Developmental exposure to methylmercury elicits early cell death in the cerebral cortex and long-term memory deficits in the rat

International Journal of Developmental Neuroscience

Volumn 27, Issue 2, 2009, Pages 165-174

  Ferraro, Luca ^a   Tomasini, Maria Cristina ^a   Tanganelli, Sergio ^a   Mazza, Roberta ^a   Coluccia, Addolorata ^b   Carratù, Maria Rosaria ^b   Gaetani, Silvana ^c   Cuomo, Vincenzo ^c   Antonelli, Tiziana ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Apoptosis; Cortical neuron cultures; Glutamate; Microtubule disruption; MTT reduction assay; Nuclear chromatin condensation; Passive avoidance task

Indexed keywords

GLUTAMIC ACID; METHYLMERCURY;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN CORTEX LESION; BRAIN DEVELOPMENT; CELL DAMAGE; CELL DEATH; CELL FATE; CELL FUNCTION; CELL PROLIFERATION; CELL VIABILITY; CHROMATIN CONDENSATION; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATIONAL STUDY; EXCITOTOXICITY; FEMALE; LONG TERM MEMORY; MEMORY CONSOLIDATION; MICROTUBULE; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PASSIVE AVOIDANCE; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT;

ANIMALS; AVOIDANCE LEARNING; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CHROMATIN; FEMALE; GLUTAMIC ACID; MALE; MEMORY DISORDERS; METHYLMERCURY COMPOUNDS; NEURITES; NEURONS; NEUROTOXINS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 58849143304     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2008.11.004     Document Type: Article

References (68)

1. Alho H., Ferrarese C., Vicini S., and Vaccarino F. Subsets of GABAergic neurons in dissociated cell cultures of neonatal rat cerebral cortex show co-localization with specific modulator peptides. Dev. Brain Res. 39 (1988) 193-204
2. Allen J.W., Shanker G., Tan K.H., and Aschner M. The consequences of methylmercury exposure on interactive functions between astrocytes and neurons. Neurotoxicology 23 (2002) 755-759
3. Antonelli T., Tanganelli S., Tomasini M.C., Finetti S., Trabace L., Steardo L., Sabino V., Carratu' M.R., Cuomo V., and Ferraro L. Long-term effects on cortical glutamate release induced by prenatal exposure to the cannabinoid receptor agonist (R)-(+)-[2,3-dihydro-5-methyl-3-(4-morpholinyl-methyl)pyrrolo[1,2,3-de]-1,4-benzoxazin-6-yl]-1-naphthalenylmethanone: an in vivo microdialysis study in the awake rat. Neuroscience 124 (2004) 367-375
4. Aschner M. Astrocytes as modulators of mercury-induced neurotoxicity. Neurotoxicology 17 (1996) 663-669
5. Aschner M., Yao C.P., Allen J.V., and Tan K.H. Methylmercury alters glutamate transport in astrocytes. Neurochem. Int. 37 (2000) 199-206
6. Baraldi M., Zanoli P., Tascedda F., Blom J.M.C., and Brunello N. Cognitive deficits and changes in gene expression of NMDA receptors after prenatal methylmercury exposure. Environ. Health Perspect. 110 (2002) 855-858
7. Bontempi B., Laurent-Demir C., Destrade C., and Jaffard R. Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400 (1999) 671-675
8. Bulleit R.F., and Cui H. Methylmercury antagonizes the survival-promoting activity of insulin-like growth factor on developing cerebellar granule neurons. Toxicol. Appl. Pharmacol. 153 (1998) 161-168
9. Burbacher T.M., Rodier P.M., and Weiss B. Methylmercury developmental neurotoxicity: a comparison of effects in humans and animals. Neurotoxicol. Teratol. 12 (1990) 191-202
10. Burbacher T.M., Shen D.D., Liberato N., Grant K.S., Cernichiari E., and Clarkson T. Comparison of blood and brain mercury levels in infant monkeys exposed to methylmercury or vaccines containing thimerosal. Environ. Health Perspect. 113 (2005) 1015-1021
11. Burke K., Cheng Y., Li B., Petrov A., Joshi P., Berman R.F., Reuhl K.R., and Dicicco-Bloom E. Methylmercury elicits rapid inhibition of cell proliferation in the developing brain and decreases cell cycle regulator, cyclin E. Neurotoxicology 27 (2006) 970-981
12. Cagiano R., De Salvia M.A., Renna G., Tortella E., Braghiroli D., Parenti C., Zanoli P., Baraldi M., Annau Z., and Cuomo V. Evidence that exposure to methyl mercury during gestation induces behavioral and neurochemical changes in offspring of rats. Neurotoxicol. Teratol. 12 (1990) 23-28
13. Cameron H.A., Hazel T.G., and McKay R.D.G. Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36 (1998) 287-306
14. Carratù M.R., Borracci P., Coluccia A., Giustino A., Renna G., Tomasini M.C., Raisi E., Antonelli T., Cuomo V., Mazzoni E., and Ferraro L. Acute exposure to methylmercury at two developmental windows: focus on neurobehavioral and neurochemical effects in rat offspring. Neuroscience 141 (2006) 1619-1629
15. Carratù M.R., Coluccia A., Modafferi A.M., Borracci P., Scaccianoce S., Sakamoto M., and Cuomo V. Prenatal methylmercury exposure: effects on stress response during active learning. Bull. Environ. Contam. Toxicol. 81 (2008) 539-542
16. Castoldi A.F., Barni S., Turin I., Gandini C., and Manzo L. Early acute necrosis, delayed apoptosis and cytoskeletal breakdown in cultured cerebellar granule neurons exposed to methylmercury. J. Neurosci. Res. 59 (2000) 775-787
17. Castoldi A.F., Coccini T., Ceccatelli S., and Manzo L. Neurotoxicity and molecular effects of methylmercury. Brain Res. Bull. 55 (2001) 197-203
18. Ceccatelli S., Tamm C., Zhang Q., and Chen M. Mechanisms and modulation of neural cell damage induced by oxidative stress. Physiol. Behav. 92 (2007) 87-92
19. Choi B.H., Lapham L.W., Amin-Zaki L., and Saleem T. Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: a major effect of methylmercury poisoning in utero. J. Neuropathol. Exp. Neurol. 37 (1978) 719-733
20. Choi B.H. Effects of methylmercury on neuroepithelial germinal cells in the developing telencephalic vesicles of mice. Acta Neuropathol. 81 (1991) 359-385
21. Clarkson T.W., Nordberg G.F., and Sager P.R. Reproductive and developmental toxicity of metals. Scand. J. Work Environ. Health 11 (1985) 145-154
22. Cristol D.A., Brasso R.L., Condon A.M., Fovargue R.E., Friedman S.L., Hallinger K.K., Monroe A.P., and White A.E. The movement of aquatic mercury through terrestrial food webs. Science 320 5874 (2008) 335
23. Cuomo V., Ambrosi L., Annau Z., Cagiano R., Brunello N., and Racagni G. Behavioral and neurochemical changes in offspring of rats exposed to methyl mercury during gestation. Neurobehav. Toxicol. Teratol. 6 (1984) 249-254
24. Daré E., Gorman A.M., Ahlbom E., Götz M., Momoi T., and Ceccatelli S. Apoptotic morphology does not always require caspase activity in rat cerebellar granule neurons. Neurotox. Res. 3 (2001) 501-514
25. DiCicco-Bloom E., and Sondell M. Neural development and neurogenesis. Kaplan & Sadock's Comprehensive Textbook of Psychiatry Vol. 8 (2005), Lippincott Williams & Wilkins, Philadelphia pp. 33-49
26. Falluel-Morel A., Sokolowski K., Sisti H.M., Zhou X., Shors T.J., and DiCicco-Bloom E. Developmental mercury exposure elicits acute hippocampal cell death, reductions in neurogenesis, and severe learning deficits during puberty. J. Neurochem. 103 5 (2007) 1968-1981
27. Faustman E.M., Ponce R.A., Ou Y.C., Mendoza M.A., Lewandowski T., and Kavanagh T. Investigations of methylmercury-induced alterations in neurogenesis. Environ. Health Perspect. 110 (2002) 859-864
28. Fonfría E., Daré E., Benelli M., Suñol C., and Ceccatelli S. Translocation of apoptosis-inducing factor in cerebellar granule cells exposed to neurotoxic agents inducing oxidative stress. Eur. J. Neurosci. 16 (2002) 2013-2016
29. Forman L.J. The effect of cannabinoid receptor antagonism with SR141716A on antinociception induced by cocaine and the NMDA receptor antagonist, MK-801. Brain Res. Bull. 61 (2003) 153-158
30. Frankland P.W., O'Brien C., Ohno M., Kirkwood A., and Silva A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411 (2001) 309-313
31. Fuster J.M. Executive frontal functions. Exp. Brain Res. 133 (2000) 66-70
32. Garg T.K., and Chang J.Y. Methylmercury causes oxidative stress and cytotoxicity in microglia: attenuation by 15-deoxy-delta 12,14-prostaglandin J2. J. Neuroimmunol. 171 (2006) 17-28
33. Goulet S., Dore F.Y., and Mirault M.E. Neurobehavioral changes in mice chronically exposed to methylmercury during fetal and early postnatal development. Neurotoxicol. Teratol. 25 (2003) 335-347
34. Haseman J.K., and Piegorsch W.W. Statistical analysis of developmental toxicity data. In: Kimmel C.A., and Buelke-Sam J. (Eds). Developmental Toxicology. second ed. (1994), Raven press, New York 349-361
35. Herschkowitz N. Brain development in the fetus, neonate and infant. Biol. Neonate 54 (1988) 1-19
36. Juárez B.I., Martínez M.L., Montante M., Dufour L., García E., and Jiménez-Capdeville M.E. Methylmercury increases glutamate extracellular levels in frontal cortex of awake rats. Neurotoxicol. Teratol. 24 (2002) 767-771
37. Juárez B.I., Portillo-Salazar H., González-Amaro R., Mandeville P., Aguirre J.R., and Jiménez M.E. Participation of N-methyl-d-aspartate receptors on methylmercury-induced DNA damage in rat frontal cortex. Toxicology 207 (2005) 223-229
38. Karl T., Pabst R., and von Hörsten S. Behavioral phenotyping of mice in pharmacological and toxicological research. Exp. Toxicol. Pathol. 55 (2003) 69-83
39. Komuro H., and Rakic P. Modulation of neuronal migration by NMDA receptors. Science 260 (1993) 95-97
40. Kuo T.C., and Lin-Shiau S.Y. Early acute necrosis and delayed apoptosis induced by methyl mercury in murine peritoneal neutrophils. Basic Clin. Pharmacol. Toxicol. 94 (2004) 274-281
41. Lapham L.W., Cernichiari E., Cox C., Myers G.J., Baggs R.B., Brewer R., Shamlaye C.F., Davidson P.W., and Clarkson T.W. An analysis of autopsy brain tissue from infants prenatally exposed to methylmercury. Neurotoxicology 16 (1995) 689-704
42. Lewandowski T.A., Pierce C.H., Pingree S.D., Hong S., and Faustman E.M. Methylmercury distribution in the pregnant rat and embryo during early midbrain organogenesis. Teratology 66 (2002) 235-241
43. Magos L., and Butler W.H. The kinetics of methylmercury administered repeatedly to rats. Arch. Toxicol. 35 (1976) 25-39
44. Marsh D.O. Dose-response relationships in humans: methyl mercury epidemics in Japan and Iraq. The Toxicity of Methyl Mercury (1987), The Johns Hopkins University Press, Baltimore, MD pp. 45-53
45. Marsh D.O., Clarkson T.W., Cox C., Myers G.J., Amin-Zaki L., and Al-Tikriti S. Fetal methylmercury poisoning: relationship between concentration in single strands of maternal hair and child effects. Arch Neurol 44 (1987) 1017-1022
46. Mattson M.P., and Kroemer G. Mitochondria in cell death: novel targets for neuroprotection and cardioprotection. Trends Mol Med 9 (2003) 196-205
47. Maviel T., Durkin T.P., Menzaghi F., and Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science 305 (2004) 96-99
48. Miura K., and Imura N. Mechanism of methylmercury cytotoxicity. Crit Rev Toxicol 18 (1987) 161-188
49. Miyamoto K., Nakanishi H., Moriguchi S., Fukuyama N., Eto K., Wakamiya J., Murao K., Arimura K., and Osame M. Involvement of enhanced sensitivity of N-methyl-d-aspartate receptors in vulnerability of developing cortical neurons to methylmercury neurotoxicity. Brain Res. 901 (2001) 252-258
50. Morken T.S., Sonnewald U., Aschner M., and Syversen T. Effects of methylmercury on primary brain cells in mono- and co-culture. Toxicol. Sci. 87 (2005) 169-175
51. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
52. Nagashima K. A review of experimental methylmercury toxicity in rats: neuropathology and evidence for apoptosis. Toxicol. Pathol. 25 (1997) 624-631
53. Newland M.C., and Reile P.A. Blood and brain mercury levels after chronic gestational exposure to methylmercury in rats. Toxicol. Sci. 50 (1999) 106-116
54. Ponce R.A., Kavanagh T.J., Mottet N.K., Whittaker S.G., and Faustman E.M. Effects of methyl mercury on the cell cycle of primary rat CNS cells in vitro. Toxicol. Appl. Pharmacol. 127 (1994) 83-90
55. Prathiba J., Kumar K.B., and Karanth K.S. Effects of REM sleep deprivation on cholinergic receptor sensitivity and passive avoidance behavior in clomipramine model of depression. Brain Res. 867 (2000) 243-245
56. Rodier P.M., Aschner M., and Sager P.R. Mitotic arrest in the developing CNS after prenatal exposure to methylmercury. Neurobehav. Toxicol. Teratol. 6 (1984) 379-385
57. Rossi A.D., Ahlbom E., Ogren S.O., Nicotera P., and Ceccattelli S. Prenatal exposure to methylmercury alters locomotor activity of male but not female rats. Exp. Brain Res. 117 (1997) 428-436
58. Roy C., Prasad K.V.S., Reuhl K.R., Little J.E., Valentine B.K., and Brown D.L. Taxol protects the microtubules of concanavlin A-activated lymphocytes from disassembly by methylmercury, but DNA synthesis is still inhibited. Exp. Cell Res. 195 (1991) 345-352
59. Sager P.R., Aschner M., and Rodier P.M. Persistent, differential alterations in developing cerebellar cortex of male and female mice after methylmercury exposure. Brain Res. 314 (1984) 1-11
60. Sakaue M., Okazaki M., and Hara S. Very low levels of methylmercury induce cell death of cultured rat cerebellar neurons via calpain activation. Toxicology 213 (2005) 97-106
61. Sánchez C., Pérez M., and Avila J. GSK3beta-mediated phosphorylation of the microtubule-associated protein 2C (MAP2C) prevents microtubule bundling. Eur. J. Cell Biol. 79 (2000) 252-260
62. Shanker G., Syversen T., and Aschner M. Astrocyte-mediated methylmercury neurotoxicity. Biol. Trace Elem. Res. 95 (2003) 1-10
63. Spurgeon A. Prenatal methylmercury exposure and developmental outcomes: review of the evidence and discussion of future directions. Environ. Health Perspect. 114 (2006) 307-312
64. Stephenson F.A., Cousins S.L., and Kenny A.V. Assembly and forward trafficking of NMDA receptors. Mol. Membr. Biol. 25 (2008) 311-320
65. Takehara K., Kawahara S., and Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J. Neurosci. 23 (2003) 9897-9905
66. Tamm C., Duckworth J., Hermanson O., and Ceccatelli S. High susceptibility of neural stem cells to methylmercury toxicity: effects on cell survival and neuronal differentiation. J. Neurochem. 97 (2006) 69-78
67. Tchounwou P.B., Ayensu W.K., Ninashvili N., and Sutton D. Environmental exposure to mercury and its toxicopathologic implications for public health. Environ. Toxicol. 18 (2003) 149-175
68. Wilke R.A., Kolbert C.P., Rahimi R.A., and Windebank A.J. Methylmercury induces apoptosis in cultured rat dorsal root ganglion neurons. Neurotoxicology 24 (2003) 369-378