NEUROPHYSIOLOGICAL AND BEHAVIOURAL PERTURBATIONS IN Caenorhabditis elegans EXPOSED TO ORGANOPHOSPHATE PESTICIDES

Rajul  Jain; Priyanka  Gautam

doi:10.18006/2021.9(3).343.352

Authors

Rajul Jain Bioinformatics Laboratory, Department of Zoology, Dayalbagh Educational Institute (Deemed University), Dayalbagh Agra-282005, India. https://orcid.org/0000-0001-9325-6635
Priyanka Gautam Bioinformatics Laboratory, Department of Zoology, Dayalbagh Educational Institute (Deemed University), Dayalbagh Agra-282005, India.

DOI:

https://doi.org/10.18006/2021.9(3).343.352

Keywords:

Organophosphate, Behavioural toxicity, Developmental toxicity, Neurodegeneration, Caenorhabditis elegans

Abstract

The ubiquitous use of pesticides all over the world leads to adverse effects on both targets as well as non-target species. The extensive and uncontrolled use of organophosphates (OPs), a large group of pesticidal compounds in agricultural and household products are resulting in high exposure to humans. This research has been carried out to study the adverse effect of OPs i.e., chlorpyrifos, trichlorfon, and disulfoton on model organism Caenorhabditis elegans to evaluate their behavioural as well as developmental toxicity at different time intervals i.e., 4, 24, 48, and 72 hours (hrs) of exposure. A significant difference was observed in all the behavioural endpoints like locomotion, egg-laying, offspring count, and learning along with developmental parameters like mortality, paralysis, and growth rendering from moderate to high toxic effects. Based on the above screening, trichlorfon resulted in glutamatergic and cholinergic neurodegeneration along with elevated autofluorescence. Loss in Yellow fluorescent Protein (YFP) and Green Fluorescent Protein (GFP) was recorded by 57.96% and 30.52% using transgenic strains OH11124 (otIs388 [eat-4(fosmid)::SL2::YFP::H2B + (pBX)pha-1(+)] III) and OH13083 (otIs576 [unc-17(fosmid)::GFP + lin-44::YFP]). These results have shown the biological potency of toxicants in C. elegans and pave the way forward to provide insight into various neurogenerative diseases in humans.

References

C. elegans N2 strain used in this study was kindly provided by the Caenorhabditis Genetics Center (CGC), MN, USA. This work was funded by DST- SERB [EEQ/2016/000590].

Conflict of interest

The authors declare that they have no conflicts of interest.

Reference

Abdelhack M (2016) Dopaminergic neurons modulate locomotion in Caenorhabditis elegans. bioRxiv 056192.

Alexander AG, Marfil V, Li C (2014) Use of Caenorhabditis elegans as a model to study Alzheimer’s disease and other neurodegenerative diseases. Frontiers in genetics 5:1–21. https://doi.org/10.3389/fgene.2014.00279.

Bany IA, Dong MQ, Koelle MR (2003) Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior. Journal of Neuroscience 23:8060–8069. https://doi.org/10.1523/jneurosci.23-22-08060.2003.

Bradford BR, Whidden E, Gervasio ED, Checchi PM, Raley-Susman KM (2020) Neonicotinoid-containing insecticide disruption of growth, locomotion, and fertility in Caenorhabditis elegans. PLoS ONE 15:1–21. https://doi.org/10.1371/journal.pone.0238637.

Brockie P (2006) Ionotropic glutamate receptors: genetics, behavior and electrophysiology. WormBook 1–16. https://doi.org/10.1895/wormbook.1.61.1.

Caldwell KA, Willicott CW, Caldwell GA (2020) Modeling neurodegeneration in Caenorhabditis elegans. Disease Models & Mechanisms 13. https://doi.org/10.1242/dmm.046110.

Chen P, Martinez-Finley EJ, Bornhorst J, Chakraborty S, Aschner M (2013) Metal-induced neurodegeneration in C . elegans. Frontiers in Aging Neuroscience 5:1–11. https://doi.org/10.3389/fnagi.2013.00018.

Chen X, Barclay JW, Burgoyne RD, Morgan A (2015) therapeutic compounds for ageing ‑ associated neurodegenerative diseases. Chemistry Central Journal 1–20. https://doi.org/10.1186/s13065-015-0143-y.

Cole RD, Anderson GL, Williams PL (2004) The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicology and Applied Pharmacology 194:248–256. https://doi.org/10.1016/j.taap.2003.09.013.

Francis PT, Palmer AM, Snape M, Wilcock GK (1999) The cholinergic hypothesis of Alzheimer’s disease : a review of progress. Neurol Neurosurg Psychiatry 66:137–147.

Hargreaves AJ (2012) Neurodegenerations induced by organophosphorous compounds. Advances in Experimental Medicine and Biology 724:189–204. https://doi.org/10.1007/978-1-4614-0653-2_15.

Harlow PH, Perry SJ, Widdison S, Daniels S, Bondo E, Lamberth C, Currie RA, Flemming AJ (2016) The nematode Caenorhabditis elegans as a tool to predict chemical activity on mammalian development and identify mechanisms influencing toxicological outcome. Scientific reports 6:1–13. https://doi.org/10.1038/ srep22965.

Jadhav KB, Rajini PS (2009a) Neurophysiological alterations in Caenorhabditis elegans exposed to dichlorvos, an organophosphorus insecticide. Pesticide Biochemistry and Physiology 94:79–85. https://doi.org/10.1016/j.pestbp.2009.03.004.

Jadhav KB, Rajini PS (2009b) Evaluation of sublethal effects of dichlorvos upon Caenorhabditis elegans based on a set of end points of toxicity. Pesticide Biochemistry and Physiology 23:9–17. https://doi.org/10.1002/jbt.20258.

Jain S, van Kesteren RE, Heutink P (2012) High Content Screening in Neurodegenerative Diseases. Journal of Visualized Experiments 1–9. https://doi.org/10.3791/3452.

John H, Richter A, Siegert M, Eyer F, Thiermann H (2021) Evidence of exposure to organophosphorus toxicants by detection of the propionylated butyrylcholinesterase-derived nonapeptide-adduct as a novel biomarker. Forensic Science International 323:110818. https://doi.org/10.1016/j.forsciint.2021.110818.

Ju JJ, Ruan QL, Li YH, Liu R, Yin LH, Pu YP (2010) Neurotoxicity Evaluation of Chlorpyrifos Exposure with Caenorhabditis elegans. In 2010 4th International Conference on Bioinformatics and Biomedical Engineering (Pp 1-4) IEEE.

Leelaja BC, Rajini PS (2013) Biochemical and physiological responses in Caenorhabditis elegans exposed to sublethal concentrations of the organophosphorus insecticide, monocrotophos. Ecotoxicology and environmental safety 94:8–13. https://doi.org/10.1016/j.ecoenv.2013.04.015.

Lewis JA, Gehman EA, Baer CE, Jackson DA (2013) Alterations in gene expression in Caenorhabditis elegans associated with organophosphate pesticide intoxication and recovery. BMC Genomics 14(1):1:17.

Meyer-Baron M, Knapp G, Schäper M, van Thriel C (2015) Meta-analysis on occupational exposure to pesticides - Neurobehavioral impact and dose-response relationships. Environmental Research 136:234–245. https://doi.org/10.1016/j.envres.2014.09.030.

Meyer D, Williams PL (2014) Toxicity Testing of Neurotoxic Pesticides in Caenorhabditis elegans. Journal of Toxicology and Environmental Health, Part B 17:284–306. https://doi.org/10.1080/10937404.2014.933722.

Mille T, Quilgars C, Cazalets JR, Bertrand SS (2021) Acetylcholine and spinal locomotor networks: The insider. Physiological Reports 9:1–10. https://doi.org/10.14814/phy2.14736.

Monici M (2005) Cell and tissue autofluorescence research and diagnostic applications. Biotechnology Annual Review 11:227–256.https://doi.org/10.1016/S1387-2656(05)11007-2.

Muir JL (1997) Alzheimer ’ s Disease. Pharmacology Biochemistry and Behavior 56:687–696.

Mukherjee S, Gupta RD (2020) Organophosphorus Nerve Agents: Types, Toxicity, and Treatments. Journal of Toxicology. https://doi.org/10.1155/2020/3007984.

Muñoz-Quezada MT, Lucero BA, Iglesias VP, Muñoz MP, Cornejo CA, Achu E, Baumert B, Hanchey A, Concha C, Brito AM, Villalobos M (2016) Chronic exposure to organophosphate (OP) pesticides and neuropsychological functioning in farm workers: a review. International Journal of Occupational and Environmental Health 22(1):68–79. https://doi.org/10.1080/10773525.2015.1123848.

Nonet ML, Saifee O, Zhao H, Rand JB, Wei L (1998) Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. Journal of Neuroscience 18:70–80. https://doi.org/10.1523/jneurosci.18-01-00070.1998.

Pereira L, Kratsios P, Serrano-Saiz E, Sheftel H, Mayo AE, Hall DH, White JG, LeBoeuf B, Garcia LR, Alon U, Hobert O (2015) A cellular and regulatory map of the cholinergic nervous system of C . elegans. Elife 4: e12432 1–46. https://doi.org/10.7554/eLife.12432.

Peris-Sampedro F, Basaure P, Reverte I, Cabré M, Domingo JL, Colomina MT (2015) Chronic exposure to chlorpyrifos triggered body weight increase and memory impairment depending on human apoE polymorphisms in a targeted replacement mouse model. Physiology and Behavior 144:37–45. https://doi.org/10.1016/j.physbeh.2015.03.006.

Pincus Z, Mazer TC, Slack FJ (2016) Autofluorescence as a measure of senescence in C. elegans: Look to red, not blue or green. Aging 8:889–898. https://doi.org/10.18632/aging.100936.

Queirós L, Pereira JL, Gonçalves FJ, Pacheco M, Aschner M, Pereira P (2019) Caenorhabditis elegans as a tool for Environmental Risk Assessment – emerging and promising applications for a “nobelized worm.” Physiology & Behavior 176:139–148. https://doi.org/10.1080/10408444.2019.1626801.Caenorhabditis.

Rajini PS, Melstrom P, Williams PL (2008) A comparative study on the relationship between various toxicological endpoints in Caenorhabditis elegans exposed to organophosphorus insecticides. Journal of Toxicology and Environmental Health - Part A 71:1043–1050. https://doi.org/10.1080/15287390801989002.

Rand J (2007) Acetylcholine. WormBook 1–21. https://doi.org/ 10.1895/wormbook.1.131.1.

Reynoso EC, Torres E, Bettazzi F, Palchetti I (2019) Trends and perspectives in immunosensors for determination of currently-used pesticides: The case of glyphosate, organophosphates, and neonicotinoids. Biosensors 9:. https://doi.org/10.3390/bios9010020.

Roh JY, Choi J (2011) Cyp35a2 gene expression is involved in toxicity of fenitrothion in the soil nematode Caenorhabditis elegans. Chemosphere 84:1356–1361. https://doi.org/10.1016/ j.chemosphere.2011.05.010.

Roldan-Tapia L, Nieto-Escamez FA, del Aguila EM, Laynez F, Parron T, Sanchez-Santed F (2006) Neuropsychological sequelae from acute poisoning and long-term exposure to carbamate and organophosphate pesticides. Neurotoxicology and Teratology 28(6):94–703. https://doi.org/10.1016/j.ntt.2006.07.004.

Ruszkiewicz JA, Pinkas A, Miah MR, Weitz RL, Lawes MJ, Akinyemi AJ, Ijomone OM, Aschner M (2018) C . elegans as a model in developmental neurotoxicology. Toxicology and Applied Pharmacology 354:126-135. https://doi.org/10.1016/j.taap. 2018.03.016.

Salim C, Rajini PS (2014) Glucose feeding during development aggravates the toxicity of the organophosphorus insecticide Monocrotophos in the nematode, Caenorhabditis elegans. Physiology and Behavior 131:142–148. https://doi.org/10.1016/ j.physbeh.2014.04.022.

Sánchez-Santed F, Colomina MT, Herrero Hernández E (2016) Organophosphate pesticide exposure and neurodegeneration. Cortex 74:417–426. https://doi.org/10.1016/j.cortex.2015.10.003.

Silveira da TL, Zamberlan DC, Arantes LP, Machado ML, da Silva TC, de Freitas Câmara D, Santamaría A, Aschner M, Soares FA (2018) Quinolinic Acid and glutamatergic neurodegeneration in Caenorhabditis elegans. Neurotoxicology 67:94–101. https://doi.org/10.1016/j.neuro.2018.04.015.

Stiernagle T (2006) Maintenance of C. elegans. WormBook 1–11. https://doi.org/10.1895/wormbook.1.101.1.

Tejeda L, Olivero-verbel J, Tejeda-benitez L, Olivero-verbel J (2016) Caenorhabditis elegans, a Biological Model for Research in Toxicology. Reviews of Environmental Contamination and Toxicology 237. https://doi.org/10.1007/978-3-319-23573-8.

Terry AV (2012) Functional consequences of repeated organophosphate exposure: Potential non-cholinergic mechanisms. Pharmacology and Therapeutics 134:355–365. https://doi.org/10.1016/j.pharmthera.2012.03.001.

Teuscher AC, Ewald CY (2018) Europe PMC Funders Group Overcoming Autofluorescence to Assess GFP Expression During Normal Physiology and Aging in Caenorhabditis elegans. Bio-protocol 8. https://doi.org/10.21769/BioProtoc.2940.Overcoming.

Walker DS, Chew YL, Schafer WR (2017) Oxford Handbooks Online Genetics of Behavior in C. elegans.

Wen X, Chen YH, Li R, Ge MH, Yin SW, Wu JJ, Huang JH, Liu H, Wang PZ, Gross E, Wu ZX (2020). Signal Decoding for Glutamate Modulating Egg Laying Oppositely in Caenorhabditis elegans under Varied Environmental Conditions. Iscience, 23(10), 101588. https://doi.org/10.1016/ j.isci.2020.101588.

Zhuang Z, Zhao Y, Wu Q, Li M, Liu H, Sun L, Gao W, Wang D (2014) Adverse effects from clenbuterol and ractopamine on nematode Caenorhabditis elegans and the underlying mechanism. PLoS ONE 9:1–11. https://doi.org/10.1371/journal.pone.0085482.