Alterations in gene expression in Caenorhabditis elegans associated with organophosphate pesticide intoxication and recovery

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Lewis, John A ^a   Gehman, Elizabeth A ^b   Baer, Christine E ^c   Jackson, David A ^a  

^a US Army Center for Environmental Health Research   (United States)

^b MITRE CORPORATION   (United States)

^c EXCET INC   (United States)

Author keywords

Acetylcholinesterase inhibition; Caenorhabditis elegans; Dichlorvos; Dichlorvos induced developmental delay; Gene expression; Mitochondrial disruption; Organophosphate pesticide intoxication

Indexed keywords

DICHLORVOS; GENOMIC RNA; ORGANOPHOSPHATE PESTICIDE; TRANSCRIPTION FACTOR DAF 16;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DAMAGE; CONTROLLED STUDY; ENERGY METABOLISM; GENE; GENE EXPRESSION; GENOME ANALYSIS; IMMUNE RESPONSE; INNATE IMMUNITY; INS 7 GENE; INTOXICATION; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; NONHUMAN; PESTICIDE RESISTANCE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEADY STATE; UPREGULATION; WORM;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DICHLORVOS; IMMUNITY, INNATE; MOVEMENT; MUSCLES; NERVOUS SYSTEM; PESTICIDES; STRESS, PHYSIOLOGICAL; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

CAENORHABDITIS ELEGANS;

EID: 84876802100     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-291     Document Type: Article

References (69)

1. Jeyaratnam J. Acute pesticide poisoning: a major global health problem. World Health Statatistics Quarterly 1990, 43(3):139-144.
2. Weinbroum AA. Pathophysiological and clinical aspects of combat anticholinesterase poisoning. Br Med Bull 2005, 72:119-133. 10.1093/bmb/ldh038, 15845747.
3. Brown MA, Brix KA. Review of health consequences from high-, intermediate- and low-level exposure to organophosphorus nerve agents. J Appl Toxicol 1998, 18(6):393-408. 10.1002/(SICI)1099-1263(199811/12)18:6<393::AID-JAT528>3.0.CO;2-0, 9840747.
4. Costa LG. Current issues in organophosphate toxicology. Clin Chim Acta 2006, 366(1-2):1-13.
5. Jokanovic M, Stukalov PV, Kosanovic M. Organophosphate induced delayed polyneuropathy. Curr Drug Targets CNS Neurol Disord 2002, 1(6):593-602. 10.2174/1568007023338879, 12769600.
6. Kamel F, Hoppin JA. Association of pesticide exposure with neurologic dysfunction and disease. Environ Health Perspect 2004, 112(9):950-958. 10.1289/ehp.7135, 1247187, 15198914.
7. Raveh L, Brandeis R, Gilat E, Cohen G, Alkalay D, Rabinovitz I, Sonego H, Weissman BA. Anticholinergic and antiglutamatergic agents protect against soman-induced brain damage and cognitive dysfunction. Toxicol Sci 2003, 75(1):108-116. 10.1093/toxsci/kfg166, 12832655.
8. Sarin S, Gill KD. Biochemical and behavioral deficits in adult rat following chronic dichlorvos exposure. Pharmacol Biochem Behav 1998, 59(4):1081-1086. 10.1016/S0091-3057(97)00517-0, 9586870.
9. Jamal GA, Hansen S, Julu PO. Low level exposures to organophosphorus esters may cause neurotoxicity. Toxicology 2002, 181-182:23-33.
10. Worek F, Koller M, Thiermann H, Szinicz L. Diagnostic aspects of organophosphate poisoning. Toxicology 2005, 214(3):182-189. 10.1016/j.tox.2005.06.012, 16051411.
11. Pope CN. Organophosphorus pesticides: do they all have the same mechanism of toxicity?. J Toxicol Environ Health B Crit Rev 1999, 2(2):161-181. 10.1080/109374099281205, 10230392.
12. Cole RD, Anderson GL, Williams PL. The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicol Appl Pharmacol 2004, 194(3):248-256. 10.1016/j.taap.2003.09.013, 14761681.
13. Combes D, Fedon Y, Toutant JP, Arpagaus M. Multiple ace genes encoding acetylcholinesterases of Caenorhabditis elegans have distinct tissue expression. Eur J Neurosci 2003, 18(3):497-512. 10.1046/j.1460-9568.2003.02749.x, 12911746.
14. Nguyen M, Alfonso A, Johnson CD, Rand JB. Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 1995, 140(2):527-535. 1206632, 7498734.
15. Glynn P. Neuropathy target esterase and phospholipid deacylation. Biochim Biophys Acta 2005, 1736(2):87-93. 10.1016/j.bbalip.2005.08.002, 16137924.
16. Glynn P. A mechanism for organophosphate-induced delayed neuropathy. Toxicol Lett 2006, 162(1):94-97. 10.1016/j.toxlet.2005.10.012, 16309859.
17. Lewis JA, Szilagyi M, Gehman E, Dennis WE, Jackson DA. Distinct patterns of gene and protein expression elicited by organophosphorus pesticides in Caenorhabditis elegans. BMCGenomics 2009, 10:202.
18. Agency for Toxic Substances and Disease Registry Toxicological Profile for Dichlorvos 1997, Atlanta, GA: U.S. Department of Health and Human Services, Agency for Toxic Substances and Disease Registry.
19. Lotti M, Moretto A. Organophosphate-induced delayed polyneuropathy. Toxicol Rev 2005, 24(1):37-49. 10.2165/00139709-200524010-00003, 16042503.
20. Opperman CH, Chang S. Effects of aldicarb and fenamiphos on acetycholinesterase and motility of caenorhabditis elegans. J Nematol 1991, 23(1):20-27. 2619128, 19283090.
21. Rand JB. Acetylcholine. WormBook : the online review of C elegans biology 2007, 1-21. : Wormbook, 10.1895/wormbook.1.131.1.
22. Mahoney TR, Luo S, Nonet ML. Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay. Nat Protoc 2006, 1(4):1772-1777. 10.1038/nprot.2006.281, 17487159.
23. DAVID Bioinformatics Resources [http://david.abcc.ncifcrf.gov].
24. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, Janette J, Chen C, Alves P, Preston E. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res 2011, 21(2):245-254. 10.1101/gr.114587.110, 3032928, 21177963.
25. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 2003, 424(6946):277-283. 10.1038/nature01789, 12845331.
26. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 1997, 389(6654):994-999. 10.1038/40194, 9353126.
27. Tissenbaum HA, Ruvkun G. An insulin-like signaling pathway affects both longevity and reproduction in Caenorhabditis elegans. Genetics 1998, 148(2):703-717. 1459840, 9504918.
28. Chan JY, Chan SH, Dai KY, Cheng HL, Chou JL, Chang AY. Cholinergic-receptor-independent dysfunction of mitochondrial respiratory chain enzymes, reduced mitochondrial transmembrane potential and ATP depletion underlie necrotic cell death induced by the organophosphate poison mevinphos. Neuropharmacology 2006, 51(7-8):1109-1119.
29. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 2007, 17(19):1646-1656. 10.1016/j.cub.2007.08.047, 2185793, 17900900.
30. Mair W, Morantte I, Rodrigues AP, Manning G, Montminy M, Shaw RJ, Dillin A. Lifespan extension induced by AMPK and calcineurin is mediated by CRTC-1 and CREB. Nature 2011, 470(7334):404-408. 10.1038/nature09706, 3098900, 21331044.
31. Koo SH, Flechner L, Qi L, Zhang X, Screaton RA, Jeffries S, Hedrick S, Xu W, Boussouar F, Brindle P. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 2005, 437(7062):1109-1111. 10.1038/nature03967, 16148943.
32. van der Linden AM, Nolan KM, Sengupta P. KIN-29 SIK regulates chemoreceptor gene expression via an MEF2 transcription factor and a class II HDAC. EMBO J 2007, 26(2):358-370. 10.1038/sj.emboj.7601479, 1783467, 17170704.
33. Lanjuin A, Sengupta P. Regulation of chemosensory receptor expression and sensory signaling by the KIN-29 Ser/Thr kinase. Neuron 2002, 33(3):369-381. 10.1016/S0896-6273(02)00572-X, 11832225.
34. Kwon ES, Narasimhan SD, Yen K, Tissenbaum HA. A new DAF-16 isoform regulates longevity. Nature 2010, 466(7305):498-502. 10.1038/nature09184, 3109862, 20613724.
35. Jadhav KB, Rajini PS. Evaluation of sublethal effects of dichlorvos upon Caenorhabditis elegans based on a set of end points of toxicity. J Biochem Mol Toxicol 2009, 23(1):9-17. 10.1002/jbt.20258, 19202558.
36. Schulenburg H, Hoeppner MP, Weiner J, Bornberg-Bauer E. Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans. Immunobiology 2008, 213(3-4):237-250.
37. Pujol N, Zugasti O, Wong D, Couillault C, Kurz CL, Schulenburg H, Ewbank JJ. Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 2008, 4(7):e1000105. 10.1371/journal.ppat.1000105, 2453101, 18636113.
38. Styer KL, Singh V, Macosko E, Steele SE, Bargmann CI, Aballay A. Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 2008, 322(5900):460-464. 10.1126/science.1163673, 2831475, 18801967.
39. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2006, 2(11):e183. 10.1371/journal.pgen.0020183, 1635533, 17096597.
40. Mizuno T, Hisamoto N, Terada T, Kondo T, Adachi M, Nishida E, Kim DH, Ausubel FM, Matsumoto K. The Caenorhabditis elegans MAPK phosphatase VHP-1 mediates a novel JNK-like signaling pathway in stress response. EMBO J 2004, 23(11):2226-2234. 10.1038/sj.emboj.7600226, 419906, 15116070.
41. Lee K, Shim J, Bae J, Kim YJ, Lee J. Stabilization of RNT-1 protein, runt-related transcription factor (RUNX) protein homolog of Caenorhabditis elegans, by oxidative stress through mitogen-activated protein kinase pathway. J Biol Chem 2012, 287(13):10444-10452. 10.1074/jbc.M111.314146, 3323012, 22308034.
42. Nix P, Hisamoto N, Matsumoto K, Bastiani M. Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. Proc Natl Acad Sci USA 2011, 108(26):10738-10743. 10.1073/pnas.1104830108, 3127873, 21670305.
43. Evans EA, Kawli T, Tan MW. Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans. PLoS Pathog 2008, 4(10):e1000175. 10.1371/journal.ppat.1000175, 2568960, 18927620.
44. Irazoqui JE, Urbach JM, Ausubel FM. Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 2010, 10(1):47-58. 10.1038/nri2689, 2965059, 20029447.
45. Coolon JD, Jones KL, Todd TC, Carr BC, Herman MA. Caenorhabditis elegans genomic response to soil bacteria predicts environment-specific genetic effects on life history traits. PLoS Genet 2009, 5(6):e1000503. 10.1371/journal.pgen.1000503, 2684633, 19503598.
46. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010, 464(7285):104-107. 10.1038/nature08780, 2843437, 20203610.
47. Aballay A. Neural regulation of immunity: role of NPR-1 in pathogen avoidance and regulation of innate immunity. Cell Cycle 2009, 8(7):966-969. 10.4161/cc.8.7.8074, 2838187, 19270528.
48. Karalliedde L, Baker D, Marrs TC. Organophosphate-induced intermediate syndrome: aetiology and relationships with myopathy. Toxicol Rev 2006, 25(1):1-14. 10.2165/00139709-200625010-00001, 16856766.
49. Lotti M. The pathogenesis of organophosphate polyneuropathy. Crit Rev Toxicol 1991, 21(6):465-487.
50. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M. Axon regeneration requires a conserved MAP kinase pathway. Science 2009, 323(5915):802-806. 10.1126/science.1165527, 2729122, 19164707.
51. Morita K, Chow KL, Ueno N. Regulation of body length and male tail ray pattern formation of Caenorhabditis elegans by a member of TGF-beta family. Development 1999, 126(6):1337-1347.
52. Sagasti A, Hisamoto N, Hyodo J, Tanaka-Hino M, Matsumoto K, Bargmann CI. The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 2001, 105(2):221-232. 10.1016/S0092-8674(01)00313-0, 11336672.
53. Tanaka-Hino M, Sagasti A, Hisamoto N, Kawasaki M, Nakano S, Ninomiya-Tsuji J, Bargmann CI, Matsumoto K. SEK-1 MAPKK mediates Ca2+ signaling to determine neuronal asymmetric development in Caenorhabditis elegans. EMBO Rep 2002, 3(1):56-62. 10.1093/embo-reports/kvf001, 1083920, 11751572.
54. Masoud A, Kiran R, Sandhir R. Impaired mitochondrial functions in organophosphate induced delayed neuropathy in rats. Cell Mol Neurobiol 2009, 29(8):1245-1255. 10.1007/s10571-009-9420-4, 19517227.
55. Rohlfing AK, Miteva Y, Hannenhalli S, Lamitina T. Genetic and physiological activation of osmosensitive gene expression mimics transcriptional signatures of pathogen infection in C. elegans. PLoS One 2010, 5(2):e9010. 10.1371/journal.pone.0009010, 2814864, 20126308.
56. Welker NC, Habig JW, Bass BL. Genes misregulated in C. elegans deficient in Dicer, RDE-4, or RDE-1 are enriched for innate immunity genes. RNA 2007, 13(7):1090-1102. 10.1261/rna.542107, 1894926, 17526642.
57. Park SK, Tedesco PM, Johnson TE. Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 2009, 8(3):258-269. 10.1111/j.1474-9726.2009.00473.x, 2762118, 19627265.
58. Castello PR, Drechsel DA, Patel M. Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J Biol Chem 2007, 282(19):14186-14193. 10.1074/jbc.M700827200, 3088512, 17389593.
59. Ruaud AF, Bessereau JL. Activation of nicotinic receptors uncouples a developmental timer from the molting timer in C. elegans. Development 2006, 133(11):2211-2222. 10.1242/dev.02392, 16672334.
60. Gupta RC, Goad JT, Kadel WL. Cholinergic and noncholinergic changes in skeletal muscles by carbofuran and methyl parathion. J Toxicol Environ Health 1994, 43(3):291-304. 10.1080/15287399409531922, 7966439.
61. You YJ, Kim J, Cobb M, Avery L. Starvation activates MAP kinase through the muscarinic acetylcholine pathway in Caenorhabditis elegans pharynx. Cell Metab 2006, 3(4):237-245. 10.1016/j.cmet.2006.02.012, 3433278, 16581001.
62. Raheja G, Gill KD. Calcium homeostasis and dichlorvos induced neurotoxicity in rat brain. Mol Cell Biochem 2002, 232(1-2):13-18.
63. Szilagyi M, Gehman E, Lapenotiere H, Lewis J, Clegg E, Jackson DA. Global Alterations in Gene Expression During Organophosphate Pesticide Intoxication and Recovery: Interim Report 2006, Ft. Belvoir, VA: DTIC (Defense Technical Information Center).
64. Hope IA. C. elegans A Practical Approach 1999, Oxford: Oxford University Press.
65. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics (Oxford, England) 2003, 4(2):249-264.
66. GEO Gene Expression Omnibus [http://www.ncbi.nlm.nih.gov/geo/], GEO.
67. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B - Methodological 1995, 57(1):289-300.
68. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4(5):P3-P3. 10.1186/gb-2003-4-5-p3, 12734009.
69. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.