Effects of developmental lead exposure on the hippocampal transcriptome: Influences of sex, developmental period, and lead exposure level

Toxicological Sciences

Volumn 129, Issue 1, 2012, Pages 108-125

  Schneider, Jay S ^a   Anderson, David W ^a   Talsania, Keyur ^a   Mettil, William ^a   Vadigepalli, Rajanikanth ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Development; Hippocampus; Lead; RNA; Transcription

Indexed keywords

LEAD; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; LACTATION; MALE; NONHUMAN; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PREGNANCY; RAT; RNA HYBRIDIZATION; RNA METABOLISM; SEX;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; LEAD; MALE; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, LONG-EVANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

ANIMALIA; RATTUS;

EID: 84865705867     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs189     Document Type: Article

References (65)

1. ACCLPP (2012). Low Level Lead Exposure Harms Children: A Renewed Call for Primary Prevention.
2. Akira, S. (1999). Functional roles of stat family proteins: Lessons from knockout mice. Stem Cells 17, 138-146.
3. Anderson, D. W., Pothakos, K., and Schneider, J. S. (Forthcoming). Sex and rearing condition modify the effects of perinatal lead exposure on learning and memory. Neurotoxicology. http://dx.doi.org/10.1016/j.neuro.2012.04.016
4. Angell, N. F., and Weiss B. (1982). Operant behavior of rats exposed to lead before or after weaning. Toxicol. Appl. Pharmacol. 63, 62-71.
5. Banks, E. C., Ferretti, L. E., and Shucard, D. W. (1997). Effects of low level lead exposure on cognitive function in children: A review of behavioral, neuropsychological and biological evidence. Neurotoxicology 18, 237-281.
6. Bellinger, D., and Rappaport, L. (2002). Developmental assessment and interventions. Managing elevated blood lead levels among young children: Recommendations from the advisory committee on childhood lead poisoning prevention. U.S. Department of Health and Human Services, Public Health Services. 77-95.
7. Bozon, B., Davis, S., and Laroche, S. (2002). Regulated transcription of the immediate-early gene Zif268: Mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus 12, 570-577.
8. Bozon, B., Davis, S., and Laroche, S. (2003). A requirement for the immediate early gene Zif268 in reconsolidation of recognition memory after retrieval. Neuron 40, 695-701.
9. Bozon, B., Kelly, A., Josselyn, S. A., Silva, A. J., Davis, S., and Laroche, S. (2003). Mapk, Creb and Zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358, 805-814.
10. Canfield, R. L., Henderson, C. R., Jr., Cory-Slechta, D. A., Cox, C., Jusko, T. A., and Lanphear, B. P. (2003). Intellectual impairment in children with blood lead concentrations below 10 microg per deciliter. N. Engl. J. Med. 348, 1517-1526.
11. CDC. (2002). Managing Elevated Blood Lead Levels among Young Children: Recommendations from the Advisory Committee on Childhood Lead Poisoning Prevention, Centers for Disease Control and Prevention (CDC).
12. CDC. (2004). A Review of the Evidence of Health Effects of Blood Lead Levels <10mg/Dl in Children. Report by the Working Group of the Advisory Committee on Childhood Lead Poisoning Prevention, Centers for Disease Control and Prevention (CDC).
13. Chiodo, L. M., Jacobson, S. W., and Jacobson, J. L. (2004). Neurodevelopmental effects of postnatal lead exposure at very low levels. Neurotoxicol. Teratol. 26, 359-371.
14. Cole, A. J., Saffen, D. W., Baraban, J. M., and Worley, P. F. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474-476.
15. Cory-Slechta, D. A., Virgolini, M. B., Rossi-George, A., Thiruchelvam, M., Lisek, R., and Weston, D. (2008). Lifetime consequences of combined maternal lead and stress. Basic Clin. Pharmacol. Toxicol. 102, 218-227.
16. Cory-Slechta, D. A., Virgolini, M. B., Thiruchelvam, M., Weston, D. D., and Bauter, M. R. (2004). Maternal stress modulates the effects of developmental lead exposure. Environ. Health Perspect. 112, 717-730.
17. Dallas, P. B., Gottardo, N. G., Firth, M. J., Beesley, A. H., Hoffmann, K., Terry, P. A., Freitas, J. R., Boag, J. M., Cummings, A. J., and Kees, U. R. (2005). Gene expression levels assessed by oligonucleotide microarray analysis and quantitative real-time RT-PCR-How well do they correlate? BMC Genomics 6, 59.
18. Deisseroth, K., Bito, H., and Tsien, R. W. (1996). Signaling from synapse to nucleus: Postsynaptic Creb phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16, 89-101.
19. Draski, L. J., Burright, R. G., and Donovick, P. J. (1989). The influence of prenatal and/or postnatal exposure to lead on behavior of preweaning mice. Physiol. Behav. 45, 711-715.
20. Gashler, A., and Sukhatme, V. P. (1995). Early growth response protein 1 (Egr-1): Prototype of a zinc-finger family of transcription factors. Prog. Nucleic Acid Res. Mol. Biol. 50, 191-224.
21. Gilbert, M. E., Mack, C. M., and Lasley, S. M. (1999). Chronic developmental lead exposure and hippocampal long-term potentiation: Biphasic dose-response relationship. Neurotoxicology 20, 71-82.
22. Gould, E. (2009). Childhood lead poisoning: Conservative estimates of the social and economic benefits of lead hazard control. Environ. Health Perspect. 117, 1162-1167.
23. Gu, Y. Z., Hogenesch, J. B., and Bradfield, C. A. (2000). The Pas superfamily: Sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
24. Guidotti, G., Calabrese, F., Auletta, F., Olivier, J., Racagni, G., Homberg, J., and Riva, M. A. (2012). Developmental influence of the serotonin transporter on the expression of Npas4 and GABAergic markers: Modulation by antidepressant treatment. Neuropsychopharmacology 37, 746-758.
25. Horvath, C. M. (2000). Stat proteins and transcriptional responses to extracellular signals. Trends Biochem. Sci. 25, 496-502.
26. Howe, E., Holton, K., Nair, S., Schlauch, D., Sinha, R., and Quackenbush, J. (2010). Mev: Multiexperiment viewer. Biomedical Informatics for Cancer Research. Springer, New York, NY, pp. 267-277.
27. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protocols 4, 44-57.
28. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
29. Jones, M. W., Errington, M. L., French, P. J., Fine, A., Bliss, T. V., Garel, S., Charnay, P., Bozon, B., Laroche, S., and Davis, S. (2001). A requirement for the immediate early gene Zif268 in the expression of late Ltp and long-term memories. Nat. Neurosci. 4, 289-296.
30. Jones, S. P., Rahimi, O., O'Boyle, M. P., Diaz, D. L., and Claiborne, B. J. (2003). Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field Ca3. Hippocampus 13, 413-427.
31. Kober, T. E., and Cooper, G. P. (1976). Lead competitively inhibits calcium-dependent synaptic transmission in the bullfrog sympathetic ganglion. Nature 262, 704-705.
32. Koller, K., Brown, T., Spurgeon, A., and Levy, L. (2004). Recent developments in low-level lead exposure and intellectual impairment in children. Environ. Health Perspect. 112, 987-994.
33. Korb, E., and Finkbeiner, S. (2011). Arc in synaptic plasticity: From gene to behavior. Trends Neurosci. 34, 591-598.
34. Kuhlmann, A. C., McGlothan, J. L., and Guilarte, T. R. (1997). Developmental lead exposure causes spatial learning deficits in adult rats. Neurosci. Lett. 233, 101-104.
35. Landrigan, P. J., Silbergeld, E. K., Froines, J. R., and Pfeffer, R. M. (1990). Lead in the modern workplace. Am. J. Public Health 80, 907-908.
36. Lanphear, B. P., Dietrich, K., Auinger, P., and Cox, C. (2000). Cognitive deficits associated with blood lead concentrations <10 microg/dl in U.S. children and adolescents. Public Health Rep. 115, 521-529.
37. Lanphear, B. P., Hornung, R., Khoury, J., Yolton, K., Baghurst, P., Bellinger, D. C., Canfield, R. L, Dietrich, K. N., Bornschein, R., Greene, T., et al. (2005). Low-level environmental lead exposure and children's intellectual function: An international pooled analysis. Environ. Health Perspect. 113, 894-899.
38. Leasure, J. L., Giddabasappa, A., Chaney, S., Johnson, J. E., Jr., Pothakos, K., Lau, Y. S., and Fox, D. A. (2008). Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ. Health Perspect. 116, 355-361.
39. Lin, J. L., Tan, D. T., Hsu, K. H., and Yu, C. C. (2001). Environmental lead exposure and progressive renal insufficiency. Arch. Intern. Med. 161, 264-271.
40. Lin, Y., Bloodgood, B. L., Hauser, J. L., Lapan, A. D., Koon, A. C., Kim, T. K., Hu, L. S., Malik, A. N., and Greenberg, M. E. (2008). Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198-1204.
41. Mendola, P., Selevan, S. G., Gutter, S., and Rice, D. (2002). Environmental factors associated with a spectrum of neurodevelopmental deficits. Ment. Retard. Dev. Disabil. Res. Rev. 8, 188-197.
42. Milbrandt, J. (1987). A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238, 797-799.
43. Mitchell, A. C., and Mirnics, K. (2012). Gene expression profiling of the brain: Pondering facts and fiction. Neurobiol. Dis. 45, 3-7.
44. Muennig, P. (2009). The social costs of childhood lead exposure in the post-lead regulation era. Arch. Pediatr. Adolesc. Med. 163, 844-849.
45. Needleman, H. L., McFarland, C., Ness, R. B., Fienberg, S. E., and Tobin, M. J. (2002). Bone lead levels in adjudicated delinquents. A case control study. Neurotoxicol. Teratol. 24, 711-717.
46. Needleman, H. L., Schell, A., Bellinger, D., Leviton, A., and Allred, E. N. (1990). The long-term effects of exposure to low doses of lead in childhood. An 11-year follow-up report. N. Engl. J. Med. 322, 83-88.
47. Nicholson, C. (2008). Synaptogenesis: Altering your inhibitions. Nat. Rev. Neurosci. 9, 800-801.
48. Nie, L., Wu, G., Culley, D. E., Scholten, J. C., and Zhang, W. (2007). Integrative analysis of transcriptomic and proteomic data: Challenges, solutions and applications. Crit. Rev. Biotechnol. 27, 63-75.
49. Ooe, N., Motonaga, K., Kobayashi, K., Saito, K., and Kaneko, H. (2009). Functional characterization of basic helix-loop-helix-pas type transcription factor Nxf in vivo: Putative involvement in an " on demand" neuroprotection system. J. Biol. Chem. 284, 1057-1063.
50. Ooe, N., Saito, K., and Kaneko, H. (2009). Characterization of functional heterodimer partners in brain for a Bhlh-Pas factor Nxf. Biochem. Biophys. Acta 1789, 192-197.
51. Ploski, J. E., Monsey, M. S., Nguyen, T., DiLeone, R. J., and Schafe, G. E. (2011). The neuronal pas domain protein 4 (Npas4) is required for new and reactivated fear memories. PLoS One 6, e23760.
52. Pongrac, J., Middleton, F. A., Lewis, D. A., Levitt, P., and Mirnics, K. (2002). Gene expression profiling with DNA microarrays: Advancing our understanding of psychiatric disorders. Neurochem. Res. 27, 1049-1063.
53. Rice, D., and 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.
54. Schnaas, L., Rothenberg, S. J., Perroni, E., Martinez, S., Hernandez, C., and Hernandez, R. M. (2000). Temporal pattern in the effect of postnatal blood lead level on intellectual development of young children. Neurotoxicol. Teratol. 22, 805-810.
55. Schneider, J. S., and Decamp, E. (2007). Postnatal lead poisoning impairs behavioral recovery following brain damage. Neurotoxicology 28, 1153-1157.
56. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.
57. Storey, J. D., and Tibshirani, R. (2003). Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U.S.A. 100, 9440-9445.
58. Tan, C. S., Salim, A., Ploner, A., Lehtio, J., Chia, K. S., and Pawitan, Y. (2009). Correlating gene and protein expression data using correlated factor analysis. BMC Bioinformatics 10, 272.
59. Tarca, A. L., Romero, R., and Draghici, S. (2006). Analysis of microarray experiments of gene expression profiling. Am. J. Obstet. Gynecol. 195, 373-388.
60. Toscano, C. D., and Guilarte, T. R. (2005). Lead neurotoxicity: From exposure to molecular effects. Brain Res. Rev. 49, 529-554.
61. Vupputuri, S., Batuman, V., Muntner, P., Bazzano, L. A., Lefante, J. J., Whelton, P. K., and He, J. (2003). Effect of blood pressure on early decline in kidney function among hypertensive men. Hypertension 42, 1144-1149.
62. Wang, H.-L., Chen, X.-T., Luo, L., Lou, Z.-Y., Wang, S., Chen, J.-T., Wang, M., Sun, L.-G., and Ruan, D.-Y. (2006). Reparatory effects of nicotine on Nmda receptor-mediated synaptic plasticity in the hippocampal ca1 region of chronically lead-exposed rats. Eur. J. Neurosci. 23, 1111-1119.
63. White, L. D., Cory-Slechta, D. A., Gilbert, M. E., Tiffany-Castiglioni, E., Zawia, N. H., Virgolini, M., Rossi-George, A., Lasley, S. M., Qian, Y. C., and Basha, M. R. (2007). New and evolving concepts in the neurotoxicology of lead. Toxicol. Appl. Pharmacol. 225, 1-27.
64. Yun, J., Koike, H., Ibi, D., Toth, E., Mizoguchi, H., Nitta, A., Yoneyama, M., Ogita, K., Yoneda, Y, Nabeshima, T., et al. (2010). Chronic restraint stress impairs neurogenesis and hippocampus-dependent fear memory in mice: Possible involvement of a brain-specific transcription factor Npas4. J. Neurochem. 114, 1840-1851.
65. Zenick, H., Lasley, S. M., Greenland, R., Caruso, V., Succop, P., Price, D., and Michaelson, I. A. (1982). Regional brain distribution of alpha-amphetamine in lead-exposed rats. Toxicol. Appl. Pharmacol. 64, 52-63.