Toluene effects on gene expression in the hippocampus of young adult, middle-age, and senescent brown norway rats

Toxicological Sciences

Volumn 126, Issue 1, 2012, Pages 193-212

  Royland, Joyce E ^a   Kodavanti, Prasada Rao S ^a   Schmid, Judith E ^a   MacPhail, Robert C ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Genomics; Hippocampus; Life stage; Oxidative stress; Susceptibility; Toluene

Indexed keywords

TOLUENE; TRANSCRIPTOME;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL METABOLISM; CONTROLLED STUDY; CYTOSKELETON; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INTERACTION; GENETIC SUSCEPTIBILITY; GENOME ANALYSIS; HIPPOCAMPUS; IMMUNE RESPONSE; LIFESPAN; MALE; MIDDLE AGED; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN METABOLISM; RAT; SENESCENCE; UPREGULATION;

RATTUS; RATTUS NORVEGICUS;

EID: 84857968209     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr340     Document Type: Article

References (66)

1. Aylward, L. L., Barton, H. A., and Hays, S. M. (2008). Biomonitoring equivalents (BE) dossier for toluene (CAS No. 108-88-3). Regul. Toxicol. Pharmacol. 51, S27-S36.
2. Benignus, V. A., Boyes, W. K., Kenyon, E. M., and Bushnell, P. J. (2007). Quantitative comparisons of the acute neurotoxicity of toluene in rats and humans. Toxicol. Sci. 100, 146-145.
3. Boey, K. W., Foo, S. C., and Jeyaratnam, J. (1997). Effects of occupational exposure to toluene: A neuropsychological study on workers in Singapore. Ann. Acad. Med. Singapore 26, 184-187.
4. Bowen, S. E., Hannigan, J. H., and Irtenkauf, S. (2007). Maternal and fetal blood and organ toluene levels in rats following acute and repeated binge inhalation exposure. Reprod. Toxicol. 24, 343-352.
5. Bushnell, P. J., Oshiro, W. M., Samsam, T. E., Benignus, V. A., Krantz, Q. T., and Kenyon, E. M. (2007a). A dosimetric analysis of the acute behavioral effects of inhaled toluene in rats. Toxicol. Sci. 99, 181-189.
6. Bushnell, P. J., Oshiro, W. M., Samsam, T. E., and Klinger, R. (2007b). The role of physical activity and feeding schedule on the kinetics of inhaled and oral toluene in rats. J. Toxicol. Environ. Health A 70, 1806-1814.
7. Campagna, D., Stengel, B., Mergler, D., Limasset, J. C., Diebold, F., Michard, D., and Huel, G. (2001). Color vision and occupational toluene exposure. Neurotoxicol. Teratol. 23, 473-480.
8. Chouaniere, D., Wild, P., Fontana, J. M., Hery, M., Fournier, M., Baudin, V., Subra, I., Rousselle, D., Toamain, J. P., Saurin, S., et al. (2002). Neurobehavioral disturbances arising from occupational toluene exposure. Am. J. Ind. Med. 41, 77-88.
9. Colvin, M., Myers, J., Nell, V., Rees, D., and Cronje, R. (1993). A cross-sectional survey of neurobehavioral effects of chronic solvent exposure on workers in a paint manufacturing plant. Environ. Res. 63, 122-132.
10. Copois, V., Bibeau, F., Bascoul-Mollevi, C., Salvetat, N., Chalbos, P., Bareil, C., Candeil, L., Fraslon, C., Conseiller, E., Granci, V., et al. (2007). Impact of RNA degradation on gene expression profiles: Assessment of different methods to reliably determine RNA quality. J. Biotechnol. 127, 549-559.
11. Crofton, K. M., Lassiter, T. L., and Rebert, C. S. (1994). Solvent-induced ototoxicity in rats: An atypical selective mid-frequency hearing deficit. Hear. Res. 80, 25-30.
12. Dai, M., Wang, P., Boyd, A. D., Kostov, G., Athey, B., Jones, E. G., Bunney, W. E., Myers, R. M., Speed, T. P., Akil, H., et al. (2005). Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175.
13. Di Domenico, F., Perluigi, M., Butterfield, D. A., Cornelius, C., and Calabrese, V. (2010). Oxidative damage in rat brain during aging: Interplay between energy and metabolic key target proteins. Neurochem. Res. 35, 2184-2192.
14. Dick, R. B., Setzer, J. V., Wait, R., Hayden, M. B., Taylor, B. J., Tolos, B., and Putz-Anderson, V. (1984). Effects of acute exposure of toluene and methyl ethyl ketone on psychomotor performance. Int. Arch. Occup. Environ. Health 54, 91-109.
15. Eller, N., Netterstrom, B., and Laursen, P. (1999). Risk of chronic effects on the central nervous system at low toluene exposure. Occup. Med. (Lond) 49, 389-395.
16. Filley, C. M., Halliday, W., and Kleinschmidt-DeMasters, B. K. (2004). The effects of toluene on the central nervous system. J. Neuropathol. Exp. Neurol. 63, 1-12.
17. Fleige, S., and Pfaffl, M. W. (2006). RNA integrity and the effect on the realtime qRT-PCR performance. Mol. Aspects Med. 27, 126-139.
18. Frenzel, M., Rommelspacher, H., Sugawa, M. D., and Dencher, N. A. (2010). Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp. Gerontol. 45, 563-572.
19. Gamberale, F., and Hultengren, M. (1972). Toluene exposure II. Psychophysiological functions. Scand. J. Work Environ. Health 9, 131-139.
20. Gelazonia, L., Japaridze, N., and Svanidze, I. (2006). Pyramidal cell loss in hippocampus of young rats exposed to toluene. Georgian Med. News 6, 126-128.
21. Gordon, C. J., Gottipolu, R. R., Kenyon, E. M., Thomas, R., Schladweiler, M. C., Mack, C. M., Shannahan, J. H., Wallenborn, J. G., Nyska, A., MacPhail, R. C., et al. (2010). Aging and susceptibility to toluene in rats: A pharmacokinetic, biomarker, and physiological approach. J. Toxicol. Environ. Health A 73, 301-318.
22. Gospe, S. M., Jr., and Al-Bayati, A. S. (1994). Comparison of oral and inhalation exposures to toluene. Int. J. Toxicol. 13, 21-32.
23. Gotohda, T., Tokunaga, I., Kubo, S., Kitamura, O., and Ishigami, A. (2002). Toluene inhalation induces glial cell line-derived neurotrophic factor, transforming growth factor and tumor necrosis factor in rat cerebellum. Leg. Med. (Tokyo) 4, 21-28.
24. Harbig, J., Sprinkle, R., and Enkemann, S. A. (2005). A sequence-based identification of the genes detected by probesets on the Affymetrix U133 plus 2.0 array. Nucleic Acids Res. 33, e31.
25. Hines, R. N., Sargent, D., Autrup, H., Birnbaum, L. S., Brent, R. L., Doerrer, N. G., Cohen Hubal, E. A., Juberg, D. R., Laurent, C., Luebke, R., et al. (2010). Approaches for assessing risks to sensitive populations: Lessons learned from evaluating risks in the pediatric population. Toxicol. Sci. 113, 4-26.
26. Honma, T., and Suda, M. (2004). Brain microdialysis study of the effects of hazardous chemicals on the central nervous system 2. Toluene exposure and cerebral acetylcholine. Ind. Health 42, 336-347.
27. Imbeaud, S., Graudens, E., Boulanger, V., Barlet, X., Zaborski, P., Eveno, E., Mueller, O., Schroeder, A., and Auffray, C. (2005). Towards standardization of RNA quality assessment using user-independent classifiers of microcapillary electrophoresis traces. Nucleic Acids Res. 33, e56.
28. Irizarry, R. A., Wu, Z., and Jaffee, H. A. (2006). Comparison of Affymetrix GeneChip expression measures. Bioinformatics 22, 789-794.
29. Kenyon, E. M., Benignus, V., Eklund, C., Highfill, J. W., Oshiro, W. M., Samsam, T. E., and Bushnell, P. J. (2008). Modeling the toxicokinetics of inhaled toluene in rats: Influence of physical activity and feeding status. J. Toxicol. Environ. Health A 71, 249-265.
30. Kilbride, S. M., Telford, J. E., and Davey, G. P. (2008). Age-related changes in H2O2 production and bioenergetics in rat brain synaptosomes. Biochim. Biophys. Acta 1777, 783-788.
31. Kodavanti, P. R., Royland, J. E., Richards, J. E., Besas, J., and Macphail, R. C. (2011). Toluene effects on oxidative stress in brain regions of young-adult, middle-age, and senescent Brown Norway rats. Toxicol. Appl. Pharmacol 256, 386-398.
32. Le Bel, C. P., and Schatz, R. A. (1988). Toluene-induced alterations in rat synaptosomal membrane composition and function. J. Biochem. Toxicol. 3, 279-293.
33. Lin, H. M., Liu, C. Y., Jow, G. M., and Tang, C. Y. (2009). Toluene disrupts synaptogenesis in cultured hippocampal neurons. Toxicol. Lett. 184, 90-96.
34. Liu, F., Yuan, R., Benashski, S. E., and McCullough, L. D. (2009). Changes in experimental stroke outcome across the life span. J. Cereb. Blood Flow Metab. 29, 792-802.
35. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402-408.
36. Lubman, D. I., Yucel, M., and Lawrence, A. J. (2008). Inhalant abuse among adolescents: Neurobiological considerations. Br. J. Pharmacol. 154, 316-326.
37. MacPhail, R. C., Farmer, J. D., and Jarema, K. A. (Forthcoming). Toluene effects on the motor activity of adolescent, young-adult, middle-age and senescent male Brown Norway rats. Neurotoxicology.
38. Mattia, C. J., Ali, S. F., and Bondy, S. C. (1993). Toluene-induced oxidative stress in several brain regions and other organs. Mol. Chem. Neuropathol. 18, 313-328.
39. Miyagawa, M., Honma, T., Sato, M., and Hasegawa, H. (1984). Effects of single exposure to toluene on operant behavior and brain toluene levels in rats. Ind. Health 22, 127-131.
40. Morata, T. C., Fiorini, A. C., Fischer, F. M., Colacioppo, S., Wallingford, K. M., Krieg, E. F., Dunn, D. E., Gozzoli, L., Padrao, M. A., and Cesar, C. L. (1997). Toluene-induced hearing loss among rotogravure printing workers. Scand. J. Work Environ. Health 23, 289-298.
41. Moser, V. C., and Balster, R. L. (1981). The effects of acute and repeated toluene exposure on operant behavior in mice. Neurobehav. Toxicol. Teratol. 3, 471-475.
42. National Resources Council (2011). National Institute of Health Guide for the Care and Use of Laboratory Animals, 8th ed. National Acadamies Press, Washington, DC.
43. Neubert, D., Bochert, G., Gericke, C., Hanke, B., and Beckmann, G. (2001). Multicenter field trial on possible health effects of toluene. I. Toluene body burdens in workers of the rotogravure industry. Toxicology 168, 139-157.
44. Perluigi, M., Di Domenico, F., Giorgi, A., Schinina, M. E., Coccia, R., Cini, C., Bellia, F., Cambria, M. T., Cornelius, C., Butterfield, D. A., et al. (2010). Redox proteomics in aging rat brain: Involvement of mitochondrial reduced glutathione status and mitochondrial protein oxidation in the aging process. J. Neurosci. Res. 88, 3498-3507.
45. Rebert, C. S., Matteucci, M. J., and Pryor, G. T. (1989). Multimodal effects of acute exposure to toluene evidenced by sensory-evoked potentials from Fischer 344 rats. Pharmacol. Biochem. Behav. 32, 757-768.
46. Riegel, A. C., and French, E. D. (1999). Acute toluene induces biphasic changes in rat spontaneous locomotor activity which are blocked by remoxipride. Pharmacol. Biochem. Behav. 62, 399-402.
47. Rowe, B. L., Toccalino, P. L., Moran, M. J., Zogorski, J. S., and Price, C. V. (2007). Occurrence and potential human-health relevance of volatile organic compounds in drinking water from domestic wells in the United States. Environ. Health Perspect. 115, 1539-1546.
48. Schiffer, W. K., Lee, D. E., Alexoff, D. L., Ferrieri, R., Brodie, J. D., and Dewey, S. L. (2006). Metabolic correlates of toluene abuse: Decline and recovery of function in adolescent animals. Psychopharmacology (Berl) 186, 159-167.
49. Schroeder, A., Mueller, O., Stocker, S., Salowsky, R., Leiber, M., Gassmann, M., Lightfoot, S., Menzel, W., Granzow, M., and Ragg, T. (2006). The RIN: An RNA integrity number for assigning integrity values to RNA measurements. BMC Mol. Biol. 7, 3.
50. Seo, J., and Hoffman, E. P. (2006). Probe set algorithms: Is there a rational best bet. BMC Bioinformatics 7, 395-402.
51. Slagboom, P. E., de Leeuw, W. J., and Vijg, J. (1990). Messenger RNA levels and methylation patterns of GAPDH and beta-actin genes in rat liver, spleen and brain in relation to aging. Mech. Ageing Dev. 53, 243-57.
52. Smyth, G. K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3.
53. Smyth, G. K. (2005). Limma: Linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor (V. C. R. Gentleman, S. Dudoit, R. Irizarry, and W. Huber, Eds.). pp. 397-420. Springer, New York, NY.
54. Storey, J. D. (2002). A direct approach to false discovery rates. J. R. Stat. Soc. Ser. B Stat. Methodol. 64, 479-498.
55. Storey, J. D., and Tibshirani, R. (2003). Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U.S.A. 100, 9440-9445.
56. Sullivan, M. J., and Conolly, R. B. (1988). Comparison of blood toluene levels after inhalation and oral administration. Environ. Res. 45, 64-70.
57. Thrall, K. D., Gies, R. A., Muniz, J., Woodstock, A. D., and Higgins, G. (2002). Route-of-entry and brain tissue partition coefficients for common superfund contaminants. J. Toxicol. Environ. Health A 65, 2075-2086.
58. Tukey, J. W., Ciminera, J. L., and Heyse, J. F. (1985). Testing the statistical certainty of a response to increasing doses of a drug. Biometrics 41, 295-301.
59. Waters, M., Boorman, G., Bushel, P., Cunningham, M., Irwin, R., Merrick, A., Olden, K., Paules, R., Selkirk, J., Stasiewicz, S., et al. (2003). Systems toxicology and the chemical effects in biological systems (CEBS) knowledge base. EHP Toxicogenomics 111, 15-28.
60. Wigle, D. T., Arbuckle, T. E., Walker, M., Wade, M. G., Liu, S., and Krewski, D. (2007). Environmental hazards: Evidence for effects on child health. J. Toxicol. Environ. Health B Crit. Rev. 10, 3-39.
61. Win-Shwe, T. T., Kunugita, N., Yoshida, Y., Nakajima, D., Tsukahara, S., and Fujimaki, H. (2012). Differential mRNA expression of neuromimmune markers in the hippocampus of infant mice following toluene exposure during brain developmental period. J. Appl. Toxicol. 32, 126-134.
62. Win-Shwe, T. T., Mitsushima, D., Nakajima, D., Ahmed, S., Yamamoto, S., Tsukahara, S., Kakeyama, M., Goto, S., and Fujimaki, H. (2007). Toluene induces rapid and reversible rise of hippocampal glutamate and taurine neurotransmitter levels in mice. Toxicol. Lett. 168, 75-82.
63. Wood, R. W., and Colotla, V. A. (1990). Biphasic changes in mouse motor activity during exposure to toluene. Fund. Appl. Toxicol. 14, 6-14.
64. Wood, R. W., and Cox, C. (1995). A repeated measures approach to the detection of the acute behavioral effects of toluene at low concentrations. Fund. Appl. Toxicol. 25, 293-301.
65. Wu, Z., Irizarry, R. A., Gentleman, R., Urillo, F. M., and Spencer, F. (2003). A model based background adjustment for oligonucleotide expression arrays. Technical Report. John Hopkins University, Department of Biostatistics Working Papers, Baltimore, MD.
66. Yucel, M., Takagi, M., Walterfang, M., and Lubman, D. I. (2008). Toluene misuse and long-term harms: A systematic review of the neuropsychological and neuroimaging literature. Neurosci. Biobehav. Rev. 32, 910-926.