Mass spectrometric analyses of organophosphate insecticide oxon protein adducts

Environmental Health Perspectives

Volumn 118, Issue 1, 2010, Pages 11-19

  Thompson, Charles M ^a   Prins, John M ^a   George, Kathleen M ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

Acetylcholinesterase; Adduct; Butyrylcholinesterase; Insecticide; Mass spectrometry; Organophosphate; Organophosphorus; Peptide; Protein

Indexed keywords

AMINO ACID; BIOLOGICAL MARKER; CHOLINESTERASE; ORGANOPHOSPHATE INSECTICIDE; PROTEIN;

CHEMICAL BOND; CHEMICAL REACTION; CHEMICAL STRUCTURE; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVE SITE; HEALTH HAZARD; HUMAN; MASS SPECTROMETRY; MEDLINE; MOLECULAR PROBE; MOLECULAR WEIGHT; NONHUMAN; PREDICTOR VARIABLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; CHOLINESTERASES; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLLUTANTS; HUMANS; INSECTICIDES; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; ORGANOPHOSPHORUS COMPOUNDS; PROTEINS;

HEXAPODA;

EID: 77149136393     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.0900824     Document Type: Review

References (112)

1. Aardema MJ, MacGregor JT. 2002. Toxicology and genetic toxicology in the new era of "toxicogenomics": impact of "-omics" technologies. Mutat Res 499:13-25.
2. Adam GC, Cravatt BF, Sorensen EJ. 2001. Profiling the specific reactivity of the proteome with non-directed activity-based probes. Chem Biol 8:81-95.
3. Adam GC, Sorensen EJ, Cravatt BF. 2002. Trifunctional chemical probes for the consolidated detection and identification of enzyme activities from complex proteomes. Mol Cell Proteomics 1:828-835.
4. Adamczyk M, Gebler JC, Wu J. 2001. Selective analysis of phosphopeptides within a protein mixture by chemical modification, reversible biotinylation and mass spectrometry. Rapid Commun Mass Spectrom 15:1481-1488.
5. Albuquerque EX, Aracava Y, Cintra WM, Brossi A, Schonenberger B, Deshpande SS. 1988. Structure-activity relationship of reversible cholinesterase inhibitors: activation, channel blockade and stereospecificity of the nicotinic acetylcholine receptor-ion channel complex. Braz J Med Biol Res 21:1173-1196.
6. Arima H, Sobue K, So M, Morishima T, Ando H, Katsuya H. 2003. Transient and reversible parkinsonism after acute organophosphate poisoning. J Toxicol Clin Toxicol 41:67-70.
7. Ashani Y, Gentry MK, Doctor BP. 1990. Differences in conformational stabilty between native and phosphorylated acetylcholinesterase as evidenced by a monoclonal antibody. Biochemistry 29:2456-2463.
8. Ashani Y, Leader H, Rothschild N, Dosoretz C. 1998. Combined effect of organophosphorus hydrolase and oxime on the reactivation rate of diethylphosphoryl-acetylcholinesterase conjugates. Biochem Pharmacol 55:159-168.
9. Ashani Y, Radic Z, Tsigelny I, Vellom DC, Pickering NA, Quinn DM, et al. 1995. Amino acid residues controlling reactivation of organophosphonyl conjugates of acetylcholinesterase by mono- and bisquaternary oximes. J Biol Chem 270:6370-6380.
10. Ballantyne B, Marrs T. 1992. Clinical and Experimental Toxicology of Organophosphates and Carbamates. Boston:Butterworth Heinemann.
11. Barak R, Ordentlich A, Barak D, Fischer M, Benschop HP, De Jong LPA, et al. 1997. Direct determination of the chemical composition of acetylcholinesterase phos phonylation products utilizing electrospray-ionization mass spectrometry. FEBS Lett 407:347-352.
12. Barr DB, Allen R, Olsson AO, Bravo R, Caltabiano LM, Montesano A, et al. 2005. Concentrations of selective metabolites of organophosphorus pesticides in the United States population. Environ Res 99:314-326.
13. Bennett KL, Stensballe A, Podtelejnikov AV, Moniatte M, Jensen ON. 2002. Phosphopeptide detection and sequencing by matrix-assisted laser desorption/ionization quadru pole time-of-flight tandem mass spectrometry. J Mass Spectrom 37:179-190.
14. Berkman CE, Quinn DA, Thompson CM. 1993a. Interaction of acetylcholinesterase with the enantiomers of malaoxon and isomalathion. Chem Res Toxicol 6:724-730.
15. Berkman CE, Ryu S, Quinn DA, Thompson CM. 1993b. Kinetics of the postinhibitory reactions of acetylcholinesterase poisoned by chiral isomalathion: a surprising nonreactivation induced by the RP stereoisomers. Chem Res Toxicol 6:28-32.
16. Berkman CE, Thompson CM, Perrin SR. 1993c. Synthesis, absolute configuration, and analysis of malathion, malaoxon, and isomalathion enantiomers. Chem Res Toxicol 6:718-723.
17. Bomser J, Casida JE. 2000. Activation of extracellular signal-regulated kinases (ERK 44/42) by chlorpyrifos oxon in Chinese hamster ovary cells. J Biochem Mol Toxicol 14:346-353.
18. Bomser JA, Casida JE. 2001. Diethylphosphorylation of rat cardiac M2 muscarinic receptor by chlorpyrifos oxon in vitro. Toxicol Lett 119:21-26.
19. Bomser JA, Quistad GB, Casida JE. 2002. Chlorpyrifos oxon potentiates diacylglycerol-induced extracellular signal-regulated kinase (ERK 44/42) activation, possibly by diacylglycerol lipase inhibition. Toxicol Appl Pharmacol 178:29-36.
20. Bronstein AC, Spyker DA, Cantilena LR Jr, Green JL, Rumack BH, Heard SE. 2008. 2007 Annual report of the American Association of Poison Control Centers' National Poison Data System (NPDS): 25th annual report. Clin Toxicol (Phila) 46:927-1057.
21. Broomfield CA, Millard CB, Lockridge O, Caviston TL. 1995. Enzymes of the Cholinesterase Family. New York:Plenum Press.
22. Casida JE, Quistad GB. 2005. Serine hydrolase targets of organophosphorus toxicants. Chem Biol Interact 157-158:277-283.
23. Centers for Disease Control and Prevention. 2005. Third National Report on Human Exposure to Environmental Chemicals. Available: http://www.cdc.gov/ exposurereport/pdf/thirdreport.pdf [accessed 17 November 2009].
24. Claudio L, Kwa WC, Russell AL, Wallinga D. 2000. Testing methods for developmental neurotoxicity of environmental chemicals. Toxicol Appl Pharmacol 164:1-14.
25. Corrigan FM, MacDonald S, Brown A, Armstrong K, Armstrong EM. 1994. Neurasthenic fatigue, chemical sensitivity and GABAa receptor toxins. Med Hypotheses 43:195-200.
26. Costa LG. 1998. Neurotoxicity testing: a discussion of in vitro alternatives. Environ Health Perspect 106(suppl 2):505-510.
27. Costa LG. 2006. Current issues in organophosphate toxicology. Clin Chim Acta 366:1-13.
28. Costa LG, Cole TB, Vitalone A, Furlong CE. 2005. Measurement of paraoxonase (PON1) status as a potential biomarker of susceptibility to organophosphate toxicity. Clin Chim Acta 352:37-47.
29. Costa LG, Richter RJ, Li WF, Cole T, Guizzetti M, Furlong CE. 2003. Paraoxonase (PON 1) as a biomarker of susceptibility for organophosphate toxicity. Biomarkers 8:1-12.
30. Dahlgren JG, Takhar HS, Ruffalo CA, Zwass M. 2004. Health effects of diazinon on a family. J Toxicol Clin Toxicol 42:579-591.
31. Ding SJ, Carr J, Carlson JE, Tong L, Xue W, Li Y, et al. 2008. Five tyrosines and two serines in human albumin are labeled by the organophosphorus agent FP-biotin. Chem Res Toxicol 21:1787-1794.
32. Doorn JA, Gage DA, Schall M, Talley TT, Thompson CM, Richardson RJ. 2000. Inhibition of acetylcholinesterase by (1S,3S)-isomalathion proceeds with loss of thiomethyl: kinetic and mass spectral evidence for an unexpected primary leaving group. Chem Res Toxicol 13:1313-1320.
33. Doorn JA, Schall M, Gage DA, Talley TT, Thompson CM, Richardson RJ. 2001a. Identification of butyrylcholinesterase adducts after inhibition with isomalathion using mass spectrometry: difference in mechanism between (1R)- and (1S)-stereoisomers. Toxicol Appl Pharmacol 176:73-80.
34. Doorn JA, Talley TT, Thompson CM, Richardson RJ. 2001b. Probing the active sites of butyrylcholinesterase and cholesterol esterase with isomalathion: conserved stereo selective inactivation of serine hydrolases structurally related to acetyl cholinesterase. Chem Res Toxicol 14:807-813.
35. Ehrich M, Intropido L, Costa LG. 1994. Interaction of organophosphorus compounds with muscarinic receptors in SH-SY5Y human neuroblastoma cells. J Toxicol Environ Health 43:51-63.
36. Eldefrawi ME, Eldefrawi AT. 1983. Neurotransmitter receptors as targets for pesticides. J Environ Sci Health B 18:65-88.
37. Elhanany E, Ordentlich A, Dgany O, Kaplan D, Segall Y, Barak R, et al. 2001. Resolving pathways of interaction of covalent inhibitors with the active site of acetylcholinesterases: MALDI-TOF/MS analysis of various nerve agent phosphyl adducts. Chem Res Toxicol 14:912-918.
38. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95.
39. Eskenazi B, Marks AR, Bradman A, Harley K, Barr DB, Johnson C, et al. 2007. Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ Health Perspect 115:792-798.
40. Eto M. 1974. Organophosphorus Pesticides; Organic and Biological Chemistry. Cleveland, OH:CRC Press.
41. Fenske RA, Kissel JC, Lu C, Kalman DA, Simcox NJ, Allen EH, et al. 2000. Biologically based pesticide dose estimates for children in an agricultural community. Environ Health Perspect 108:515-520.
42. Fest C, Schmidt KJ. 1973. The Chemistry of Organophosphorus Pesticides; Reactivity, Synthesis, Mode of Action, Toxicology. New York:Springer Verlag.
43. Fukuto TR. 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245-254.
44. Godovac-Zimmermann J, Soskic V, Poznanovic S, Brianza F. 1999. Functional proteomics of signal transduction by membrane receptors. Electrophoresis 20:952-961.
45. Goldman LR, Koduru S. 2000. Chemicals in the environment and developmental toxicity to children: a public health and policy perspective. Environ Health Perspect 108(suppl 3):443-448.
46. Gordon C. 1993. Acute and delayed effects of diisopropyl fluorophosphate on body temperature, heart rate, and motor activity in the awake, unrestrained rat. J Toxic Environ Health 39:247-260.
47. Grigoryan H, Schopfer LM, Thompson CM, Terry AV, Masson P, Lockridge O. 2008. Mass spectrometry identifies covalent binding of soman, sarin, chlorpyrifos oxon, diisopropyl fluoro phosphate, and FP-biotin to tyrosines on tubulin: a potential mechanism of long term toxicity by organophosphorus agents. Chem Biol Interact 175:180-186.
48. Haas R, Jackson B, Reinhold B, Foster J, Rosenberry T. 1996. Glycoinositol phospholipid anchor and protein C-terminus of bovine erythrocyte acetylcholinesterase: analysis by mass spectrometry and by protein and DNA sequencing. Biochem J 314:817-825.
49. Haas R, Rosenberry T. 1995. Protein denaturation by addition and removal of acetonitrile: application to tryptic digestion of acetylcholinesterase. Anal Biochem 224:425-427.
50. Harel M, Su CT, Frolow F, Ashani Y, Silman I, Sussman JL. 1991. Refined crystal structures of "aged" and "non-aged" organophosphoryl conjugates of gamma-chymotrypsin. J Mol Biol 221:909-918.
51. Huff RA, Corcoran JJ, Anderson JK, Abou-Donia MB. 1994. Chlorpyrifos oxon binds directly to muscarinic receptors and inhibits cAMP accumulation in rat striatum. J Pharmacol Exp Ther 269:329-335.
52. Jacobson SW, Jacobson JL. 2006. New evidence of effects of organophosphate pesticides on neurodevelopment in children: commentary on the article by Kofman et al. on page 88. Pediatr Res 60:22-23.
53. Jayawardane P, Dawson AH, Weerasinghe V, Karalliedde L, Buckley NA, Senanayake N. 2008. The spectrum of intermediate syndrome following acute organophosphate poisoning: a prospective cohort study from Sri Lanka. PLoS Med 5:e147; doi:10.1371/journal.pmed.0050147 [Online 15 July 2008].
54. Jennings LL, Malecki M, Komives EA, Taylor P. 2003. Direct analysis of the kinetic profiles of organophosphate-acetylcholinesterase adducts by MALDI-TOF mass spectrometry. Biochemistry 42:11083-11091.
55. Jiang X, Wang Y. 2004. Beta-elimination coupled with tandem mass spectrometry for the identification of in vivo and in vitro phosphorylation sites in maize dehydrin DHN1 protein. Biochemistry 43:15567-15576.
56. Johal MS, Sharma ML, Ravneet. 2007. Impact of low dose of organophosphate, monocrotophos on the epithelial cells of gills of Cyprinus carpio communis Linn. - SEM study. J Environ Biol 28:663-667.
57. Katz L, Marquis J. 1992. Organophosphate-induced alteration in muscarinic receptor binding and phosphoinositide hydrolysis in the human SK-N-SH cell line. Neurotoxicology 13:365-378.
58. Kidd D, Liu Y, Cravatt BF. 2001. Profiling serine hydrolase activities in complex proteomes. Biochemistry 40:4005-4015.
59. Kofman O, Berger A, Massarwa A, Friedman A, Jaffar AA. 2006. Motor inhibition and learning impairments in school-aged children following exposure to organophosphate pesticides in infancy. Pediatr Res 60:88-92.
60. Langenberg JP, De Jong LP, Otto MF, Benschop HP. 1988. Spontaneous and oxime-induced reactivation of acetylcholinesterase inhibited by phosphoramidates. Arch Toxicol 62:305-310.
61. Lanks KW, Seleznick MJ. 1981. Spontaneously reactivation of acetylcholinesterase inhibited by diisopropylfluorophosphate. Biochim Biophys Acta 660:91-95.
62. Larsen MR, Sørensen GL, Fey SJ, Larsen PM, Roepstorff P. 2001. Phospho-proteomics: evaluation of the use of enzymatic de-phosphorylation and differential mass spectrometric peptide mass mapping for site specific phosphorylation assignment in proteins separated by gel electrophoresis. Proteomics 1:223-238.
63. Li Y, Li M, Xing G, Hu Z, Wang Q, Dong C, et al. 2000a. Stimulation of the mitogen-activated protein kinase cascade and tyrosine phosphorylation of the epidermal growth factor receptor by hepatopoietin. J Biol Chem 275:37443-37447.
64. Li Y, Liu L, Kang J, Sheng JG, Barger SW, Mrak RE, et al. 2000b. Neuronal-glial interactions mediated by inter leukin-1 enhance neuronal acetylcholinesterase activity and mRNA expression. J Neurosci 20:149-155.
65. Liu Y, Patricelli MP, Cravatt BF. 1999. Activity-based protein profiling: the serine hydrolases. Proc Natl Acad Sci USA 96:14694-14699.
66. Lockridge O, Masson P. 2000. Pesticides and susceptible populations: people with butyrylcholinesterase genetic variants may be at risk. Neurotoxicology 21:113-126.
67. Lotti M, Becker CE, Aminoff MJ. 1984. Organophosphate polyneuropathy: pathogenesis and prevention. Neurology 34:658-662.
68. Menzies GW, MacConnell CB. 1998. Integrated Pest Management for Raspberries: A Guide for Sampling and Decision-Making for Key Raspberry Pests in Northwest Washington. Available: http://whatcom.wsu.edu/ag/comhort/nooksack/ ipmweb/Pesticideselection.html [accessed 17 November 2009].
69. Murray A, Rathbone A, Ray D. 2005. Novel protein targets for organophosphorus pesticides in rat brain. Environ Toxicol Pharmacol 19:451-454.
70. National Center for Biotechnology Information. 2009. PubMed. Available: http://www.ncbi.nlm.nih.gov/pubmed/ [accessed 17 November 2009].
71. Niven AS, Roop SA. 2004. Inhalational exposure to nerve agents. Respir Care Clin N Am 10:59-74.
72. Nomura DK, Durkin KA, Chiang KP, Quistad GB, Cravatt BF, Casida JE. 2006. Serine hydrolase KIAA1363: toxicological and structural features with emphasis on organophosphate interactions. Chem Res Toxicol 19:1142-1150.
73. Noort D, Fidder A, van der Schans MJ, Hulst AG. 2006. Verification of exposure to organophosphates: generic mass spectrometric method for detection of human butyrylcholinesterase adducts. Anal Chem 78:6640-6644.
74. Pala I, Vig PJ, Desaiah D, Srinivasan A. 1991. In vitro effects of organophosphorus compounds on calmodulin activity. J Appl Toxicol 11:391-395.
75. Peeples ES, Schopfer LM, Duysen EG, Spaulding R, Voelker T, Thompson CM, et al. 2005. Albumin, a new biomarker of organophosphorus toxicant exposure, identified by mass spectrometry. Toxicol Sci 83:303-312.
76. Qian WJ, Goshe MB, Camp DG II, Yu LR, Tang K, Smith RD. 2003. Phosphoprotein isotope-coded solid-phase tag approach for enrichment and quantitative analysis of phosphopeptides from complex mixtures. Anal Chem 75:5441-5450.
77. Quistad GB, Casida JE. 2000. Sensitivity of blood-clotting factors and digestive enzymes to inhibition by organophosphorus pesticides. J Biochem Mol Toxicol 14:51-56.
78. Quistad GB, Sparks SE, Casida JE. 2001. Fatty acid amide hydrolase inhibition by neurotoxic organophosphorus pesticides. Toxicol Appl Pharmacol 173:48-55.
79. Quistad GB, Zhang N, Sparks SE, Casida JE. 2000. Phosphoacetyl cholinesterase: toxicity of phosphorus oxychloride to mammals and insects that can be attributed to selective phosphorylation of acetylcholinesterase by phosphorodichloridic acid. Chem Res Toxicol 13:652-657.
80. Richards P, Johnson M, Ray D, Walker C. 1999. Novel protein targets for organophosphorus compounds. Chem Biol Interact 119-120:503-511.
81. Roberts WL, Santikarn S, Reinhold VN, Rosenberry TL. 1988. Structural characterization of the glycoinositol phospho lipid membrane anchor of human erythrocyte acetyl cholinesterase by fast atom bombardment mass spectrometry. J Biol Chem 263:18776-18784.
82. Rowsey PJ, Gordon CJ. 1999. Tumor necrosis factor is involved in chlorpyrifos-induced changes in core temperature in the female rat. Toxicol Lett 109:51-59.
83. Schopfer LM, Champion MM, Tamblyn N, Thompson CM, Lockridge O. 2005a. Characteristic mass spectral fragments of the organophosphorus agent FP-biotin and FP-biotinylated peptides from trypsin and bovine albumin (Tyr410). Anal Biochem 345:122-132.
84. Schopfer LM, Voelker T, Bartels CF, Thompson CM, Lockridge O. 2005b. Reaction kinetics of biotinylated organophosphorus toxicant, FP-biotin, with human acetyl cholinesterase and human butyrylcholinesterase. Chem Res Toxicol 18:747-754.
85. Schuh RA, Lein PJ, Beckles RA, Jett DA. 2002. Noncholinesterase mechanisms of chlorpyrifos neurotoxicity: altered phosphorylation of Ca2+/cAMP response element binding protein in cultured neurons. Toxicol Appl Pharmacol 182:176-185.
86. Sickmann A, Meyer HE. 2001. Phosphoamino acid analysis. Proteomics 1:200-206.
87. Slotkin TA. 2004. Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol Appl Pharmacol 198:132-151.
88. Slotkin TA, Ryde IT, Levin ED, Seidler FJ. 2008. Developmental neurotoxicity of low dose diazinon exposure of neonatal rats: effects on serotonin systems in adolescence and adulthood. Brain Res Bull 75:640-647.
89. Solomon C, Poole J, Palmer KT, Peveler R, Coggon D. 2007. Acute symptoms following work with pesticides. Occup Med (Lond) 57:505-511.
90. Spaulding RS, George KM, Thompson CM. 2006. Analysis and sequencing of the active-site peptide from native and organophosphate-inactivated acetylcholinesterase by electrospray ionization, quadrupole/time-of-flight (QTOF) mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 830:105-113.
91. Stephens R, Spurgeon A, Calvert IA, Beach J, Levy LS, Berry H, et al. 1995. Neuropsychological effects of long-term exposure to organophosphates in sheep dip. Lancet 345:1135-1139.
92. Sudakin DL, Power LE. 2007. Organophosphate exposures in the United States: a longitudinal analysis of incidents reported to poison centers. J Toxicol Environ Health A 70:141-147.
93. Sultatos LG. 1994. Mammalian toxicology of organophosphorus pesticides. J Toxicol Environ Health 43:271-289.
94. Swiss Institute of Bioinformatics. 2007. PeptideCutter. Available: http://www.expasy.org/tools/peptidecutter/ [accessed 17 November 2009].
95. Thaler F, Valsasina B, Baldi R, Xie J, Stewart A, Isacchi A, et al. 2003. A new approach to phosphoserine and phosphothreonine analysis in peptides and proteins: chemical modification, enrichment via solid-phase reversible binding, and analysis by mass spectrometry. Anal Bioanal Chem 376:366-373.
96. Thompson CM, Fukuto TR. 1982. Mechanism of cholinesterase inhibition by methamidophos. J Agric Food Chem 30:282-284.
97. Timofeeva OA, Roegge CS, Seidler FJ, Slotkin TA, Levin ED. 2008. Persistent cognitive alterations in rats after early postnatal exposure to low doses of the organophosphate pesticide, diazinon. Neurotoxicol Teratol 30:38-45.
98. Tseng HC, Ovaa H, Wei NJ, Ploegh H, Tsai LH. 2005. Phosphoproteomic analysis with a solid-phase capture-release-tag approach. Chem Biol 12:769-777.
99. U.S. EPA. 2006. Organophosphorus Cumulative Risk Assessment (2006 Update). EPA-HQ-OPP-2006-0618-0002. Washington, DC:U.S. Environmental Protection Agency. Available: http://www.regulations.gov/search/Regs/home. html#documentDetail?R=09000064801ac312 [accessed 17 November 2009].
100. van den Beukel I, van Kleef RG, Oortgiesen M. 1998. Differential effects of physostigmine and organophosphates on nicotinic receptors in neuronal cells of different species. Neurotoxicology 19:777-787.
101. Ward TR, Ferris DJ, Tilson HA, Mundy WR. 1993. Correlation of the anticholinesterase activity of a series of organophosphates with their ability to compete with agonist binding to muscarinic receptors. Toxicol Appl Pharmacol 122:300-307.
102. Ward TR, Mundy WR. 1996. Organophosphorus compounds preferentially affect second messenger systems coupled to M2/M4 receptors in rat frontal cortex. Brain Res Bull 39:49-55.
103. Whyatt RM, Camann D, Perera FP, Rauh VA, Tang D, Kinney PL, et al. 2005. Biomarkers in assessing residential insecticide exposures during pregnancy and effects on fetal growth. Toxicol Appl Pharmacol 206:246-254.
104. Whyatt RM, Rauh V, Barr DB, Camann DE, Andrews HF, Garfinkel R, et al. 2004. Prenatal insecticide exposures and birth weight and length among an urban minority cohort. Environ Health Perspect 112:1125-1132.
105. Wieseler S, Schopfer L, Lockridge O. 2006. Markers of organophosphate exposure in human serum. J Mol Neurosci 30:93-94.
106. Wilson BW, Henderson JD. 1992. Blood esterase determinations as markers of exposure. Rev Environ Contam Toxicol 128:55-69.
107. Wilson BW, Hooper MJ, Hansen ME, Nieberg PS. 1992. Reactivation of organophosphorus inhibited AChE with oximes. In: Organophosphates: Chemistry, Fate, and Effects (Chambers JE, Levi PE, eds). San Diego, CA:Academic Press, 107-137.
108. Wilson BW, Padilla S, Henderson JD, Brimijoin S, Dass PD, Elliot G, et al. 1996. Factors in standardizing automated cholinesterase assays. J Toxicol Environ Health 48:187-195.
109. Yanagisawa N, Morita H, Nakajima T. 2006. Sarin experiences in Japan: acute toxicity and long-term effects. J Neurol Sci 249:76-85.
110. Young JG, Eskenazi B, Gladstone EA, Bradman A, Pedersen L, Johnson C, et al. 2005. Association between in utero organophosphate pesticide exposure and abnormal reflexes in neonates. Neurotoxicology 26:199-209.
111. Zaim M, Jambulingam P. 2007. Global Insecticide Use for Vector-Borne Disease Control. Geneva:World Health Organization. Available: http://whqlibdoc.who.int/HQ/2007/WHO-CDS-NTD-WHOPES-GCDPP-2007.2-eng.pdf [accessed 17 November 2009].
112. Zwiener RJ, Ginsburg CM. 1988. Organophosphate and carbamate poisoning in infants and children. Pediatrics 81:121-126.