Developmental mercury exposure elicits acute hippocampal cell death, reductions in neurogenesis, and severe learning deficits during puberty

Journal of Neurochemistry

Volumn 103, Issue 5, 2007, Pages 1968-1981

  Falluel Morel, Anthony ^a   Sokolowski, Katie ^a   Sisti, Helene M ^b   Zhou, Xiaofeng ^a   Shors, Tracey J ^b   DiCicco Bloom, Emanuel ^a,c  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

Cell cycle; Hippocampus; Learning; Methylmercury; Neurogenesis; Programmed cell death

Indexed keywords

CYCLIN D1; CYCLIN D3; CYCLIN E; DNA; MERCURY;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN NERVE CELL; BRAIN SIZE; CELL COUNT; CELL DEATH; CEREBELLUM; CONTROLLED STUDY; DENTATE GYRUS; DEVELOPMENTAL DISORDER; DNA SYNTHESIS; EXPOSURE; FEMALE; GRANULE CELL; HIPPOCAMPUS; LEARNING DISORDER; NERVOUS SYSTEM DEVELOPMENT; NEUROTOXICITY; NEWBORN; NONHUMAN; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; PUBERTY; RAT; TRAINING;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BROMODEOXYURIDINE; CELL COUNT; CELL DEATH; CELL PROLIFERATION; CELLS, CULTURED; CYCLINS; DRUG INTERACTIONS; EMBRYO, MAMMALIAN; FEMALE; HIPPOCAMPUS; LEARNING DISORDERS; MAZE LEARNING; METHYLMERCURY COMPOUNDS; NEURONS; PEROXIDES; RATS; RATS, SPRAGUE-DAWLEY; THYMIDINE; TIME FACTORS; TRITIUM;

RATTUS;

EID: 36248961154     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04882.x     Document Type: Article

References (45)

1. Adams J., Barone S. Jr., LaMantia A., Philen R., Rice D. C., Spear L. Susser E. (2000) Workshop to identify critical windows of exposure for children's health: neurobehavioral work group summary. Environ. Health Perspect. 108 (Suppl. 3 535 544.
2. Alessandri B., Nishioka T., Heimann A., Bullock R. M. Kempski O. (2006) Caspase-dependent cell death involved in brain damage after acute subdural hematoma in rats. Brain Res. 1111, 196 202.
3. Burke K., Cheng Y., Li B., Petrov A., Joshi P., Berman R. F., Reuhl K. R. Dicicco-Bloom E. (2006) Methylmercury elicits rapid inhibition of cell proliferation in the developing brain and decreases cell cycle regulator, cyclin E. Neurotoxicology 27, 970 981.
4. Cheng Y., Tao Y., Black I. B. DiCicco-Bloom E. (2001) A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. J. Neurobiol. 46, 220 229.
5. Cheng Y., Black I. B. DiCicco-Bloom E. (2002) Hippocampal granule neuron production and population size are regulated by levels of bFGF. Eur. J. Neurosci. 15, 3 12.
6. Choi B. H., Lapham L. W., Amin-Zaki L. Saleem T. (1978) 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, 719 733.
7. DiCicco-Bloom E. Sondell M. (2005) Neural development and neurogenesis, in Kaplan & Sadock's Comprehensive Textbook of Psychiatry, Eighth Edn (Sadock B. J. Sadock V. A., eds pp. 33 49. Williams & Wilkins, Philadelphia, PA.
8. Falluel-Morel A., Aubert N., Vaudry D., Basille M., Fontaine M., Fournier A., Vaudry H. Gonzalez B. J. (2004) Opposite regulation of the mitochondrial apoptotic pathway by C2-ceramide and PACAP through a MAP-kinase-dependent mechanism in cerebellar granule cells. J. Neurochem. 91, 1231 1243.
9. Garg T. K. Chang J. Y. (2006) Methylmercury causes oxidative stress and cytotoxicity in microglia: attenuation by 15-deoxy-delta 12, 14-prostaglandin J2. J. Neuroimmunol. 171, 17 28.
10. Gould E., Beylin A., Tanapat P., Reeves A. Shors T. J. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260 265.
11. Hassoun E. A., Al-Ghafri M. Abushaban A. (2003) The role of antioxidant enzymes in TCDD-induced oxidative stress in various brain regions of rats after subchronic exposure. Free Radic. Biol. Med. 35, 1028 1036.
12. Jacobson M. (1991) Developmental Neurobiology. Plenum Publishing Corp, New York.
13. Kandel E., Schwartz J. H. Jessell T. M. (2000) Principles of Neural Science. Elsevier, New York.
14. Kanit L., Taskiran D., Yilmaz O. A., Balkan B., Demirgoren S., Furedy J. J. Pogun S. (2000) Sexually dimorphic cognitive style in rats emerges after puberty. Brain Res. Bull. 52, 243 248.
15. Kaur P., Aschner M. Syversen T. (2006) Glutathione modulation influences methyl mercury induced neurotoxicity in primary cell cultures of neurons and astrocytes. Neurotoxicology 27, 492 500.
16. Kerr J. F., Wyllie A. H. Currie A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239 257.
17. Kolb B. Cioe J. (2000) Recovery from early cortical damage in rats, VIII. Earlier may be worse: behavioural dysfunction and abnormal cerebral morphogenesis following perinatal frontal cortical lesions in the rat. Neuropharmacology 39, 756 764.
18. Lapham L. W., Cernichiari E., Cox C., Myers G. J., Baggs R. B., Brewer R., Shamlaye C. F., Davidson P. W. Clarkson T. W. (1995) An analysis of autopsy brain tissue from infants prenatally exposed to methymercury. Neurotoxicology 16, 689 704.
19. Lewandowski T. A., Pierce C. H., Pingree S. D., Hong S. Faustman E. M. (2002) Methylmercury distribution in the pregnant rat and embryo during early midbrain organogenesis. Teratology 66, 235 241.
20. Lu N. DiCicco-Bloom E. (1997) Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc. Natl Acad. Sci. USA 94, 3357 3362.
21. Mazumder S., Gong B., Chen Q., Drazba J. A., Buchsbaum J. C. Almasan A. (2002) Proteolytic cleavage of cyclin E leads to inactivation of associated kinase activity and amplification of apoptosis in hematopoietic cells. Mol. Cell. Biol. 22, 2398 2409.
22. Monfils M. H., Driscoll I., Vandenberg P. M., Thomas N. J., Danka D., Kleim J. A. Kolb B. (2005) Basic fibroblast growth factor stimulates functional recovery after neonatal lesions of motor cortex in rats. Neuroscience 134, 1 8.
23. Morris R. G., Anderson E., Lynch G. S. Baudry M. (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319, 774 776.
24. Myers G. J. Davidson P. W. (2000) Does methylmercury have a role in causing developmental disabilities in children? Environ. Health Perspect. 108 (Suppl. 3 413 420.
25. O'Keefe J. (1990) A computational theory of the hippocampal cognitive map. Prog. Brain Res. 83, 301 312.
26. Rice D. Barone S. Jr. (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108 (Suppl. 3 511 533.
27. Riedel G., Micheau J., Lam A. G., Roloff E. L., Martin S. J., Bridge H., de Hoz L., Poeschel B., McCulloch J. Morris R. G. (1999) Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat. Neurosci. 2, 898 905.
28. Rodier P. M. (1995) Developing brain as a target of toxicity. Environ. Health Perspect. 103 (Suppl. 6) 73 76.
29. Sakamoto M., Kakita A., de Oliveira R. B., Sheng Pan H. Takahashi H. (2004) Dose-dependent effects of methylmercury administered during neonatal brain spurt in rats. Brain Res. Dev. Brain Res. 152, 171 176.
30. Sava V., Reunova O., Velasquez A., Song S. Sanchez-Ramos J. (2006) Neuroanatomical mapping of DNA repair and antioxidative responses in mouse brain: effects of a single dose of MPTP. Neurotoxicology 27, 1080 1093.
31. Segal M. Landis S. (1974) Afferents to the hippocampus of the rat studied with the method of retrograde transport of horseradish peroxidase. Brain Res. 78, 1 15.
32. Seress L. Pokorny J. (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J. Anat. 133, 181 195.
33. Shila S., Kokilavani V., Subathra M. Panneerselvam C. (2005) Brain regional responses in antioxidant system to alpha-lipoic acid in arsenic intoxicated rat. Toxicology 210, 25 36.
34. Shors T. J., Townsend D. A., Zhao M., Kozorovitskiy Y. Gould E. (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12, 578 584.
35. Snyder J. S., Hong N. S., McDonald R. J. Wojtowicz J. M. (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843 852.
36. Spurgeon A. (2006) Prenatal methylmercury exposure and developmental outcomes: review of the evidence and discussion of future directions. Environ. Health Perspect. 114, 307 312.
37. Stanfield B. B. Cowan W. M. (1979) The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185, 393 422.
38. Stein J., Schettler T., Wallinga D. Valenti M. (2002) In harm's way: toxic threats to child development. J. Dev. Behav. Pediatr. 23, S13 S22.
39. Stringari J., Meotti F. C., Souza D. O., Santos A. R. Farina M. (2006) Postnatal methylmercury exposure induces hyperlocomotor activity and cerebellar oxidative stress in mice: dependence on the neurodevelopmental period. Neurochem. Res. 31, 563 569.
40. Tao Y., Black I. B. DiCicco-Bloom E. (1996) Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF). J. Comp. Neurol. 376, 653 663.
41. Toga A. W. Lothman E. W. (1983) Learning deficits after lesions of dentate gyrus granule cells. Exp. Neurol. 82, 192 202.
42. Vaccarino F. M., Schwartz M. L., Raballo R., Rhee J. Lyn-Cook R. (1999) Fibroblast growth factor signaling regulates growth and morphogenesis at multiple steps during brain development. Curr. Top. Dev. Biol. 46, 179 200.
43. Wagner J. P., Black I. B. DiCicco-Bloom E. (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J. Neurosci. 19, 6006 6016.
44. Wiessner C., Sauer D., Alaimo D. Allegrini P. R. (2000) Protective effect of a caspase inhibitor in models for cerebral ischemia in vitro and in vivo. Cell. Mol. Biol. (Noisy-le-grand) 46, 53 62.
45. Zornetzer S. F., Boast C. Hamrick M. (1974) Neuroanatomic localization and memory processing in mice: the role of the dentate gyrus of the hippocampus. Physiol. Behav. 13, 569 575.