Harris H.H., Pickering I.J., George G.N. The chemical form of mercury in fish. Science 2003, 301:1203.
26. Hibbeln J.R., Davis J.M., Steer C., Emmett P., Rogers I., Williams C., Golding J. Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in. childhood (ALSPAC study): an observational cohort study. Lancet 2007, 369:578-585.
27. Igata A. Epidemiological and clinical features of Minimata disease. Environ. Res. 1993, 63:157-169.
28. Innis S.M. Dietary (n-3) fatty acids and brain development. J. Nutr. 2007, 137:855-859.
29. Ikemoto A., Kobayashi T., Watanabe S., Okuyama H. Membrane fatty acid. modifications of PC12 cells by arachidonate or docosahexaenoate affect neurite outgrowth but not norepinephrine release. Neurochem. Res. 1997, 22:671-678.
30. Jayashankar S., Glover C., Folven K.I., Brattelid T., Hogstrand C., Lundebye A.-K. Cerebral gene expression in response to single or combined gestational exposure to methylmercury and selenium through the maternal diet. Cell Biol. Toxicol. 2010, 27:181-197.
31. Jin X., Lok E., Bondy G., Caldwell D., Mueller R., Kapal K., Armstrong C., Taylor M., Kubow S., Mehta R., Chan H.M. Modulating effects of dietary fats on methylmercury toxicity and distribution in rats. Toxicology 2007, 230:22-44.
32. Julshamn K., Måge A., Norli H.S., Grobecker K.H., Jorhem L., Fecher P. Determination of arsenic, cadmium, mercury and lead by ICP-MS in foods after pressure digestion: NMKL Collaborative study. J. AOAC Int. 2007, 90:844-856.
33. Kaur P., Schulz K., Aschner M., Syversen T. Role of docosahexaenoic acid in modulating methylmercury-induced neurotoxicity. Toxicol. Sci. 2007, 100:423-432.
34. Kitajka K., Puskas L.G., Zvara A., Hackler L., Barcelo-Coblijn G., Yeo Y.K., Farkas T. The role of n-3 polyunsaturated fatty acids in brain: Modulation of rat brain gene expression by dietary n-3 fatty acids. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2619-2624.
35. Kim H.Y. Novel metabolism of docosahexaenoic acid in neural cells. J. Biol. Chem. 2007, 282:18661-18665.
36. Lewandowski T.A., Ponce R.A., Charleston J.S., Hong S., Faustman E.M. Effect of methylmercury on midbrain cell proliferation during organogenesis: potential cross species differences and implications for risk assessment. Toxicol. Sci. 2003, 75:124-133.
37. Lie Ø., Lambertsen G. Fatty acid composition of glycerophospholipids in seven tissues of cod (Gadus morhua), determined by a combined HPLC/GC method. J. Chromatograph. 1991, 565:119-129.
38. Mahaffey K.R. Fish and shellfish as dietary sources of methylmercury and the omega-3 fatty acids, eicosahexaenoic acid and docosahexaenoic acid: risks and benefits. Environ. Res. 2004, 95:414-428.
39. Mahaffey K.R., Clickner P.R., Jeffries R.A. Methylmercury and omega-3 fatty acids: Co-occurrence of dietary sources with emphasis on fish and shellfish. Environ. Res. 2008, 107:20-29.
40. Markowski V.P., Flaugher C.B., Baggs R.B., Rawleigh R.C., Cox C., Weiss B. Prenatal and lactational exposure to methylmercury affects select parameters of mouse cerebellar development. Neurotoxicology 1998, 19:879-892.
41. McKee A.E., Minet E., Stern C., Riahi S., Stiles C.D., Silver P.A. A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev. Biol. 2005, 5:14.
42. Mechenthaler I. Galanin and the neuroendocrine axes. Cell. Mol. Life Sci. 2008, 65:1826-1835.
43. Myers G.J., Davidson P.W., Cox C., Shamlaye C.F., Palumbo D., Cernichiari E., Sloane-Reeves J., Wilding G.E., Kost J., Huang L.S., Clarkson T.W. Prenatal methylmercury exposure from ocean fish consumption in the Seychelles child development study. Lancet 2003, 361:1686-1692.
44. Padhi B.K., Pelletier G., Williams A., Berndt-Weis L., Yauk C., Bowers W.J., Chu I. Gene expression profiling in rat cerebellum following in utero and lactational exposure to mixtures of methylmercury, polychlorinated biphenyls and organochlorine pesticides. Toxicol. Lett. 2008, 176:93-103.
45. Raingeaud J., Whitmarsh A.J., Barrett T., Dérijard B., Davis R.J. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell Biol. 1996, 16:1247-1255.
46. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
47. Sager P.R., Doherty R.A., Rodier P.M. Effects of methylmercury on developing mouse cerebellar cortex. Exp. Neurol. 1982, 77:179-193.
48. Sarafian T.A. Methylmercury-induced generation of free radicals: biological implications. Metal Ions Biol. Syst. 1999, 36:415-444.
49. Shanker G., Aschner M. Methylmercury-induced reactive oxygen species formation in neonatal cerebral astrocytic cultures is attenuated by antioxidants. Mol. Brain Res. 2003, 110:85-91.
50. Shiomi T., Harada Y., Saito T., Shiomi N., Okuno Y., Yamaizumi M. An ERCC5 gene with homology to yeast RAD2 is involved in group G xeroderma pigmentosum. Mutat. Res. 1994, 314:167-175.
51. Stern S., Cox C., Cernichiari E., Balys M., Weiss B. Perinatal and lifetime exposure to methylmercury in the mouse: Blood and brain concentrations of mercury to 26 months of age. Neurotoxicology 2001, 22:467-477.
52. Takahashi T., Yamashita H., Nagano Y., Nakamura T., Ohmori H., Avraham H., Avraham S., Yasuda M., Matsumoto M. Identification and characterization of a novel Pyk2/related adhesion focal tyrosine kinase-associated protein that inhibits alpha-synuclein phosphorylation. J. Biol. Chem. 2003, 278:42225-42233.
53. Taylor N.J., Wong Y.S., Chieh P.C., Carty A.J. Syntheses, X-ray crystal-structure, and vibrational-spectra of L-cysteinato(methyl)mercury(II) monohydrate. J. Chem. Soc. Dalton Trans. 1975, 5:438-442.
54. Tillmann H., Eschrich K. Isolation and characterization of an allelic cDNA for human muscle fructose-1,6-bisphosphatase. Gene 1998, 212:295-304.
55. Torstensen B.E., Espe M., Sanden M., Stubhaug I., Waagbø R., Hemre G.I., Fontanillas R., Nordgarden U., Hevrøy E.M., Olsvik P., Berntssen M.H.G. Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 2008, 285:193-200.
56. Uauy R., Calderon F., Mena P. Essential fatty acids in somatic growth and brain development. World Rev. Nutr. Diet. 2001, 89:134-160.
57. Verity M.A., Brown W.J., Cheung M. Organic mercurial encephalopathy: in vivo and in vitro effects of methylmercury on synaptosomal respiration. J. Neurochem. 1975, 25:759-766.
58. Zuo P., Maniatis T. The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev. 1996, 10:1356-1368.
59. Zheng D., Kille P., Feeney G.P., Cunningham P., Handy R.D., Hogstrand C. Dynamic transcriptomic profiles of zebrafish gills in response to zinc depletion. BMC Genom. 2010, 11:548.