Repeated developmental exposure of mice to chlorpyrifos oxon is associated with paraoxonase 1 (PON1)-modulated effects on cerebellar gene expression

Toxicological Sciences

Volumn 123, Issue 1, 2011, Pages 155-169

  Cole, Toby B ^a,b   Beyer, Richard P ^a   Bammler, Theo K ^a   Park, Sarah S ^a,b   Farin, Federico M ^a   Costa, Lucio G ^a   Furlong, Clement E ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Chlorpyrifos; Chlorpyrifos oxon; Microarrays; Neurotoxicity; Organophosphorus insecticides; Paraoxonase

Indexed keywords

ACETYLCHOLINESTERASE; ARYLDIALKYLPHOSPHATASE 1; CHLORPYRIFOS; CHLORPYRIFOS OXON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENOTYPE; HUMAN; IN VIVO STUDY; MALE; MOUSE; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; POSTNATAL DEVELOPMENT; PRENATAL EXPOSURE; PROTEIN POLYMORPHISM;

ACETYLCHOLINESTERASE; ANIMALS; ANIMALS, NEWBORN; ARYLDIALKYLPHOSPHATASE; BRAIN; CEREBELLUM; CHLORPYRIFOS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; HUMANS; INSECTICIDES; MALE; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER;

MUS;

EID: 80052498017     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr157     Document Type: Article

References (44)

1. Aldridge, J. E., Meyer, A., Seidler, F. J., and Slotkin, T. A. (2005). Alterations in central nervous system serotonergic and dopaminergic synaptic activity in adulthood after prenatal or neonatal chlorpyrifos exposure. Environ. Health Perspect. 113, 1027-1031.
2. Betancourt, A. M., Burgess, S. C., and Carr, R. L. (2006). Effect of developmental exposure to chlorpyrifos on the expression of neurotrophin growth factors and cell-specific markers in neonatal rat brain. Toxicol. Sci. 92, 500-506.
3. Brazma, A., Hingamp, P., Quackenbush, J., Sherlock, G., Spellman, P., Stoeckert, C., Aach, J., Ansorge, W., Ball, C. A., Causton, H. C., et al. (2001). Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat. Genet. 29, 365-371.
4. California Environmental Protection Agency (Cal-EPA), Air Resources Board. (1998). Report for the application and ambient air monitoring of chlorpyrifos (and the oxon analogue) in Tulare County during spring/ summer 1996. Projects No. C96-040 and C96-041:28 Cal-EPA, Sacramento, CA.
5. Camon, E., Magrane, M., Barrell, D., Lee, V., Dimmer, E., Maslen, J., Binns, D., Harte, N., Lopez, R., and Apweiler, R. (2004). The Gene Ontology Annotation (GOA) database: sharing knowledge in Uniprot with Gene Ontology. Nucleic Acids Res. 32, D262-D266.
6. Chambers, H., Brown, B., and Chambers, J. E. (1990). Noncatalytic detoxication of 6 organophosphorus compounds by rat-liver homogenates. Pestic. Biochem. Physiol. 36, 308-315.
7. Cole, T. B., Jampsa, R. L., Walter, B. J., Arndt, T. L., Richter, R. J., Shih, D. M., Tward, A., Lusis, A. J., Jack, R. M., Costa, L. G., et al. (2003). Expression of human paraoxonase (PON1) during development. Pharmacogenetics 13, 357-364.
8. Cole, T. B., Walter, B. J., Shih, D. M., Tward, A. D., Lusis, A. J., Timchalk, C., Richter, R. J., Costa, L. G., and Furlong, C. E. (2005). Toxicity of chlorpyrifos and chlorpyrifos oxon in a transgenic mouse model of the human paraoxonase (PON1) Q192R polymorphism. Pharmacogenet. Genomics 15, 589-598.
9. Efron, B., and Tibshirani, R. (2007). On testing the significance of sets of genes. Ann. Appl. Stat. 1, 107-129.
10. Fenske, R. A., Lu, C., Curl, C. L., Shirai, J. H., and Kissel, J. C. (2005). Biologic monitoring to characterize organophosphorus pesticide exposure among children and workers: an analysis of recent studies in Washington State. Environ. Health Perspect. 113, 1651-1657.
11. Furlong, C. E. (2008). The Bert La Du Memorial Lecture: Paraoxonases: an historical perspective. In: The Paraoxonases: Their Role in Disease, Development and Xenobiotic Metabolism (M. M. B. Mackness, M. Aviram, and G. Paragh, Eds.), pp. 3-31. Springer, Dordrecht, The Netherlands.
12. Furlong, C. E., Holland, N., Richter, R. J., Bradman, A., Ho, A., and Eskenazi, B. (2006). PON1 status of farmworker mothers and children as a predictor of organophosphate sensitivity. Pharmacogenet. Genomics 16, 183-190.
13. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
14. Heudorf, U., Butte, W., Schulz, C., and Angerer, J. (2006). Reference values for metabolites of pyrethroid and organophosphorous insecticides in urine for human biomonitoring in environmental medicine. Int. J. Hyg. Environ. Health 209, 293-299.
15. Hofmann, J. N., Keifer, M. C., Furlong, C. E., De Roos, A. J., Farin, F. M., Fenske, R. A., van Belle, G., and Checkoway, H. (2009). Serum cholinesterase inhibition in relation to paraoxonase-1 (PON1) status among organophosphate-exposed agricultural pesticide handlers. Environ. Health Perspect. 117, 1402-1408.
16. Huen, K., Harley, K., Brooks, J., Hubbard, A., Bradman, A., Eskenazi, B., and Holland, N. (2009). Developmental changes in PON1 enzyme activity in young children and effects of PON1 polymorphisms. Environ. Health Perspect. 117, 1632-1638.
17. Huff, R. A., Corcoran, J. J., Anderson, J. K., and Abou-Donia, M. B. (1994). Chlorpyrifos oxon binds directly to muscarinic receptors and inhibits cAMP accumulation in rat striatum. J. Pharmacol. Exp. Ther. 269, 329-335.
18. Jameson, R. R., Seidler, F. J., and Slotkin, T. A. (2007). Nonenzymatic functions of acetylcholinesterase splice variants in the developmental neurotoxicity of organophosphates: chlorpyrifos, chlorpyrifos oxon, and diazinon. Environ. Health Perspect. 115, 65-70.
19. Jansen, K. L., Cole, T. B., Park, S. S., Furlong, C. E., and Costa, L. G. (2009). Paraoxonase 1 (PON1) modulates the toxicity of mixed organophosphorus compounds. Toxicol. Appl. Pharmacol. 236, 142-153.
20. Lee, B. W., London, L., Paulauskis, J., Myers, J., and Christiani, D. C. (2003). Association between human paraoxonase gene polymorphism and chronic symptoms in pesticide-exposed workers. J. Occup. Environ. Med. 45, 118-122.
21. Li, W. F., Costa, L. G., Richter, R. J., Hagen, T., Shih, D. M., Tward, A., Lusis, A. J., and Furlong, C. E. (2000). Catalytic efficiency determines the in-vivo efficacy of PON1 for detoxifying organophosphorus compounds. Pharmacogenetics 10, 767-779.
22. Lotti, M., Moretto, A., Zoppellari, R., Dainese, R., Rizzuto, N., and Barusco, G. (1986). Inhibition of lymphocytic neuropathy target esterase predicts the development of organophosphate-induced delayed polyneuropathy. Arch. Toxicol. 59, 176-179.
23. Mense, S. M., Sengupta, A., Lan, C., Zhou, M., Bentsman, G., Volsky, D. J., Whyatt, R. M., Perera, F. P., and Zhang, L. (2006). The common insecticides cyfluthrin and chlorpyrifos alter the expression of a subset of genes with diverse functions in primary human astrocytes. Toxicol. Sci. 93, 125-135.
24. Moreira, E. G., Yu, X., Robinson, J. F., Griffith, W., Hong, S. W., Beyer, R. P., Bammler, T. K., and Faustman, E. M. (2010). Toxicogenomic profiling in maternal and fetal rodent brains following gestational exposure to chlorpyrifos. Toxicol. Appl. Pharmacol. 245, 310-325.
25. Nolan, R. J., Rick, D. L., Freshour, N. L., and Saunders, J. H. (1984). Chlorpyrifos: pharmacokinetics in human volunteers. Toxicol. Appl. Pharmacol. 73, 8-15.
26. Perez-Herrera, N., Polanco-Minaya, H., Salazar-Arredondo, E., Solis-Heredia, M. J., Hernandez-Ochoa, I., Rojas-Garcia, E., Alvarado-Mejia, J., Borja-Aburto, V. H., and Quintanilla-Vega, B. (2008). PON1Q192R genetic polymorphism modifies organophosphorous pesticide effects on semen quality and DNA integrity in agricultural workers from southern Mexico. Toxicol. Appl. Pharmacol. 230, 261-268.
27. Pope, C. N. (1999). Organophosphorus pesticides: do they all have the same mechanism of toxicity? J. Toxicol. Environ. Health B Crit. Rev. 2, 161-181.
28. Richter, R. J., and Furlong, C. E. (1999). Determination of paraoxonase (PON1) status requires more than genotyping. Pharmacogenetics 9, 745-753.
29. Richter, R. J., Jarvik, G. P., and Furlong, C. E. (2008). Determination of paraoxonase 1 status without the use of toxic organophosphate substrates. Circ. Cardiovasc. Genet. 1, 147-152.
30. Salazar-Arredondo, E., de Jesus Solis-Heredia, M., Rojas-Garcia, E., Hernandez-Ochoa, I., and Quintanilla-Vega, B. (2008). Sperm chromatin alteration and DNA damage by methyl-parathion, chlorpyrifos and diazinon and their oxon metabolites in human spermatozoa. Reprod. Toxicol. 25, 455-460.
31. Schuh, R. A., Lein, P. J., Beckles, R. A., and Jett, D. A. (2002). Noncholinesterase mechanisms of chlorpyrifos neurotoxicity: altered phosphorylation of Ca2+/cAMP response element binding protein in cultured neurons. Toxicol. Appl. Pharmacol. 182, 176-185.
32. Shenouda, J., Green, P., and Sultatos, L. (2009). An evaluation of the inhibition of human butyrylcholinesterase and acetylcholinesterase by the organophosphate chlorpyrifos oxon. Toxicol. Appl. Pharmacol. 241, 135-142.
33. Shih, D. M., Gu, L., Xia, Y. R., Navab, M., Li, W. F., Hama, S., Castellani, L. W., Furlong, C. E., Costa, L. G., Fogelman, A. M., et al. (1998). Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394, 284-287.
34. Slotkin, T. A., and Seidler, F. J. (2007). Comparative developmental neurotoxicity of organophosphates in vivo: transcriptional responses of pathways for brain cell development, cell signaling, cytotoxicity and neurotransmitter systems. Brain Res. Bull. 72, 232-274.
35. Slotkin, T., and Seidler, F. (2009). Transcriptional profiles reveal similarities and differences in the effects of developmental neurotoxicants on differentiation into neurotransmitter phenotypes in PC12 cells. Brain Res. Bull. 78, 211-225.
36. Smyth, G. K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 1-25.
37. Stapleton, A. R., and Chan, V. T. (2009). Subtoxic chlorpyrifos treatment resulted in differential expression of genes implicated in neurological functions and development. Arch. Toxicol. 83, 319-333.
38. Stevens, R. C., Suzuki, S. M., Cole, T. B., Park, S. S., Richter, R. J., and Furlong, C. E. (2008). Engineered recombinant human paraoxonase 1 (rHuPON1) purified from Escherichia coli protects against organophosphate poisoning. Proc. Natl. Acad. Sci. U.S.A. 105, 12780-12784.
39. Storey, J. D., and Tibshirani, R. (2003). Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U.S.A. 100, 9440-9445.
40. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550.
41. Udarbe Zamora, E. M., Liu, J., and Pope, C. N. (2008). Effects of chlorpyrifos oxon on M2 muscarinic receptor internalization in different cell types. J. Toxicol. Environ. Health A. 71, 1440-1447.
42. Vidal, J. L. M., Gonzalez, F. J. E., Galera, M. M., and Cano, M. L. C. (1998). Diminution of chlorpyrifos and chlorpyrifos oxon in tomatoes and green beans grown in greenhouses. J. Agric. Food Chem. 46, 1440-1444.
43. Whitney, K. D., Seidler, F. J., and Slotkin, T. A. (1995). Developmental neurotoxicity of chlorpyrifos: cellular mechanisms. Toxicol. Appl. Pharmacol. 134, 53-62.
44. Yuknavage, K. L., Fenske, R. A., Kalman, D. A., Keifer, M. C., and Furlong, C. E. (1997). Simulated dermal contamination with capillary samples and field cholinesterase biomonitoring. J. Toxicol. Environ. Health 51, 35-55.